Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014 (2014), Article ID 832704, 11 pages
http://dx.doi.org/10.1155/2014/832704
Review Article

The Role of the Selective Adaptor p62 and Ubiquitin-Like Proteins in Autophagy

Department of Anatomy, Cell and Developmental Biology, Eötvös Loránd University, Pázmány Péter sétány 1/C., Budapest 1117, Hungary

Received 4 April 2014; Revised 15 May 2014; Accepted 19 May 2014; Published 12 June 2014

Academic Editor: Ioannis P. Nezis

Copyright © 2014 Mónika Lippai and Péter Lőw. 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. D. H. Wolf, “Proteasomes: a historical retrospective,” in Proteasomes: The World of Regulatory Proteolysis, W. Hilt and D. H. Wolf, Eds., pp. 1–7, Madame Curie Bioscience Database: Landes Bioscience, 2000. View at Google Scholar
  2. Y. Feng, D. He, Z. Yao, and D. J. Klionsky, “The machinery of macroautophagy,” Cell Research, vol. 24, no. 1, pp. 24–41, 2014. View at Google Scholar
  3. V. I. Korolchuk, F. M. Menzies, and D. C. Rubinsztein, “Mechanisms of cross-talk between the ubiquitin-proteasome and autophagy-lysosome systems,” FEBS Letters, vol. 584, no. 7, pp. 1393–1398, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. H.-C. Tai and E. M. Schuman, “Ubiquitin, the proteasome and protein degradation in neuronal function and dysfunction,” Nature Reviews Neuroscience, vol. 9, no. 11, pp. 826–838, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. L. Huang, E. Kinnucan, G. Wang et al., “Structure of an E6AP-UbcH7 complex: insights into ubiquitination by the E2-E3 enzyme cascade,” Science, vol. 286, no. 5443, pp. 1321–1326, 1999. View at Publisher · View at Google Scholar · View at Scopus
  6. J. M. Huibregtse, M. Scheffner, S. Beaudenon, and P. M. Howley, “A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 7, pp. 2563–2567, 1995. View at Publisher · View at Google Scholar · View at Scopus
  7. M. D. Petroski and R. J. Deshaies, “Function and regulation of cullin-RING ubiquitin ligases,” Nature Reviews Molecular Cell Biology, vol. 6, no. 1, pp. 9–20, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Hochstrasser, “Lingering mysteries of ubiquitin-chain assembly,” Cell, vol. 124, no. 1, pp. 27–34, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. J. S. Thrower, L. Hoffman, M. Rechsteiner, and C. M. Pickart, “Recognition of the polyubiquitin proteolytic signal,” The EMBO Journal, vol. 19, no. 1, pp. 94–102, 2000. View at Google Scholar · View at Scopus
  10. O. Coux, K. Tanaka, and A. L. Goldberg, “Structure and functions of the 20S and 26S proteasomes,” Annual Review of Biochemistry, vol. 65, pp. 801–847, 1996. View at Google Scholar · View at Scopus
  11. W. Baumeister, J. Walz, F. Zühl, and E. Seemüller, “The proteasome: paradigm of a self-compartmentalizing protease,” Cell, vol. 92, no. 3, pp. 367–380, 1998. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Murata, H. Yashiroda, and K. Tanaka, “Molecular mechanisms of proteasome assembly,” Nature Reviews Molecular Cell Biology, vol. 10, no. 2, pp. 104–115, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. C. Behrends and J. W. Harper, “Constructing and decoding unconventional ubiquitin chains,” Nature Structural and Molecular Biology, vol. 18, no. 5, pp. 520–528, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. R. L. Welchman, C. Gordon, and R. J. Mayer, “Ubiquitin and ubiquitin-like proteins as multifunctional signals,” Nature Reviews Molecular Cell Biology, vol. 6, no. 8, pp. 599–609, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. E. Walinda, D. Morimoto, K. Sugase, T. Konuma, H. Tochio, and M. Shirakawa, “Solution atructure of the ubiquitin-associated (UBA) domain of human autophagy receptor NBR1 and its interaction with ubiquitin and polyubiquitin,” Journal of Biological Chemistry, vol. 289, no. 20, pp. 13890–13902, 2014. View at Google Scholar
