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Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 2969271, 18 pages
https://doi.org/10.1155/2017/2969271
Review Article

Unfolded Protein Response of the Endoplasmic Reticulum in Tumor Progression and Immunogenicity

1Department of Biochemistry, Chungnam National University School of Medicine, Daejeon 35015, Republic of Korea
2Department of Medical Science, Chungnam National University School of Medicine, Daejeon 35015, Republic of Korea

Correspondence should be addressed to Young Joo Jeon; rk.ca.unc@noejjy

Received 12 September 2017; Accepted 29 November 2017; Published 21 December 2017

Academic Editor: Dieter Wolf

Copyright © 2017 Yoon Seon Yoo et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. Griffiths, G. Warren, P. Quinn, O. Mathieu-Costello, and H. Hoppeler, “Density of newly synthesized plasma membrane proteins in intracellular membranes. I. Stereological studies,” Journal of Cell Biology, vol. 98, no. 6, pp. 2133–2141, 1984. View at Publisher · View at Google Scholar
  2. O. Baumann and B. Walz, “Endoplasmic reticulum of animal cells and its organization into structural and functional domains,” International Review of Cytology, vol. 205, pp. 149–214, 2001. View at Publisher · View at Google Scholar · View at Scopus
  3. D. T. Rutkowski and R. S. Hegde, “Regulation of basal cellular physiology by the homeostatic unfolded protein response,” The Journal of Cell Biology, vol. 189, no. 5, pp. 783–794, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. M. J. Berridge, P. Lipp, and M. D. Bootman, “The versatility and universality of calcium signalling,” Nature Reviews Molecular Cell Biology, vol. 1, no. 1, pp. 11–21, 2000. View at Publisher · View at Google Scholar
  5. S. A. Oakes and F. R. Papa, “The role of endoplasmic reticulum stress in human pathology,” Annual Review of Pathology: Mechanisms of Disease, vol. 10, no. 1, pp. 173–194, 2015. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Wang and R. J. Kaufman, “The impact of the endoplasmic reticulum protein-folding environment on cancer development,” Nature Reviews Cancer, vol. 14, no. 9, pp. 581–597, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. D. Morito and K. Nagata, “Pathogenic hijacking of ER-associated degradation: is ERAD flexible?” Molecular Cell, vol. 59, no. 3, pp. 335–344, 2015. View at Publisher · View at Google Scholar · View at Scopus
  8. F. U. Hartl and M. Hayer-Hartl, “Converging concepts of protein folding in vitro and in vivo,” Nature Structural & Molecular Biology, vol. 16, no. 6, pp. 574–581, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Ruggiano, O. Foresti, and P. Carvalho, “Quality control: ER-associated degradation: protein quality control and beyond,” Journal of Cell Biology, vol. 204, no. 6, pp. 869–879, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. J. L. Brodsky and R. J. Wojcikiewicz, “Substrate-specific mediators of ER associated degradation (ERAD),” Current Opinion in Cell Biology, vol. 21, no. 4, pp. 516–521, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. R. Y. Hampton, “ER-associated degradation in protein quality control and cellular regulation,” Current Opinion in Cell Biology, vol. 14, no. 4, pp. 476–482, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. S. S. Vembar and J. L. Brodsky, “One step at a time: endoplasmic reticulum-associated degradation,” Nature Reviews Molecular Cell Biology, vol. 9, no. 12, pp. 944–957, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Hershko and A. Ciechanover, “The ubiquitin system,” Annual Review of Biochemistry, vol. 67, no. 1, pp. 425–479, 1998. View at Publisher · View at Google Scholar · View at Scopus
  14. C. Lopez-Otin, M. A. Blasco, L. Partridge, M. Serrano, and G. Kroemer, “The hallmarks of aging,” Cell, vol. 153, no. 6, pp. 1194–1217, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. R. C. Taylor and A. Dillin, “Aging as an event of proteostasis collapse,” Cold Spring Harbor Perspectives in Biology, vol. 3, no. 5, pp. 1–17, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. F. Chiti and C. M. Dobson, “Protein misfolding, functional amyloid, and human disease,” Annual Review of Biochemistry, vol. 75, no. 1, pp. 333–366, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Wang and R. J. Kaufman, “Protein misfolding in the endoplasmic reticulum as a conduit to human disease,” Nature, vol. 529, no. 7586, pp. 326–335, 2016. View at Publisher · View at Google Scholar · View at Scopus
  18. T. K. Rainbolt, J. M. Saunders, and R. L. Wiseman, “Stress-responsive regulation of mitochondria through the ER unfolded protein response,” Trends in Endocrinology & Metabolism, vol. 25, no. 10, pp. 528–537, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. N. Hiramatsu, W. C. Chiang, T. D. Kurt, C. J. Sigurdson, and J. H. Lin, “Multiple mechanisms of unfolded protein response-induced cell death,” The American Journal of Pathology, vol. 185, no. 7, pp. 1800–1808, 2015. View at Publisher · View at Google Scholar · View at Scopus
  20. J. H. Otero, B. Lizak, and L. M. Hendershot, “Life and death of a BiP substrate,” Seminars in Cell & Developmental Biology, vol. 21, no. 5, pp. 472–478, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Bertolotti, Y. Zhang, L. M. Hendershot, H. P. Harding, and D. Ron, “Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response,” Nature Cell Biology, vol. 2, no. 6, pp. 326–332, 2000. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Shen, E. L. Snapp, J. Lippincott-Schwartz, and R. Prywes, “Stable binding of ATF6 to BiP in the endoplasmic reticulum stress response,” Molecular and Cellular Biology, vol. 25, no. 3, pp. 921–932, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. D. Pincus, M. W. Chevalier, T. Aragon et al., “BiP binding to the ER-stress sensor Ire1 tunes the homeostatic behavior of the unfolded protein response,” PLoS Biology, vol. 8, no. 7, article e1000415, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. B. M. Gardner and P. Walter, “Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response,” Science, vol. 333, no. 6051, pp. 1891–1894, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. A. V. Korennykh, P. F. Egea, A. A. Korostelev et al., “The unfolded protein response signals through high-order assembly of Ire1,” Nature, vol. 457, no. 7230, pp. 687–693, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Li, A. V. Korennykh, S. L. Behrman, and P. Walter, “Mammalian endoplasmic reticulum stress sensor IRE1 signals by dynamic clustering,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 37, pp. 16113–16118, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. P. Walter and D. Ron, “The unfolded protein response: from stress pathway to homeostatic regulation,” Science, vol. 334, no. 6059, pp. 1081–1086, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. D. Ron and P. Walter, “Signal integration in the endoplasmic reticulum unfolded protein response,” Nature Reviews Molecular Cell Biology, vol. 8, no. 7, pp. 519–529, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. G. V. Di Prisco, W. Huang, S. A. Buffington et al., “Translational control of mGluR-dependent long-term depression and object-place learning by eIF2α,” Nature Neuroscience, vol. 17, no. 8, pp. 1073–1082, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Han, S. H. Back, J. Hur et al., “ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death,” Nature Cell Biology, vol. 15, no. 5, pp. 481–490, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. H. P. Harding, Y. Zhang, D. Scheuner, J. J. Chen, R. J. Kaufman, and D. Ron, “Ppp1r15 gene knockout reveals an essential role for translation initiation factor 2 alpha (eIF2α) dephosphorylation in mammalian development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 6, pp. 1832–1837, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. D. T. Rutkowski, S. M. Arnold, C. N. Miller et al., “Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins,” PLoS Biology, vol. 4, no. 11, article e374, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. J. H. Lin, H. Li, D. Yasumura et al., “IRE1 signaling affects cell fate during the unfolded protein response,” Science, vol. 318, no. 5852, pp. 944–949, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. H. P. Harding, Y. Zhang, and D. Ron, “Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase,” Nature, vol. 397, no. 6716, pp. 271–274, 1999. View at Publisher · View at Google Scholar · View at Scopus
  35. K. M. Vattem and R. C. Wek, “Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 31, pp. 11269–11274, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. H. P. Harding, Y. Zhang, H. Zeng et al., “An integrated stress response regulates amino acid metabolism and resistance to oxidative stress,” Molecular Cell, vol. 11, no. 3, pp. 619–633, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. S. J. Marciniak, C. Y. Yun, S. Oyadomari et al., “CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum,” Genes & Development, vol. 18, no. 24, pp. 3066–3077, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. B. Song, D. Scheuner, D. Ron, S. Pennathur, and R. J. Kaufman, “Chop deletion reduces oxidative stress, improves β cell function, and promotes cell survival in multiple mouse models of diabetes,” The Journal of Clinical Investigation, vol. 118, no. 10, pp. 3378–3389, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. N. S. Chitnis, D. Pytel, E. Bobrovnikova-Marjon et al., “miR-211 is a prosurvival microRNA that regulates chop expression in a PERK-dependent manner,” Molecular Cell, vol. 48, no. 3, pp. 353–364, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. C. W. Woo, L. Kutzler, S. R. Kimball, and I. Tabas, “Toll-like receptor activation suppresses ER stress factor CHOP and translation inhibition through activation of eIF2B,” Nature Cell Biology, vol. 14, no. 2, pp. 192–200, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. W. Tirasophon, A. A. Welihinda, and R. J. Kaufman, “A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells,” Genes & Development, vol. 12, no. 12, pp. 1812–1824, 1998. View at Publisher · View at Google Scholar
  42. H. Yoshida, T. Matsui, A. Yamamoto, T. Okada, and K. Mori, “XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor,” Cell, vol. 107, no. 7, pp. 881–891, 2001. View at Publisher · View at Google Scholar · View at Scopus
  43. A. H. Lee, N. N. Iwakoshi, and L. H. Glimcher, “XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response,” Molecular and Cellular Biology, vol. 23, no. 21, pp. 7448–7459, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. J. R. Hassler, D. L. Scheuner, S. Wang et al., “The IRE1α/XBP1s pathway is essential for the glucose response and protection of β cells,” PLoS Biology, vol. 13, no. 10, article e1002277, 2015. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Calfon, H. Zeng, F. Urano et al., “IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA,” Nature, vol. 415, no. 6867, pp. 92–96, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. H. Yoshida, M. Oku, M. Suzuki, and K. Mori, “pXBP1(U) encoded in XBP1 pre-mRNA negatively regulates unfolded protein response activator pXBP1(S) in mammalian ER stress response,” Journal of Cell Biology, vol. 172, no. 4, pp. 565–575, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. R. Ghosh, L. Wang, E. S. Wang et al., “Allosteric inhibition of the IRE1α RNase preserves cell viability and function during endoplasmic reticulum stress,” Cell, vol. 158, no. 3, pp. 534–548, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. A. G. Lerner, J. P. Upton, P. V. Praveen et al., “IRE1α induces thioredoxin-interacting protein to activate the NLRP3 inflammasome and promote programmed cell death under irremediable ER stress,” Cell Metabolism, vol. 16, no. 2, pp. 250–264, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. J. P. Upton, L. Wang, D. Han et al., “IRE1α cleaves select microRNAs during ER stress to derepress translation of proapoptotic caspase-2,” Science, vol. 338, no. 6108, pp. 818–822, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. K. Haze, H. Yoshida, H. Yanagi, T. Yura, and K. Mori, “Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress,” Molecular Biology of the Cell, vol. 10, no. 11, pp. 3787–3799, 1999. View at Publisher · View at Google Scholar
  51. K. Lee, W. Tirasophon, X. Shen et al., “IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response,” Genes & Development, vol. 16, no. 4, pp. 452–466, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. K. Yamamoto, T. Sato, T. Matsui et al., “Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6α and XBP1,” Developmental Cell, vol. 13, no. 3, pp. 365–376, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. M. D. Shoulders, L. M. Ryno, J. C. Genereux et al., “Stress-independent activation of XBP1s and/or ATF6 reveals three functionally diverse ER proteostasis environments,” Cell Reports, vol. 3, no. 4, pp. 1279–1292, 2013. View at Publisher · View at Google Scholar · View at Scopus
  54. K. E. Matlack, W. Mothes, and T. A. Rapoport, “Protein translocation: tunnel vision,” Cell, vol. 92, no. 3, pp. 381–390, 1998. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Helenius, T. Marquardt, and I. Braakman, “The endoplasmic reticulum as a protein-folding compartment,” Trends in Cell Biology, vol. 2, no. 8, pp. 227–231, 1992. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Helenius, E. S. Trombetta, D. N. Hebert, and J. F. Simons, “Calnexin, calreticulin and the folding of glycoproteins,” Trends in Cell Biology, vol. 7, no. 5, pp. 193–200, 1997. View at Publisher · View at Google Scholar · View at Scopus
  57. L. Ellgaard, M. Molinari, and A. Helenius, “Setting the standards: quality control in the secretory pathway,” Science, vol. 286, no. 5446, pp. 1882–1888, 1999. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Zapun, C. A. Jakob, D. Y. Thomas, and J. J. Bergeron, “Protein folding in a specialized compartment: the endoplasmic reticulum,” Structure, vol. 7, no. 8, pp. R173–R182, 1999. View at Publisher · View at Google Scholar · View at Scopus
  59. C. S. Sevier and C. A. Kaiser, “Formation and transfer of disulphide bonds in living cells,” Nature Reviews Molecular Cell Biology, vol. 3, no. 11, pp. 836–847, 2002. View at Publisher · View at Google Scholar · View at Scopus
  60. B. P. Tu and J. S. Weissman, “Oxidative protein folding in eukaryotes: mechanisms and consequences,” Journal of Cell Biology, vol. 164, no. 3, pp. 341–346, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. H. Saibil, “Chaperone machines for protein folding, unfolding and disaggregation,” Nature Reviews Molecular Cell Biology, vol. 14, no. 10, pp. 630–642, 2013. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Schroder and R. J. Kaufman, “The mammalian unfolded protein response,” Annual Review of Biochemistry, vol. 74, no. 1, pp. 739–789, 2005. View at Publisher · View at Google Scholar · View at Scopus
  63. J. C. Christianson and Y. Ye, “Cleaning up in the endoplasmic reticulum: ubiquitin in charge,” Nature Structural & Molecular Biology, vol. 21, no. 4, pp. 325–335, 2014. View at Publisher · View at Google Scholar · View at Scopus
  64. J. A. Olzmann, R. R. Kopito, and J. C. Christianson, “The mammalian endoplasmic reticulum-associated degradation system,” Cold Spring Harbor Perspectives in Biology, vol. 5, no. 9, pp. 1–16, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. C. Xu and D. T. Ng, “Glycosylation-directed quality control of protein folding,” Nature Reviews Molecular Cell Biology, vol. 16, no. 12, pp. 742–752, 2015. View at Publisher · View at Google Scholar · View at Scopus
  66. E. J. Wiertz, T. R. Jones, L. Sun, M. Bogyo, H. J. Geuze, and H. L. Ploegh, “The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol,” Cell, vol. 84, no. 5, pp. 769–779, 1996. View at Publisher · View at Google Scholar · View at Scopus
  67. K. Fujita, S. Omura, and J. Silver, “Rapid degradation of CD4 in cells expressing human immunodeficiency virus type 1 Env and Vpu is blocked by proteasome inhibitors,” Journal of General Virology, vol. 78, no. 3, pp. 619–625, 1997. View at Publisher · View at Google Scholar
  68. U. Schubert, L. C. Anton, I. Bacik et al., “CD4 glycoprotein degradation induced by human immunodeficiency virus type 1 Vpu protein requires the function of proteasomes and the ubiquitin-conjugating pathway,” Journal of Virology, vol. 72, no. 3, pp. 2280–2288, 1998. View at Google Scholar
  69. N. Yagishita, K. Ohneda, T. Amano et al., “Essential role of synoviolin in embryogenesis,” Journal of Biological Chemistry, vol. 280, no. 9, pp. 7909–7916, 2005. View at Publisher · View at Google Scholar · View at Scopus
  70. A. B. Francisco, R. Singh, S. Li et al., “Deficiency of suppressor enhancer Lin12 1 like (SEL1L) in mice leads to systemic endoplasmic reticulum stress and embryonic lethality,” Journal of Biological Chemistry, vol. 285, no. 18, pp. 13694–13703, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. Y. Eura, H. Yanamoto, Y. Arai, T. Okuda, T. Miyata, and K. Kokame, “Derlin-1 deficiency is embryonic lethal, Derlin-3 deficiency appears normal, and Herp deficiency is intolerant to glucose load and ischemia in mice,” PLoS One, vol. 7, no. 3, article e34298, 2012. View at Publisher · View at Google Scholar · View at Scopus