  16. M. Hochstrasser, “Origin and function of ubiquitin-like proteins,” Nature, vol. 458, no. 7237, pp. 422–429, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. N. Mulakkal, P. Nagy, S. Takáts, R. Tusco, G. Juhász, and I. P. Nezis, “Autophagy in Drosophila: from historical studies to current knowledge,” BioMed Research International, vol. 2014, Article ID 273473, 24 pages, 2014. View at Publisher · View at Google Scholar
  18. N. Mizushima, T. Yoshimori, and Y. Ohsumi, “The role of atg proteins in autophagosome formation,” Annual Review of Cell and Developmental Biology, vol. 27, pp. 107–132, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. B. Érdi, P. Nagy, Á. Zvara et al., “Loss of the starvation-induced gene Rack1 leads to glycogen deficiency and impaired autophagic responses in Drosophila,” Autophagy, vol. 8, no. 7, pp. 1124–1135, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. J. Kim, M. Kundu, B. Viollet, and K.-L. Guan, “AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1,” Nature Cell Biology, vol. 13, no. 2, pp. 132–141, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. D. J. Klionsky and B. A. Schulman, “Dynamic regulation of macroautophagy by distinctive ubiquitin-like proteins,” Nature Structural and Molecular Biology, vol. 21, no. 4, pp. 336–345, 2014. View at Google Scholar
  22. E. Itakura, C. Kishi-Itakura, and N. Mizushima, “The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes,” Cell, vol. 151, no. 6, pp. 1256–1269, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Hegedüs, S. Takáts, A. L. Kovács, and G. Juhász, “Evolutionarily conserved role and physiological relevance of a STX17/Syx17 (syntaxin 17)-containing SNARE complex in autophagosome fusion with endosomes and lysosomes,” Autophagy, vol. 9, no. 10, pp. 1642–1646, 2013. View at Google Scholar
  24. S. Takáts, P. Nagy, Á. Varga et al., “Autophagosomal Syntaxin17-dependent lysosomal degradation maintains neuronal function in Drosophila,” Journal of Cell Biology, vol. 201, no. 4, pp. 531–539, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. P. Jiang, T. Nishimura, Y. Sakamaki et al., “The HOPS complex mediates autophagosome-lysosome fusion through interaction with syntaxin 17,” Molecular Biology of the Cell, vol. 25, no. 8, pp. 1327–1337, 2014. View at Google Scholar
  26. S. Takats, K. Pircs, P. Nagy et al., “Interaction of the HOPS complex with Syntaxin 17 mediates autophagosome clearance in Drosophila,” Molecular Biology of the Cell, vol. 25, no. 8, pp. 1338–1354, 2014. View at Google Scholar
  27. V. Kirkin, D. G. McEwan, I. Novak, and I. Dikic, “A role for ubiquitin in selective autophagy,” Molecular Cell, vol. 34, no. 3, pp. 259–269, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Johansen and T. Lamark, “Selective autophagy goes exclusive,” Nature Cell Biology, vol. 16, no. 5, pp. 395–397, 2014. View at Google Scholar
  29. J. Sawa-Makarska, C. Abert, J. Romanov, B. Zens, I. Ibiricu, and S. Martens, “Cargo binding to Atg19 unmasks additional Atg8 binding sites to mediate membrane-cargo apposition during selective autophagy,” Nature Cell Biology, vol. 16, no. 5, pp. 425–433, 2014. View at Google Scholar
  30. N. Mizushima, T. Noda, T. Yoshimori et al., “A protein conjugation system essential for autophagy,” Nature, vol. 395, no. 6700, pp. 395–398, 1998. View at Publisher · View at Google Scholar · View at Scopus
  31. T. Kirisako, M. Baba, N. Ishihara et al., “Formation process of autophagosome is traced with Apg8/Aut7p in yeast,” Journal of Cell Biology, vol. 147, no. 2, pp. 435–446, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. Y. Ichimura, T. Kirisako, T. Takao et al., “A ubiquitin-like system mediates protein lipidation,” Nature, vol. 408, no. 6811, pp. 488–492, 2000. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Dengjel and H. Abeliovich, “Musical chairs during mitophagy,” Autophagy, vol. 10, no. 4, pp. 706–707, 2014. View at Google Scholar
  34. T. Lamark and T. Johansen, “Aggrephagy: selective disposal of protein aggregates by macroautophagy,” International Journal of Cell Biology, vol. 2012, Article ID 736905, 21 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. M. E. Pareja and M. I. Colombo, “Autophagic clearance of bacterial pathogens: molecular recognition of intracellular microorganisms,” Frontiers in Cellular and Infection Microbiology, vol. 3, article 54, 2013. View at Google Scholar
  36. T. Wileman, “Autophagy as a defence against intracellular pathogens,” Essays in Biochemistry, vol. 55, pp. 153–163, 2013. View at Google Scholar
  37. A. Till, R. Lakhani, S. F. Burnett, and S. Subramani, “Pexophagy: the selective degradation of peroxisomes,” International Journal of Cell Biology, vol. 2012, Article ID 512721, 18 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. T. Hara, K. Nakamura, M. Matsui et al., “Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice,” Nature, vol. 441, no. 7095, pp. 885–889, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Komatsu, S. Waguri, T. Chiba et al., “Loss of autophagy in the central nervous system causes neurodegeneration in mice,” Nature, vol. 441, no. 7095, pp. 880–884, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. G. Juhász, B. Érdi, M. Sass, and T. P. Neufeld, “Atg7-dependent autophagy promotes neuronal health, stress tolerance, and longevity but is dispensable for metamorphosis in Drosophila,” Genes and Development, vol. 21, no. 23, pp. 3061–3066, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Pankiv, T. H. Clausen, T. Lamark et al., “p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy,” Journal of Biological Chemistry, vol. 282, no. 33, pp. 24131–24145, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Moscat and M. T. Diaz-Meco, “p62 at the crossroads of autophagy, apoptosis, and cancer,” Cell, vol. 137, no. 6, pp. 1001–1004, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. B. Ciani, R. Layfield, J. R. Cavey, P. W. Sheppard, and M. S. Searle, “Structure of the ubiquitin-associated domain of p62 (SQSTM1) and implications for mutations that cause Paget's disease of bone,” Journal of Biological Chemistry, vol. 278, no. 39, pp. 37409–37412, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Komatsu, S. Waguri, M. Koike et al., “Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice,” Cell, vol. 131, no. 6, pp. 1149–1163, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. I. P. Nezis, A. Simonsen, A. P. Sagona et al., “Ref(2)P, the Drosophila melanogaster homologue of mammalian p62, is required for the formation of protein aggregates in adult brain,” Journal of Cell Biology, vol. 180, no. 6, pp. 1065–1071, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. B. J. Bartlett, P. Isakson, J. Lewerenz et al., “p62, Ref(2)P and ubiquitinated proteins are conserved markers of neuronal aging, aggregate formation and progressive autophagic defects,” Autophagy, vol. 7, no. 6, pp. 572–583, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. D. J. Klionsky, F. C. Abdalla, H. Abeliovich et al., “Guidelines for the use and interpretation of assays for monitoring autophagy,” ,Autophagy, vol. 8, no. 4, pp. 445–544, 2012. View at Google Scholar
  48. N. Myeku and M. E. Figueiredo-Pereira, “Dynamics of the degradation of ubiquitinated proteins by proteasomes and autophagy: association with sequestosome 1/p62,” Journal of Biological Chemistry, vol. 286, no. 25, pp. 22426–22440, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. M. H. Sahani, E. Itakura, and N. Mizushima, “Expression of the autophagy substrate SQSTM1/p62 is restored during prolonged starvation depending on transcriptional upregulation and autophagy-derived amino acids,” Autophagy, vol. 10, no. 3, 2014. View at Google Scholar
  50. T. Lamark, M. Perander, H. Outzen et al., “Interaction codes within the family of mammalian Phox and Bem1p domain-containing proteins,” Journal of Biological Chemistry, vol. 278, no. 36, pp. 34568–34581, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. J. Zhou, J. Wang, Y. Cheng et al., “NBR1-mediated selective autophagy targets insoluble ubiquitinated protein aggregates in plant stress responses,” PLoS Genetics, vol. 9, no. 1, Article ID e1003196, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. K. Zientara-Rytter and A. Sirko, “Significant role of PB1 and UBA domains in multimerization of Joka2, a selective autophagy cargo receptor from tobacco,” Frontiers in Plant Science, vol. 5, article 13, 2014. View at Publisher · View at Google Scholar