  72. C. J. Guerriero and J. L. Brodsky, “The delicate balance between secreted protein folding and endoplasmic reticulum-associated degradation in human physiology,” Physiological Reviews, vol. 92, no. 2, pp. 537–576, 2012. View at Publisher · View at Google Scholar · View at Scopus
  73. A. Helenius and M. Aebi, “Roles of N-linked glycans in the endoplasmic reticulum,” Annual Review of Biochemistry, vol. 73, no. 1, pp. 1019–1049, 2004. View at Publisher · View at Google Scholar · View at Scopus
  74. M. Aebi, R. Bernasconi, S. Clerc, and M. Molinari, “N-glycan structures: recognition and processing in the ER,” Trends in Biochemical Sciences, vol. 35, no. 2, pp. 74–82, 2010. View at Publisher · View at Google Scholar · View at Scopus
  75. D. N. Hebert, R. Bernasconi, and M. Molinari, “ERAD substrates: which way out?” Seminars in Cell & Developmental Biology, vol. 21, no. 5, pp. 526–532, 2010. View at Publisher · View at Google Scholar · View at Scopus
  76. G. Z. Lederkremer, “Glycoprotein folding, quality control and ER-associated degradation,” Current Opinion in Structural Biology, vol. 19, no. 5, pp. 515–523, 2009. View at Publisher · View at Google Scholar · View at Scopus
  77. D. S. Gonzalez, K. Karaveg, A. S. Vandersall-Nairn, A. Lal, and K. W. Moremen, “Identification, expression, and characterization of a cDNA encoding human endoplasmic reticulum mannosidase I, the enzyme that catalyzes the first mannose trimming step in mammalian Asn-linked oligosaccharide biosynthesis,” Journal of Biological Chemistry, vol. 274, no. 30, pp. 21375–21386, 1999. View at Publisher · View at Google Scholar · View at Scopus
  78. L. O. Tremblay and A. Herscovics, “Cloning and expression of a specific human alpha 1,2-mannosidase that trims Man9GlcNAc2 to Man8GlcNAc2 isomer B during N-glycan biosynthesis,” Glycobiology, vol. 9, no. 10, pp. 1073–1078, 1999. View at Publisher · View at Google Scholar · View at Scopus
  79. S. Olivari, T. Cali, K. E. Salo, P. Paganetti, L. W. Ruddock, and M. Molinari, “EDEM1 regulates ER-associated degradation by accelerating de-mannosylation of folding-defective polypeptides and by inhibiting their covalent aggregation,” Biochemical and Biophysical Research Communications, vol. 349, no. 4, pp. 1278–1284, 2006. View at Publisher · View at Google Scholar · View at Scopus
  80. N. Hosokawa, L. O. Tremblay, B. Sleno et al., “EDEM1 accelerates the trimming of alpha1,2-linked mannose on the C branch of N-glycans,” Glycobiology, vol. 20, no. 5, pp. 567–575, 2010. View at Publisher · View at Google Scholar · View at Scopus
  81. K. Hirao, Y. Natsuka, T. Tamura et al., “EDEM3, a soluble EDEM homolog, enhances glycoprotein endoplasmic reticulum-associated degradation and mannose trimming,” Journal of Biological Chemistry, vol. 281, no. 14, pp. 9650–9658, 2006. View at Publisher · View at Google Scholar · View at Scopus
  82. N. Hosokawa, Y. Kamiya, D. Kamiya, K. Kato, and K. Nagata, “Human OS-9, a lectin required for glycoprotein endoplasmic reticulum-associated degradation, recognizes mannose-trimmed N-glycans,” Journal of Biological Chemistry, vol. 284, no. 25, pp. 17061–17068, 2009. View at Publisher · View at Google Scholar · View at Scopus
  83. N. Hosokawa, Z. You, L. O. Tremblay, K. Nagata, and A. Herscovics, “Stimulation of ERAD of misfolded null Hong Kong α1-antitrypsin by Golgi α1,2-mannosidases,” Biochemical and Biophysical Research Communications, vol. 362, no. 3, pp. 626–632, 2007. View at Publisher · View at Google Scholar · View at Scopus
  84. R. Bernasconi, T. Pertel, J. Luban, and M. Molinari, “A dual task for the Xbp1-responsive OS-9 variants in the mammalian endoplasmic reticulum: inhibiting secretion of misfolded protein conformers and enhancing their disposal,” Journal of Biological Chemistry, vol. 283, no. 24, pp. 16446–16454, 2008. View at Publisher · View at Google Scholar · View at Scopus
  85. J. C. Christianson, T. A. Shaler, R. E. Tyler, and R. R. Kopito, “OS-9 and GRP94 deliver mutant α1-antitrypsin to the Hrd1-SEL1L ubiquitin ligase complex for ERAD,” Nature Cell Biology, vol. 10, no. 3, pp. 272–282, 2008. View at Publisher · View at Google Scholar · View at Scopus
  86. N. Hosokawa, I. Wada, K. Nagasawa, T. Moriyama, K. Okawa, and K. Nagata, “Human XTP3-B forms an endoplasmic reticulum quality control scaffold with the HRD1-SEL1L ubiquitin ligase complex and BiP,” Journal of Biological Chemistry, vol. 283, no. 30, pp. 20914–20924, 2008. View at Publisher · View at Google Scholar · View at Scopus
  87. R. Bernasconi, C. Galli, V. Calanca, T. Nakajima, and M. Molinari, “Stringent requirement for HRD1, SEL1L, and OS-9/XTP3-B for disposal of ERAD-LS substrates,” Journal of Cell Biology, vol. 188, no. 2, pp. 223–235, 2010. View at Publisher · View at Google Scholar · View at Scopus
  88. R. K. Plemper, S. Bohmler, J. Bordallo, T. Sommer, and D. H. Wolf, “Mutant analysis links the translocon and BiP to retrograde protein transport for ER degradation,” Nature, vol. 388, no. 6645, pp. 891–895, 1997. View at Publisher · View at Google Scholar · View at Scopus
  89. R. Ushioda, J. Hoseki, and K. Nagata, “Glycosylation-independent ERAD pathway serves as a backup system under ER stress,” Molecular Biology of the Cell, vol. 24, no. 20, pp. 3155–3163, 2013. View at Publisher · View at Google Scholar · View at Scopus
  90. M. Shenkman, B. Groisman, E. Ron, E. Avezov, L. M. Hendershot, and G. Z. Lederkremer, “A shared endoplasmic reticulum-associated degradation pathway involving the EDEM1 protein for glycosylated and nonglycosylated proteins,” Journal of Biological Chemistry, vol. 288, no. 4, pp. 2167–2178, 2013. View at Publisher · View at Google Scholar · View at Scopus
  91. J. L. Brodsky and W. R. Skach, “Protein folding and quality control in the endoplasmic reticulum: recent lessons from yeast and mammalian cell systems,” Current Opinion in Cell Biology, vol. 23, no. 4, pp. 464–475, 2011. View at Publisher · View at Google Scholar · View at Scopus
  92. S. Grubb, L. Guo, E. A. Fisher, and J. L. Brodsky, “Protein disulfide isomerases contribute differentially to the endoplasmic reticulum-associated degradation of apolipoprotein B and other substrates,” Molecular Biology of the Cell, vol. 23, no. 4, pp. 520–532, 2012. View at Publisher · View at Google Scholar · View at Scopus
  93. R. Y. Hampton and T. Sommer, “Finding the will and the way of ERAD substrate retrotranslocation,” Current Opinion in Cell Biology, vol. 24, no. 4, pp. 460–466, 2012. View at Publisher · View at Google Scholar · View at Scopus
  94. H. Meyer, M. Bug, and S. Bremer, “Emerging functions of the VCP/p97 AAA-ATPase in the ubiquitin system,” Nature Cell Biology, vol. 14, no. 2, pp. 117–123, 2012. View at Publisher · View at Google Scholar · View at Scopus
  95. T. Huyton, V. E. Pye, L. C. Briggs et al., “The crystal structure of murine p97/VCP at 3.6A,” Journal of Structural Biology, vol. 144, no. 3, pp. 337–348, 2003. View at Publisher · View at Google Scholar · View at Scopus
  96. B. DeLaBarre and A. T. Brunger, “Complete structure of p97/valosin-containing protein reveals communication between nucleotide domains,” Nature Structural Biology, vol. 10, no. 10, pp. 856–863, 2003. View at Publisher · View at Google Scholar · View at Scopus
  97. I. Dreveny, H. Kondo, K. Uchiyama, A. Shaw, X. Zhang, and P. S. Freemont, “Structural basis of the interaction between the AAA ATPase p97/VCP and its adaptor protein p47,” The EMBO Journal, vol. 23, no. 5, pp. 1030–1039, 2004. View at Publisher · View at Google Scholar · View at Scopus
  98. H. Meyer and C. C. Weihl, “The VCP/p97 system at a glance: connecting cellular function to disease pathogenesis,” Journal of Cell Science, vol. 127, no. 18, pp. 3877–3883, 2014. View at Publisher · View at Google Scholar · View at Scopus
  99. P. H. Vekaria, T. Home, S. Weir, F. J. Schoenen, and R. Rao, “Targeting p97 to disrupt protein homeostasis in cancer,” Frontiers in Oncology, vol. 6, p. 181, 2016. View at Publisher · View at Google Scholar · View at Scopus
  100. M. Mehnert, T. Sommer, and E. Jarosch, “Der1 promotes movement of misfolded proteins through the endoplasmic reticulum membrane,” Nature Cell Biology, vol. 16, no. 1, pp. 77–86, 2014. View at Publisher · View at Google Scholar · View at Scopus
  101. J. Wahlman, G. N. DeMartino, W. R. Skach, N. J. Bulleid, J. L. Brodsky, and A. E. Johnson, “Real-time fluorescence detection of ERAD substrate retrotranslocation in a mammalian in vitro system,” Cell, vol. 129, no. 5, pp. 943–955, 2007. View at Publisher · View at Google Scholar · View at Scopus
  102. E. J. Greenblatt, J. A. Olzmann, and R. R. Kopito, “Derlin-1 is a rhomboid pseudoprotease required for the dislocation of mutant α-1 antitrypsin from the endoplasmic reticulum,” Nature Structural & Molecular Biology, vol. 18, no. 10, pp. 1147–1152, 2011. View at Publisher · View at Google Scholar · View at Scopus
  103. B. N. Lilley and H. L. Ploegh, “A membrane protein required for dislocation of misfolded proteins from the ER,” Nature, vol. 429, no. 6994, pp. 834–840, 2004. View at Publisher · View at Google Scholar · View at Scopus
  104. Y. Ye, Y. Shibata, C. Yun, D. Ron, and T. A. Rapoport, “A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol,” Nature, vol. 429, no. 6994, pp. 841–847, 2004. View at Publisher · View at Google Scholar · View at Scopus
  105. Y. Ye, Y. Shibata, M. Kikkert, S. van Voorden, E. Wiertz, and T. A. Rapoport, “Recruitment of the p97 ATPase and ubiquitin ligases to the site of retrotranslocation at the endoplasmic reticulum membrane,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 40, pp. 14132–14138, 2005. View at Publisher · View at Google Scholar · View at Scopus
  106. Y. Oda, T. Okada, H. Yoshida, R. J. Kaufman, K. Nagata, and K. Mori, “Derlin-2 and Derlin-3 are regulated by the mammalian unfolded protein response and are required for ER-associated degradation,” Journal of Cell Biology, vol. 172, no. 3, pp. 383–393, 2006. View at Publisher · View at Google Scholar · View at Scopus
  107. B. N. Lilley and H. L. Ploegh, “Multiprotein complexes that link dislocation, ubiquitination, and extraction of misfolded proteins from the endoplasmic reticulum membrane,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 40, pp. 14296–14301, 2005. View at Publisher · View at Google Scholar · View at Scopus
  108. L. Fleig, N. Bergbold, P. Sahasrabudhe, B. Geiger, L. Kaltak, and M. K. Lemberg, “Ubiquitin-dependent intramembrane rhomboid protease promotes ERAD of membrane proteins,” Molecular Cell, vol. 47, no. 4, pp. 558–569, 2012. View at Publisher · View at Google Scholar · View at Scopus
  109. J. L. Brodsky, “Cleaning up: ER-associated degradation to the rescue,” Cell, vol. 151, no. 6, pp. 1163–1167, 2012. View at Publisher · View at Google Scholar · View at Scopus
  110. J. M. Williams, T. Inoue, L. Banks, and B. Tsai, “The ERdj5-Sel1L complex facilitates cholera toxin retrotranslocation,” Molecular Biology of the Cell, vol. 24, no. 6, pp. 785–795, 2013. View at Publisher · View at Google Scholar · View at Scopus
  111. B. Mueller, B. N. Lilley, and H. L. Ploegh, “SEL1L, the homologue of yeast Hrd3p, is involved in protein dislocation from the mammalian ER,” Journal of Cell Biology, vol. 175, no. 2, pp. 261–270, 2006. View at Publisher · View at Google Scholar · View at Scopus
  112. B. Mueller, E. J. Klemm, E. Spooner, J. H. Claessen, and H. L. Ploegh, “SEL1L nucleates a protein complex required for dislocation of misfolded glycoproteins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 34, pp. 12325–12330, 2008. View at Publisher · View at Google Scholar · View at Scopus
  113. Y. Iida, T. Fujimori, K. Okawa, K. Nagata, I. Wada, and N. Hosokawa, “SEL1L protein critically determines the stability of the HRD1-SEL1L endoplasmic reticulum-associated degradation (ERAD) complex to optimize the degradation kinetics of ERAD substrates,” Journal of Biological Chemistry, vol. 286, no. 19, pp. 16929–16939, 2011. View at Publisher · View at Google Scholar · View at Scopus
  114. E. J. Klemm, E. Spooner, and H. L. Ploegh, “Dual role of ancient ubiquitous protein 1 (AUP1) in lipid droplet accumulation and endoplasmic reticulum (ER) protein quality control,” Journal of Biological Chemistry, vol. 286, no. 43, pp. 37602–37614, 2011. View at Publisher · View at Google Scholar · View at Scopus
  115. J. C. Christianson, J. A. Olzmann, T. A. Shaler et al., “Defining human ERAD networks through an integrative mapping strategy,” Nature Cell Biology, vol. 14, no. 1, pp. 93–105, 2011. View at Publisher · View at Google Scholar · View at Scopus
  116. R. G. Gardner, G. M. Swarbrick, N. W. Bays et al., “Endoplasmic reticulum degradation requires lumen to cytosol signaling. Transmembrane control of Hrd1p by Hrd3p,” The Journal of Cell Biology, vol. 151, no. 1, pp. 69–82, 2000. View at Publisher · View at Google Scholar · View at Scopus
  117. P. Carvalho, V. Goder, and T. A. Rapoport, “Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins,” Cell, vol. 126, no. 2, pp. 361–373, 2006. View at Publisher · View at Google Scholar · View at Scopus
  118. V. Denic, E. M. Quan, and J. S. Weissman, “A luminal surveillance complex that selects misfolded glycoproteins for ER-associated degradation,” Cell, vol. 126, no. 2, pp. 349–359, 2006. View at Publisher · View at Google Scholar · View at Scopus
  119. R. Gauss, E. Jarosch, T. Sommer, and C. Hirsch, “A complex of Yos9p and the HRD ligase integrates endoplasmic reticulum quality control into the degradation machinery,” Nature Cell Biology, vol. 8, no. 8, pp. 849–854, 2006. View at Publisher · View at Google Scholar · View at Scopus
  120. S. Sun, G. Shi, X. Han et al., “Sel1L is indispensable for mammalian endoplasmic reticulum-associated degradation, endoplasmic reticulum homeostasis, and survival,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 5, pp. E582–E591, 2014. View at Publisher · View at Google Scholar · View at Scopus
  121. J. P. Lu, Y. Wang, D. A. Sliter, M. M. Pearce, and R. J. Wojcikiewicz, “RNF170 protein, an endoplasmic reticulum membrane ubiquitin ligase, mediates inositol 1,4,5-trisphosphate receptor ubiquitination and degradation,” The Journal of Biological Chemistry, vol. 286, no. 27, pp. 24426–24433, 2011. View at Publisher · View at Google Scholar · View at Scopus
  122. Y. J. Jeon, J. H. Park, and C. H. Chung, “Interferon-stimulated gene 15 in the control of cellular responses to genotoxic stress,” Molecules and Cells, vol. 40, no. 2, pp. 83–89, 2017. View at Publisher · View at Google Scholar
  123. K. D. Wilkinson, “Regulation of ubiquitin-dependent processes by deubiquitinating enzymes,” The FASEB Journal, vol. 11, no. 14, pp. 1245–1256, 1997. View at Google Scholar
  124. Y. Shimizu, Y. Okuda-Shimizu, and L. M. Hendershot, “Ubiquitylation of an ERAD substrate occurs on multiple types of amino acids,” Molecular Cell, vol. 40, no. 6, pp. 917–926, 2010. View at Publisher · View at Google Scholar · View at Scopus
  125. X. Wang, R. A. Herr, W. J. Chua, L. Lybarger, E. J. Wiertz, and T. H. Hansen, “Ubiquitination of serine, threonine, or lysine residues on the cytoplasmic tail can induce ERAD of MHC-I by viral E3 ligase mK3,” The Journal of Cell Biology, vol. 177, no. 4, pp. 613–624, 2007. View at Publisher · View at Google Scholar · View at Scopus
  126. S. Ishikura, A. M. Weissman, and J. S. Bonifacino, “Serine residues in the cytosolic tail of the T-cell antigen receptor alpha-chain mediate ubiquitination and endoplasmic reticulum-associated degradation of the unassembled protein,” The Journal of Biological Chemistry, vol. 285, no. 31, pp. 23916–23924, 2010. View at Publisher · View at Google Scholar · View at Scopus
  127. F. Ikeda and I. Dikic, “Atypical ubiquitin chains: new molecular signals. 'Protein modifications: beyond the usual Suspects' review series,” EMBO Reports, vol. 9, no. 6, pp. 536–542, 2008. View at Publisher · View at Google Scholar · View at Scopus
  128. Y. Kulathu and D. Komander, “Atypical ubiquitylation - the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages,” Nature Reviews. Molecular Cell Biology, vol. 13, no. 8, pp. 508–523, 2012. View at Publisher · View at Google Scholar · View at Scopus
  129. C. M. Pickart and D. Fushman, “Polyubiquitin chains: polymeric protein signals,” Current Opinion in Chemical Biology, vol. 8, no. 6, pp. 610–616, 2004. View at Publisher · View at Google Scholar · View at Scopus
  130. W. Li and Y. Ye, “Polyubiquitin chains: functions, structures, and mechanisms,” Cellular and Molecular Life Sciences, vol. 65, no. 15, pp. 2397–2406, 2008. View at Publisher · View at Google Scholar · View at Scopus
  131. E. Nadav, A. Shmueli, H. Barr, H. Gonen, A. Ciechanover, and Y. Reiss, “A novel mammalian endoplasmic reticulum ubiquitin ligase homologous to the yeast Hrd1,” Biochemical and Biophysical Research Communications, vol. 303, no. 1, pp. 91–97, 2003. View at Publisher · View at Google Scholar · View at Scopus
  132. M. Kikkert, R. Doolman, M. Dai et al., “Human HRD1 is an E3 ubiquitin ligase involved in degradation of proteins from the endoplasmic reticulum,” The Journal of Biological Chemistry, vol. 279, no. 5, pp. 3525–3534, 2004. View at Publisher · View at Google Scholar · View at Scopus
  133. S. Fang, M. Ferrone, C. Yang, J. P. Jensen, S. Tiwari, and A. M. Weissman, “The tumor autocrine motility factor receptor, gp78, is a ubiquitin protein ligase implicated in degradation from the endoplasmic reticulum,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 25, pp. 14422–14427, 2001. View at Publisher · View at Google Scholar · View at Scopus
  134. G. Hassink, M. Kikkert, S. van Voorden et al., “TEB4 is a C4HC3 RING finger-containing ubiquitin ligase of the endoplasmic reticulum,” Biochemical Journal, vol. 388, no. 2, pp. 647–655, 2005. View at Publisher · View at Google Scholar · View at Scopus
  135. J. M. Younger, L. Chen, H. Y. Ren et al., “Sequential quality-control checkpoints triage misfolded cystic fibrosis transmembrane conductance regulator,” Cell, vol. 126, no. 3, pp. 571–582, 2006. View at Publisher · View at Google Scholar · View at Scopus
  136. D. Morito, K. Hirao, Y. Oda et al., “Gp78 cooperates with RMA1 in endoplasmic reticulum-associated degradation of CFTRDeltaF508,” Molecular Biology of the Cell, vol. 19, no. 4, pp. 1328–1336, 2008. View at Publisher · View at Google Scholar · View at Scopus
  137. Y. J. Jeon, S. Khelifa, B. Ratnikov et al., “Regulation of glutamine carrier proteins by RNF5 determines breast cancer response to ER stress-inducing chemotherapies,” Cancer Cell, vol. 27, no. 3, pp. 354–369, 2015. View at Publisher · View at Google Scholar · View at Scopus
  138. V. Tomati, E. Sondo, A. Armirotti et al., “Genetic inhibition of the ubiquitin ligase Rnf5 attenuates phenotypes associated to F508del cystic fibrosis mutation,” Scientific Reports, vol. 5, no. 1, p. 12138, 2015. View at Publisher · View at Google Scholar · View at Scopus
  139. Y. Imai, M. Soda, S. Hatakeyama et al., “CHIP is associated with Parkin, a gene responsible for familial Parkinson’s disease, and enhances its ubiquitin ligase activity,” Molecular Cell, vol. 10, no. 1, pp. 55–67, 2002. View at Publisher · View at Google Scholar · View at Scopus
  140. G. C. Meacham, C. Patterson, W. Zhang, J. M. Younger, and D. M. Cyr, “The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation,” Nature Cell Biology, vol. 3, no. 1, pp. 100–105, 2001. View at Publisher · View at Google Scholar · View at Scopus
  141. Y. Yoshida, T. Chiba, F. Tokunaga et al., “E3 ubiquitin ligase that recognizes sugar chains,” Nature, vol. 418, no. 6896, pp. 438–442, 2002. View at Publisher · View at Google Scholar · View at Scopus
  142. Y. Yoshida, F. Tokunaga, T. Chiba, K. Iwai, K. Tanaka, and T. Tai, “Fbs2 is a new member of the E3 ubiquitin ligase family that recognizes sugar chains,” The Journal of Biological Chemistry, vol. 278, no. 44, pp. 43877–43884, 2003. View at Publisher · View at Google Scholar · View at Scopus
  143. J. G. Magadan, F. J. Perez-Victoria, R. Sougrat, Y. Ye, K. Strebel, and J. S. Bonifacino, “Multilayered mechanism of CD4 downregulation by HIV-1 Vpu involving distinct ER retention and ERAD targeting steps,” PLoS Pathogens, vol. 6, no. 4, article e1000869, 2010. View at Publisher · View at Google Scholar
  144. X. Guo, S. Shen, S. Song et al., “The E3 ligase Smurf1 regulates Wolfram syndrome protein stability at the endoplasmic reticulum,” The Journal of Biological Chemistry, vol. 286, no. 20, pp. 18037–18047, 2011. View at Publisher · View at Google Scholar · View at Scopus
  145. W. H. Fry, C. Simion, C. Sweeney, and K. L. Carraway III, “Quantity control of the ErbB3 receptor tyrosine kinase at the endoplasmic reticulum,” Molecular and Cellular Biology, vol. 31, no. 14, pp. 3009–3018, 2011. View at Publisher · View at Google Scholar · View at Scopus
  146. Y. Jo, P. C. Lee, P. V. Sguigna, and R. A. DeBose-Boyd, “Sterol-induced degradation of HMG CoA reductase depends on interplay of two Insigs and two ubiquitin ligases, gp78 and Trc8,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 51, pp. 20503–20508, 2011. View at Publisher · View at Google Scholar · View at Scopus
  147. T. Zhang, Y. Xu, Y. Liu, and Y. Ye, “gp78 functions downstream of Hrd1 to promote degradation of misfolded proteins of the endoplasmic reticulum,” Molecular Biology of the Cell, vol. 26, no. 24, pp. 4438–4450, 2015. View at Publisher · View at Google Scholar · View at Scopus
  148. A. Stein, A. Ruggiano, P. Carvalho, and T. A. Rapoport, “Key steps in ERAD of luminal ER proteins reconstituted with purified components,” Cell, vol. 158, no. 6, pp. 1375–1388, 2014. View at Publisher · View at Google Scholar
  149. J. Stevenson, E. Y. Huang, and J. A. Olzmann, “Endoplasmic reticulum-associated degradation and lipid homeostasis,” Annual Review of Nutrition, vol. 36, no. 1, pp. 511–542, 2016. View at Publisher · View at Google Scholar · View at Scopus
  150. A. Shmueli, Y. C. Tsai, M. Yang, M. A. Braun, and A. M. Weissman, “Targeting of gp78 for ubiquitin-mediated proteasomal degradation by Hrd1: cross-talk between E3s in the endoplasmic reticulum,” Biochemical and Biophysical Research Communications, vol. 390, no. 3, pp. 758–762, 2009. View at Publisher · View at Google Scholar · View at Scopus
  151. P. Ballar, A. U. Ors, H. Yang, and S. Fang, “Differential regulation of CFTRDeltaF508 degradation by ubiquitin ligases gp78 and Hrd1,” The International Journal of Biochemistry & Cell Biology, vol. 42, no. 1, pp. 167–173, 2010. View at Publisher · View at Google Scholar · View at Scopus
  152. M. Knop, A. Finger, T. Braun, K. Hellmuth, and D. H. Wolf, “Der1, a novel protein specifically required for endoplasmic reticulum degradation in yeast,” The EMBO Journal, vol. 15, no. 4, pp. 753–763, 1996. View at Google Scholar
  153. M. Kothe, Y. Ye, J. S. Wagner et al., “Role of p97 AAA-ATPase in the retrotranslocation of the cholera toxin A1 chain, a non-ubiquitinated substrate,” The Journal of Biological Chemistry, vol. 280, no. 30, pp. 28127–28132, 2005. View at Publisher · View at Google Scholar · View at Scopus
  154. R. Gauss, T. Sommer, and E. Jarosch, “The Hrd1p ligase complex forms a linchpin between ER-lumenal substrate selection and Cdc48p recruitment,” The EMBO Journal, vol. 25, no. 9, pp. 1827–1835, 2006. View at Publisher · View at Google Scholar · View at Scopus
  155. P. Carvalho, A. M. Stanley, and T. A. Rapoport, “Retrotranslocation of a misfolded luminal ER protein by the ubiquitin-ligase Hrd1p,” Cell, vol. 143, no. 4, pp. 579–591, 2010. View at Publisher · View at Google Scholar · View at Scopus
  156. E. Rabinovich, A. Kerem, K. U. Frohlich, N. Diamant, and S. Bar-Nun, “AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation,” Molecular and Cellular Biology, vol. 22, no. 2, pp. 626–634, 2002. View at Publisher · View at Google Scholar · View at Scopus
  157. Y. Ye, H. H. Meyer, and T. A. Rapoport, “The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol,” Nature, vol. 414, no. 6864, pp. 652–656, 2001. View at Publisher · View at Google Scholar · View at Scopus
  158. J. Liang, C. Yin, H. Doong et al., “Characterization of erasin (UBXD2): a new ER protein that promotes ER-associated protein degradation,” Journal of Cell Science, vol. 119, no. 19, pp. 4011–4024, 2006. View at Publisher · View at Google Scholar · View at Scopus
  159. M. Suzuki, T. Otsuka, Y. Ohsaki et al., “Derlin-1 and UBXD8 are engaged in dislocation and degradation of lipidated ApoB-100 at lipid droplets,” Molecular Biology of the Cell, vol. 23, no. 5, pp. 800–810, 2012. View at Publisher · View at Google Scholar · View at Scopus
  160. P. Ballar, Y. Shen, H. Yang, and S. Fang, “The role of a novel p97/valosin-containing protein-interacting motif of gp78 in endoplasmic reticulum-associated degradation,” The Journal of Biological Chemistry, vol. 281, no. 46, pp. 35359–35368, 2006. View at Publisher · View at Google Scholar · View at Scopus
  161. I. Kim, J. Ahn, C. Liu et al., “The Png1-Rad23 complex regulates glycoprotein turnover,” The Journal of Cell Biology, vol. 172, no. 2, pp. 211–219, 2006. View at Publisher · View at Google Scholar · View at Scopus
  162. G. Li, G. Zhao, X. Zhou, H. Schindelin, and W. J. Lennarz, “The AAA ATPase p97 links peptide N-glycanase to the endoplasmic reticulum-associated E3 ligase autocrine motility factor receptor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 22, pp. 8348–8353, 2006. View at Publisher · View at Google Scholar · View at Scopus
  163. R. Ernst, B. Mueller, H. L. Ploegh, and C. Schlieker, “The otubain YOD1 is a deubiquitinating enzyme that associates with p97 to facilitate protein dislocation from the ER,” Molecular Cell, vol. 36, no. 1, pp. 28–38, 2009. View at Publisher · View at Google Scholar · View at Scopus
  164. M. E. Sowa, E. J. Bennett, S. P. Gygi, and J. W. Harper, “Defining the human deubiquitinating enzyme interaction landscape,” Cell, vol. 138, no. 2, pp. 389–403, 2009. View at Publisher · View at Google Scholar · View at Scopus
  165. Q. Wang, L. Li, and Y. Ye, “Regulation of retrotranslocation by p97-associated deubiquitinating enzyme ataxin-3,” The Journal of Cell Biology, vol. 174, no. 7, pp. 963–971, 2006. View at Publisher · View at Google Scholar · View at Scopus
  166. Y. Xu, Y. Liu, J. G. Lee, and Y. Ye, “A ubiquitin-like domain recruits an oligomeric chaperone to a retrotranslocation complex in endoplasmic reticulum-associated degradation,” The Journal of Biological Chemistry, vol. 288, no. 25, pp. 18068–18076, 2013. View at Publisher · View at Google Scholar · View at Scopus
  167. Q. Wang, Y. Liu, N. Soetandyo, K. Baek, R. Hegde, and Y. Ye, “A ubiquitin ligase-associated chaperone holdase maintains polypeptides in soluble states for proteasome degradation,” Molecular Cell, vol. 42, no. 6, pp. 758–770, 2011. View at Publisher · View at Google Scholar · View at Scopus
  168. Y. Xu, M. Cai, Y. Yang, L. Huang, and Y. Ye, “SGTA recognizes a noncanonical ubiquitin-like domain in the Bag6-Ubl4A-Trc35 complex to promote endoplasmic reticulum-associated degradation,” Cell Reports, vol. 2, no. 6, pp. 1633–1644, 2012. View at Publisher · View at Google Scholar · View at Scopus
  169. D. Hanahan and R. A. Weinberg, “Hallmarks of cancer: the next generation,” Cell, vol. 144, no. 5, pp. 646–674, 2011. View at Publisher · View at Google Scholar · View at Scopus
  170. Y. Ma and L. M. Hendershot, “The role of the unfolded protein response in tumour development: friend or foe?” Nature Reviews. Cancer, vol. 4, no. 12, pp. 966–977, 2004. View at Publisher · View at Google Scholar · View at Scopus
  171. D. Ruggero, “Translational control in cancer etiology,” Cold Spring Harbor Perspectives in Biology, vol. 5, no. 2, pp. 1–27, 2013. View at Publisher · View at Google Scholar · View at Scopus
  172. H. Urra, E. Dufey, T. Avril, E. Chevet, and C. Hetz, “Endoplasmic reticulum stress and the hallmarks of cancer,” Trends in Cancer, vol. 2, no. 5, pp. 252–262, 2016. View at Publisher · View at Google Scholar · View at Scopus
  173. H. Vanacker, J. Vetters, L. Moudombi, C. Caux, S. Janssens, and M. C. Michallet, “Emerging role of the unfolded protein response in tumor immunosurveillance,” Trends in Cancer, vol. 3, no. 7, pp. 491–505, 2017. View at Publisher · View at Google Scholar
  174. C. Denoyelle, G. Abou-Rjaily, V. Bezrookove et al., “Anti-oncogenic role of the endoplasmic reticulum differentially activated by mutations in the MAPK pathway,” Nature Cell Biology, vol. 8, no. 10, pp. 1053–1063, 2006. View at Publisher · View at Google Scholar · View at Scopus
  175. A. L. Huber, J. Lebeau, P. Guillaumot et al., “p58IPK-mediated attenuation of the proapoptotic PERK-CHOP pathway allows malignant progression upon low glucose,” Molecular Cell, vol. 49, no. 6, pp. 1049–1059, 2013. View at Publisher · View at Google Scholar · View at Scopus
  176. G. Ramadori, G. Konstantinidou, N. Venkateswaran et al., “Diet-induced unresolved ER stress hinders KRAS-driven lung tumorigenesis,” Cell Metabolism, vol. 21, no. 1, pp. 117–125, 2015. View at Publisher · View at Google Scholar · View at Scopus
  177. L. Niederreiter, T. M. Fritz, T. E. Adolph et al., “ER stress transcription factor Xbp1 suppresses intestinal tumorigenesis and directs intestinal stem cells,” The Journal of Experimental Medicine, vol. 210, no. 10, pp. 2041–2056, 2013. View at Publisher · View at Google Scholar · View at Scopus
  178. M. Bi, C. Naczki, M. Koritzinsky et al., “ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth,” The EMBO Journal, vol. 24, no. 19, pp. 3470–3481, 2005. View at Publisher · View at Google Scholar · View at Scopus
  179. J. D. Blais, C. L. Addison, R. Edge et al., “Perk-dependent translational regulation promotes tumor cell adaptation and angiogenesis in response to hypoxic stress,” Molecular and Cellular Biology, vol. 26, no. 24, pp. 9517–9532, 2006. View at Publisher · View at Google Scholar · View at Scopus
  180. S. Dey, C. M. Sayers, I. I. Verginadis et al., “ATF4-dependent induction of heme oxygenase 1 prevents anoikis and promotes metastasis,” The Journal of Clinical Investigation, vol. 125, no. 7, pp. 2592–2608, 2015. View at Publisher · View at Google Scholar · View at Scopus
  181. S. B. Cullinan, D. Zhang, M. Hannink, E. Arvisais, R. J. Kaufman, and J. A. Diehl, “Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival,” Molecular and Cellular Biology, vol. 23, no. 20, pp. 7198–7209, 2003. View at Publisher · View at Google Scholar · View at Scopus
  182. C. A. Del Vecchio, Y. Feng, E. S. Sokol et al., “De-differentiation confers multidrug resistance via noncanonical PERK-Nrf2 signaling,” PLoS Biology, vol. 12, no. 9, article e1001945, 2014. View at Publisher · View at Google Scholar · View at Scopus
  183. W. Zhang, V. Hietakangas, S. Wee, S. C. Lim, J. Gunaratne, and S. M. Cohen, “ER stress potentiates insulin resistance through PERK-mediated FOXO phosphorylation,” Genes & Development, vol. 27, no. 4, pp. 441–449, 2013. View at Publisher · View at Google Scholar · View at Scopus
  184. D. Pytel, I. Majsterek, and J. A. Diehl, “Tumor progression and the different faces of the PERK kinase,” Oncogene, vol. 35, no. 10, pp. 1207–1215, 2016. View at Publisher · View at Google Scholar · View at Scopus
  185. Y. Kouroku, E. Fujita, I. Tanida et al., “ER stress (PERK/eIF2α phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation,” Cell Death and Differentiation, vol. 14, no. 2, pp. 230–239, 2007. View at Publisher · View at Google Scholar · View at Scopus
  186. W. B'Chir, A. C. Maurin, V. Carraro et al., “The eIF2α/ATF4 pathway is essential for stress-induced autophagy gene expression,” Nucleic Acids Research, vol. 41, no. 16, pp. 7683–7699, 2013. View at Publisher · View at Google Scholar · View at Scopus
  187. S. I. Grivennikov and M. Karin, “Dangerous liaisons: STAT3 and NF-κB collaboration and crosstalk in cancer,” Cytokine & Growth Factor Reviews, vol. 21, no. 1, pp. 11–19, 2010. View at Publisher · View at Google Scholar · View at Scopus
  188. O. Pluquet, N. Dejeans, M. Bouchecareilh et al., “Posttranscriptional regulation of PER1 underlies the oncogenic function of IREα,” Cancer Research, vol. 73, no. 15, pp. 4732–4743, 2013. View at Publisher · View at Google Scholar · View at Scopus
  189. B. Kharabi Masouleh, H. Geng, C. Hurtz et al., “Mechanistic rationale for targeting the unfolded protein response in pre-B acute lymphoblastic leukemia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 21, pp. E2219–E2228, 2014. View at Publisher · View at Google Scholar · View at Scopus
  190. N. Mimura, M. Fulciniti, G. Gorgun et al., “Blockade of XBP1 splicing by inhibition of IRE1α is a promising therapeutic option in multiple myeloma,” Blood, vol. 119, no. 24, pp. 5772–5781, 2012. View at Publisher · View at Google Scholar · View at Scopus
  191. I. Papandreou, N. C. Denko, M. Olson et al., “Identification of an Ire1alpha endonuclease specific inhibitor with cytotoxic activity against human multiple myeloma,” Blood, vol. 117, no. 4, pp. 1311–1314, 2011. View at Publisher · View at Google Scholar · View at Scopus
  192. M. Ri, E. Tashiro, D. Oikawa et al., “Identification of Toyocamycin, an agent cytotoxic for multiple myeloma cells, as a potent inhibitor of ER stress-induced XBP1 mRNA splicing,” Blood Cancer Journal, vol. 2, no. 7, article e79, 2012. View at Publisher · View at Google Scholar · View at Scopus
  193. C. Greenman, P. Stephens, R. Smith et al., “Patterns of somatic mutation in human cancer genomes,” Nature, vol. 446, no. 7132, pp. 153–158, 2007. View at Publisher · View at Google Scholar · View at Scopus
  194. Z. Xue, Y. He, K. Ye, Z. Gu, Y. Mao, and L. Qi, “A conserved structural determinant located at the interdomain region of mammalian inositol-requiring enzyme 1α,” The Journal of Biological Chemistry, vol. 286, no. 35, pp. 30859–30866, 2011. View at Publisher · View at Google Scholar · View at Scopus
  195. D. M. Schewe and J. A. Aguirre-Ghiso, “ATF6α-Rheb-mTOR signaling promotes survival of dormant tumor cells in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 30, pp. 10519–10524, 2008. View at Publisher · View at Google Scholar · View at Scopus
  196. Y. Wang, G. N. Alam, Y. Ning et al., “The unfolded protein response induces the angiogenic switch in human tumor cells through the PERK/ATF4 pathway,” Cancer Research, vol. 72, no. 20, pp. 5396–5406, 2012. View at Publisher · View at Google Scholar · View at Scopus
  197. X. Chen, D. Iliopoulos, Q. Zhang et al., “XBP1 promotes triple-negative breast cancer by controlling the HIF1α pathway,” Nature, vol. 508, no. 7494, pp. 103–107, 2014. View at Publisher · View at Google Scholar · View at Scopus
  198. E. Karali, S. Bellou, D. Stellas et al., “VEGF Signals through ATF6 and PERK to promote endothelial cell survival and angiogenesis in the absence of ER stress,” Molecular Cell, vol. 54, no. 4, pp. 559–572, 2014. View at Publisher · View at Google Scholar · View at Scopus
  199. J. R. Cubillos-Ruiz, S. E. Bettigole, and L. H. Glimcher, “Tumorigenic and immunosuppressive effects of endoplasmic reticulum stress in cancer,” Cell, vol. 168, no. 4, pp. 692–706, 2017. View at Publisher · View at Google Scholar
  200. D. Senft and Z. A. Ronai, “Adaptive stress responses during tumor metastasis and dormancy,” Trends in Cancer, vol. 2, no. 8, pp. 429–442, 2016. View at Publisher · View at Google Scholar · View at Scopus
  201. M. A. Nieto, R. Y. Huang, R. A. Jackson, and J. P. Thiery, “EMT: 2016,” Cell, vol. 166, no. 1, pp. 21–45, 2016. View at Publisher · View at Google Scholar · View at Scopus
  202. H. Mujcic, A. Nagelkerke, K. M. Rouschop et al., “Hypoxic activation of the PERK/eIF2α arm of the unfolded protein response promotes metastasis through induction of LAMP3,” Clinical Cancer Research, vol. 19, no. 22, pp. 6126–6137, 2013. View at Publisher · View at Google Scholar · View at Scopus
  203. A. Nagelkerke, J. Bussink, H. Mujcic et al., “Hypoxia stimulates migration of breast cancer cells via the PERK/ATF4/LAMP3-arm of the unfolded protein response,” Breast Cancer Res, vol. 15, no. 1, article R2, pp. 467–480, 2013. View at Publisher · View at Google Scholar · View at Scopus
  204. H. Zhu, X. Chen, B. Chen et al., “Activating transcription factor 4 promotes esophageal squamous cell carcinoma invasion and metastasis in mice and is associated with poor prognosis in human patients,” PLoS One, vol. 9, no. 7, article e103882, 2014. View at Publisher · View at Google Scholar · View at Scopus
  205. G. Auf, A. Jabouille, S. Guerit et al., “Inositol-requiring enzyme 1alpha is a key regulator of angiogenesis and invasion in malignant glioma,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 35, pp. 15553–15558, 2010. View at Publisher · View at Google Scholar · View at Scopus
  206. N. Dejeans, O. Pluquet, S. Lhomond et al., “Autocrine control of glioma cells adhesion and migration through IRE1α-mediated cleavage of SPARC mRNA,” Journal of Cell Science, vol. 125, Part 18, pp. 4278–4287, 2012. View at Publisher · View at Google Scholar · View at Scopus
  207. N. R. Mahadevan, J. Rodvold, H. Sepulveda, S. Rossi, A. F. Drew, and M. Zanetti, “Transmission of endoplasmic reticulum stress and pro-inflammation from tumor cells to myeloid cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 16, pp. 6561–6566, 2011. View at Google Scholar
  208. N. R. Mahadevan, V. Anufreichik, J. J. Rodvold, K. T. Chiu, H. Sepulveda, and M. Zanetti, “Cell-extrinsic effects of tumor ER stress imprint myeloid dendritic cells and impair CD8+ T cell priming,” PLoS One, vol. 7, no. 12, article e51845, 2012. View at Publisher · View at Google Scholar · View at Scopus
  209. J. Pol, E. Vacchelli, F. Aranda et al., “Trial Watch: Immunogenic cell death inducers for anticancer chemotherapy,” Oncoimmunology, vol. 4, no. 4, article e1008866, 2015. View at Publisher · View at Google Scholar · View at Scopus
  210. D. V. Krysko, A. D. Garg, A. Kaczmarek, O. Krysko, P. Agostinis, and P. Vandenabeele, “Immunogenic cell death and DAMPs in cancer therapy,” Nature Reviews. Cancer, vol. 12, no. 12, pp. 860–875, 2012. View at Publisher · View at Google Scholar · View at Scopus
  211. A. R. van Vliet, S. Martin, A. D. Garg, and P. Agostinis, “The PERKs of damage-associated molecular patterns mediating cancer immunogenicity: from sensor to the plasma membrane and beyond,” Seminars in Cancer Biology, vol. 33, pp. 74–85, 2015. View at Publisher · View at Google Scholar · View at Scopus
  212. J. Fucikova, E. Becht, K. Iribarren et al., “Calreticulin expression in human non-small cell lung cancers correlates with increased accumulation of antitumor immune cells and favorable prognosis,” Cancer Research, vol. 76, no. 7, pp. 1746–1756, 2016. View at Publisher · View at Google Scholar · View at Scopus
  213. A. D. Garg, D. V. Krysko, T. Verfaillie et al., “A novel pathway combining calreticulin exposure and ATP secretion in immunogenic cancer cell death,” The EMBO Journal, vol. 31, no. 5, pp. 1062–1079, 2012. View at Publisher · View at Google Scholar · View at Scopus
  214. O. Kepp, L. Menger, E. Vacchelli et al., “Crosstalk between ER stress and immunogenic cell death,” Cytokine & Growth Factor Reviews, vol. 24, no. 4, pp. 311–318, 2013. View at Publisher · View at Google Scholar · View at Scopus
  215. C. Pozzi, A. Cuomo, I. Spadoni et al., “The EGFR-specific antibody cetuximab combined with chemotherapy triggers immunogenic cell death,” Nature Medicine, vol. 22, no. 6, pp. 624–631, 2016. View at Publisher · View at Google Scholar · View at Scopus
  216. S. E. Bettigole and L. H. Glimcher, “Endoplasmic reticulum stress in immunity,” Annual Review of Immunology, vol. 33, no. 1, pp. 107–138, 2015. View at Publisher · View at Google Scholar · View at Scopus
  217. N. N. Iwakoshi, A. H. Lee, P. Vallabhajosyula, K. L. Otipoby, K. Rajewsky, and L. H. Glimcher, “Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1,” Nature Immunology, vol. 4, no. 4, pp. 321–329, 2003. View at Publisher · View at Google Scholar · View at Scopus
  218. A. M. Reimold, N. N. Iwakoshi, J. Manis et al., “Plasma cell differentiation requires the transcription factor XBP-1,” Nature, vol. 412, no. 6844, pp. 300–307, 2001. View at Publisher · View at Google Scholar · View at Scopus
  219. R. Hu, Z. F. Chen, J. Yan et al., “Endoplasmic reticulum stress of neutrophils is required for ischemia/reperfusion-induced acute lung injury,” Journal of Immunology, vol. 195, no. 10, pp. 4802–4809, 2015. View at Publisher · View at Google Scholar · View at Scopus
  220. F. Martinon, X. Chen, A. H. Lee, and L. H. Glimcher, “TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages,” Nature Immunology, vol. 11, no. 5, pp. 411–418, 2010. View at Publisher · View at Google Scholar · View at Scopus
  221. J. R. Cubillos-Ruiz, P. C. Silberman, M. R. Rutkowski et al., “ER stress sensor XBP1 controls anti-tumor immunity by disrupting dendritic cell homeostasis,” Cell, vol. 161, no. 7, pp. 1527–1538, 2015. View at Publisher · View at Google Scholar · View at Scopus
  222. A. C. Herrera, V. J. Victorino, F. C. Campos et al., “Impact of tumor removal on the systemic oxidative profile of patients with breast cancer discloses lipid peroxidation at diagnosis as a putative marker of disease recurrence,” Clinical Breast Cancer, vol. 14, no. 6, pp. 451–459, 2014. View at Publisher · View at Google Scholar · View at Scopus
  223. D. L. Herber, W. Cao, Y. Nefedova et al., “Lipid accumulation and dendritic cell dysfunction in cancer,” Nature Medicine, vol. 16, no. 8, pp. 880–886, 2010. View at Publisher · View at Google Scholar · View at Scopus
  224. F. Hossain, A. A. Al-Khami, D. Wyczechowska et al., “Inhibition of fatty acid oxidation modulates immunosuppressive functions of myeloid-derived suppressor cells and enhances cancer therapies,” Cancer Immunology Research, vol. 3, no. 11, pp. 1236–1247, 2015. View at Publisher · View at Google Scholar · View at Scopus
  225. R. Ramakrishnan, V. A. Tyurin, F. Veglia et al., “Oxidized lipids block antigen cross-presentation by dendritic cells in cancer,” Journal of Immunology, vol. 192, no. 6, pp. 2920–2931, 2014. View at Publisher · View at Google Scholar · View at Scopus
  226. D. Yan, H. W. Wang, R. L. Bowman, and J. A. Joyce, “STAT3 and STAT6 signaling pathways synergize to promote Cathepsin secretion from macrophages via IRE1α activation,” Cell Reports, vol. 16, no. 11, pp. 2914–2927, 2016. View at Publisher · View at Google Scholar · View at Scopus
  227. T. Condamine, G. A. Dominguez, J. I. Youn et al., “Lectin-type oxidized LDL receptor-1 distinguishes population of human polymorphonuclear myeloid-derived suppressor cells in cancer patients,” Science Immunology, vol. 1, no. 2, pp. 1–15, 2016. View at Google Scholar
  228. C. H. Tang, S. Ranatunga, C. L. Kriss et al., “Inhibition of ER stress-associated IRE-1/XBP-1 pathway reduces leukemic cell survival,” The Journal of Clinical Investigation, vol. 124, no. 6, pp. 2585–2598, 2014. View at Publisher · View at Google Scholar · View at Scopus
  229. P. T. Thevenot, R. A. Sierra, P. L. Raber et al., “The stress-response sensor chop regulates the function and accumulation of myeloid-derived suppressor cells in tumors,” Immunity, vol. 41, no. 3, pp. 389–401, 2014. View at Publisher · View at Google Scholar · View at Scopus
  230. T. Condamine, V. Kumar, I. R. Ramachandran et al., “ER stress regulates myeloid-derived suppressor cell fate through TRAIL-R-mediated apoptosis,” The Journal of Clinical Investigation, vol. 124, no. 6, pp. 2626–2639, 2014. View at Publisher · View at Google Scholar · View at Scopus
  231. X. H. Ma, S. F. Piao, S. Dey et al., “Targeting ER stress-induced autophagy overcomes BRAF inhibitor resistance in melanoma,” The Journal of Clinical Investigation, vol. 124, no. 3, pp. 1406–1417, 2014. View at Publisher · View at Google Scholar · View at Scopus
  232. G. B. Park, D. Y. Hur, and D. Kim, “Combining CAL-101 with celecoxib enhances apoptosis of EBV-transformed B-cells through MAPK-induced ER stress,” Anticancer Research, vol. 35, no. 5, pp. 2699–2708, 2015. View at Google Scholar
  233. A. Strasser and H. Puthalakath, “Fold up or perish: unfolded protein response and chemotherapy,” Cell Death and Differentiation, vol. 15, no. 2, pp. 223–225, 2007. View at Publisher · View at Google Scholar · View at Scopus
  234. B. Kharabi Masouleh, E. Chevet, J. Panse et al., “Drugging the unfolded protein response in acute leukemias,” Journal of Hematology & Oncology, vol. 8, no. 1, p. 87, 2015. View at Publisher · View at Google Scholar · View at Scopus
  235. L. Vincenz, R. Jager, M. O'Dwyer, and A. Samali, “Endoplasmic reticulum stress and the unfolded protein response: targeting the Achilles heel of multiple myeloma,” Molecular Cancer Therapeutics, vol. 12, no. 6, pp. 831–843, 2013. View at Publisher · View at Google Scholar · View at Scopus
  236. K. M. Rouschop, L. J. Dubois, T. G. Keulers et al., “PERK/eIF2α signaling protects therapy resistant hypoxic cells through induction of glutathione synthesis and protection against ROS,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 12, pp. 4622–4627, 2013. View at Publisher · View at Google Scholar · View at Scopus
  237. M. Ogata, S. Hino, A. Saito et al., “Autophagy is activated for cell survival after endoplasmic reticulum stress,” Molecular and Cellular Biology, vol. 26, no. 24, pp. 9220–9231, 2006. View at Publisher · View at Google Scholar · View at Scopus
  238. Y. H. Shi, Z. B. Ding, J. Zhou et al., “Targeting autophagy enhances sorafenib lethality for hepatocellular carcinoma via ER stress-related apoptosis,” Autophagy, vol. 7, no. 10, pp. 1159–1172, 2011. View at Publisher · View at Google Scholar · View at Scopus
  239. J. R. Cubillos-Ruiz, S. Fiering, and J. R. Conejo-Garcia, “Nanomolecular targeting of dendritic cells for ovarian cancer therapy,” Future Oncology, vol. 5, no. 8, pp. 1189–1192, 2009. View at Publisher · View at Google Scholar · View at Scopus
  240. J. R. Cubillos-Ruiz, J. R. Baird, A. J. Tesone et al., “Reprogramming tumor-associated dendritic cells in vivo using miRNA mimetics triggers protective immunity against ovarian cancer,” Cancer Research, vol. 72, no. 7, pp. 1683–1693, 2012. View at Publisher · View at Google Scholar · View at Scopus
  241. T. Tanaka, T. Kajiwara, T. Torigoe, Y. Okamoto, N. Sato, and Y. Tamura, “Cancer-associated oxidoreductase ERO1-α drives the production of tumor-promoting myeloid-derived suppressor cells via oxidative protein folding,” Journal of Immunology, vol. 194, no. 4, pp. 2004–2010, 2015. View at Publisher · View at Google Scholar · View at Scopus
  242. I. Saez and D. Vilchez, “The mechanistic links between proteasome activity, aging and age-related diseases,” Current Genomics, vol. 15, no. 1, pp. 38–51, 2014. View at Publisher · View at Google Scholar · View at Scopus
  243. D. Vilchez, I. Saez, and A. Dillin, “The role of protein clearance mechanisms in organismal ageing and age-related diseases,” Nature Communications, vol. 5, p. 5659, 2014. View at Publisher · View at Google Scholar · View at Scopus
  244. M. Cattaneo, E. Fontanella, C. Canton, D. Delia, and I. Biunno, “SEL1L affects human pancreatic cancer cell cycle and invasiveness through modulation of PTEN and genes related to cell-matrix interactions,” Neoplasia, vol. 7, no. 11, pp. 1030–1038, 2005. View at Publisher · View at Google Scholar · View at Scopus
  245. H. Kim, A. Bhattacharya, and L. Qi, “Endoplasmic reticulum quality control in cancer: friend or foe,” Seminars in Cancer Biology, vol. 33, pp. 25–33, 2015. View at Publisher · View at Google Scholar · View at Scopus
  246. R. Orlandi, M. Cattaneo, F. Troglio et al., “SEL1L expression decreases breast tumor cell aggressiveness in vivo and in vitro,” Cancer Research, vol. 62, no. 2, pp. 567–574, 2002. View at Google Scholar
  247. H. Ashktorab, W. Green, G. Finzi et al., “SEL1L, an UPR response protein, a potential marker of colonic cell transformation,” Digestive Diseases and Sciences, vol. 57, no. 4, pp. 905–912, 2012. View at Publisher · View at Google Scholar · View at Scopus
  248. J. H. Baek, P. C. Mahon, J. Oh et al., “OS-9 interacts with hypoxia-inducible factor 1alpha and prolyl hydroxylases to promote oxygen-dependent degradation of HIF-1α,” Molecular Cell, vol. 17, no. 4, pp. 503–512, 2005. View at Publisher · View at Google Scholar · View at Scopus
  249. M. Ivan, K. Kondo, H. Yang et al., “HIFα targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing,” Science, vol. 292, no. 5516, pp. 464–468, 2001. View at Publisher · View at Google Scholar
  250. K. Yanagisawa, H. Konishi, C. Arima et al., “Novel metastasis-related gene CIM functions in the regulation of multiple cellular stress-response pathways,” Cancer Research, vol. 70, no. 23, pp. 9949–9958, 2010. View at Publisher · View at Google Scholar · View at Scopus
  251. L. A. Liotta, R. Mandler, G. Murano et al., “Tumor cell autocrine motility factor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 83, no. 10, pp. 3302–3306, 1986. View at Publisher · View at Google Scholar
  252. I. R. Nabi and A. Raz, “Cell shape modulation alters glycosylation of a metastatic melanoma cell-surface antigen,” International Journal of Cancer, vol. 40, no. 3, pp. 396–402, 1987. View at Publisher · View at Google Scholar · View at Scopus
  253. V. Joshi, A. Upadhyay, A. Kumar, and A. Mishra, “Gp78 E3 ubiquitin ligase: essential functions and contributions in proteostasis,” Frontiers in Cellular Neuroscience, vol. 11, p. 259, 2017. View at Publisher · View at Google Scholar
  254. S. Silletti, J. Yao, J. Sanford et al., “Autocrine motility factor-receptor in human bladder-carcinoma - gene-expression, loss of cell-contact regulation and chromosomal mapping,” International Journal of Oncology, vol. 3, no. 5, pp. 801–807, 1993. View at Google Scholar
  255. S. Nakamori, H. Watanabe, M. Kameyama et al., “Expression of autocrine motility factor receptor in colorectal cancer as a predictor for disease recurrence,” Cancer, vol. 74, no. 7, pp. 1855–1862, 1994. View at Publisher · View at Google Scholar
  256. K. Maruyama, H. Watanabe, H. Shiozaki et al., “Expression of autocrine motility factor receptor in human esophageal squamous cell carcinoma,” International Journal of Cancer, vol. 64, no. 5, pp. 316–321, 1995. View at Publisher · View at Google Scholar · View at Scopus
  257. S. Silletti, J. P. Yao, K. J. Pienta, and A. Raz, “Loss of cell-contact regulation and altered responses to autocrine motility factor correlate with increased malignancy in prostate cancer cells,” International Journal of Cancer, vol. 63, no. 1, pp. 100–105, 1995. View at Publisher · View at Google Scholar · View at Scopus
  258. T. Otto, W. Birchmeier, U. Schmidt et al., “Inverse relation of E-cadherin and autocrine motility factor receptor expression as a prognostic factor in patients with bladder carcinomas,” Cancer Research, vol. 54, no. 12, pp. 3120–3123, 1994. View at Google Scholar
  259. T. Otto, A. Bex, U. Schmidt, A. Raz, and H. Rubben, “Improved prognosis assessment for patients with bladder carcinoma,” The American Journal of Pathology, vol. 150, no. 6, pp. 1919–1923, 1997. View at Google Scholar
  260. K. Kawanishi, Y. Doki, H. Shiozaki et al., “Correlation between loss of E-cadherin expression and overexpression of autocrine motility factor receptor in association with progression of human gastric cancers,” American Journal of Clinical Pathology, vol. 113, no. 2, pp. 266–274, 2000. View at Publisher · View at Google Scholar
  261. Y. C. Tsai, A. Mendoza, J. M. Mariano et al., “The ubiquitin ligase gp78 promotes sarcoma metastasis by targeting KAI1 for degradation,” Nature Medicine, vol. 13, no. 12, pp. 1504–1509, 2007. View at Publisher · View at Google Scholar · View at Scopus
  262. B. Joshi, L. Li, and I. R. Nabi, “A role for KAI1 in promotion of cell proliferation and mammary gland hyperplasia by the gp78 ubiquitin ligase,” The Journal of Biological Chemistry, vol. 285, no. 12, pp. 8830–8839, 2010. View at Publisher · View at Google Scholar · View at Scopus
  263. L. Wang, G. Hou, L. Xue, J. Li, P. Wei, and P. Xu, “Autocrine motility factor receptor signaling pathway promotes cell invasion via activation of ROCK-2 in esophageal squamous cell cancer cells,” Cancer Investigation, vol. 28, no. 10, pp. 993–1003, 2010. View at Publisher · View at Google Scholar · View at Scopus
  264. M. Kajiro, R. Hirota, Y. Nakajima et al., “The ubiquitin ligase CHIP acts as an upstream regulator of oncogenic pathways,” Nature Cell Biology, vol. 11, no. 3, pp. 312–319, 2009. View at Publisher · View at Google Scholar · View at Scopus