  53. K. B. Boyle and F. Randow, “The role of “eat-me” signals and autophagy cargo receptors in innate immunity,” Current Opinion in Microbiology, vol. 16, no. 3, pp. 339–348, 2013. View at Publisher · View at Google Scholar · View at Scopus
  54. J. Korac, V. Schaeffer, I. Kovacevic et al., “Ubiquitin-independent function of optineurin in autophagic clearance of protein aggregates,” Journal of Cell Science, vol. 126, no. 2, pp. 580–592, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. C. Jo, S. Gundemir, S. Pritchard, Y. N. Jin, I. Rahman, and G. V. Johnson, “Nrf2 reduces levels of phosphorylated tau protein by inducing autophagy adaptor protein NDP52,” Nature Communications, vol. 5, article 3496, 2014. View at Google Scholar
  56. G. Zhu, C.-J. Wu, Y. Zhao, and J. D. Ashwell, “Optineurin negatively regulates TNFα-induced NF-κB activation by competing with NEMO for ubiquitinated RIP,” Current Biology, vol. 17, no. 16, pp. 1438–1443, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Inomata, S. Niida, K.-I. Shibata, and T. Into, “Regulation of toll-like receptor signaling by NDP52-mediated selective autophagy is normally inactivated by A20,” Cellular and Molecular Life Sciences, vol. 69, no. 6, pp. 963–979, 2012. View at Publisher · View at Google Scholar · View at Scopus
  58. I. Novak, “Mitophagy: a complex mechanism of mitochondrial removal,” Antioxidants and Redox Signaling, vol. 17, no. 5, pp. 794–802, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. J.-C. Farré, A. Burkenroad, S. F. Burnett, and S. Subramani, “Phosphorylation of mitophagy and pexophagy receptors coordinates their interaction with Atg8 and Atg11,” EMBO Reports, vol. 14, no. 5, pp. 441–449, 2013. View at Publisher · View at Google Scholar · View at Scopus
  60. I. Kalvari, S. Tsompanis, N. C. Mulakkal et al., “iLIR: a web resource for prediction of Atg8-family interacting proteins,” Autophagy, vol. 10, no. 5, pp. 913–925, 2014. View at Google Scholar
  61. V. Rogov, V. Dotsch, T. Johansen, and V. Kirkin, “Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy,” Molecular Cell, vol. 53, no. 2, pp. 167–178, 2014. View at Google Scholar
  62. N. Fujita, E. Morita, T. Itoh et al., “Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin,” Journal of Cell Biology, vol. 203, no. 1, pp. 115–128, 2013. View at Google Scholar
  63. P. Nagy, K. Hegedus, K. Pircs, A. Varga, and G. Juhasz, “Different effects of Atg2 and Atg18 mutations on Atg8a and Atg9 trafficking during starvation in Drosophila,” FEBS Letters, vol. 588, no. 3, pp. 408–413, 2014. View at Google Scholar
  64. S. V. Scott, D. C. Nice III, J. J. Nau et al., “Apg13p and Vac8p are part of a complex of phosphoproteins that are required for Cytoplasm to vacuole targeting,” Journal of Biological Chemistry, vol. 275, no. 33, pp. 25840–25849, 2000. View at Publisher · View at Google Scholar · View at Scopus
  65. P. Nagy, M. Karpati, A. Varga et al., “Atg17/FIP200 localizes to perilysosomal Ref(2)P aggregates and promotes autophagy by activation of Atg1 in Drosophila,” Autophagy, vol. 10, no. 3, pp. 453–467, 2014. View at Google Scholar
  66. J. Moscat and M. T. Diaz-Meco, “P62: a versatile multitasker takes on cancer,” Trends in Biochemical Sciences, vol. 37, no. 6, pp. 230–236, 2012. View at Publisher · View at Google Scholar · View at Scopus
  67. N. Hosokawa, T. Hara, T. Kaizuka et al., “Nutrient-dependent mTORCl association with the ULK1-Atg13-FIP200 complex required for autophagy,” Molecular Biology of the Cell, vol. 20, no. 7, pp. 1981–1991, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. Y. Sancak, L. Bar-Peled, R. Zoncu, A. L. Markhard, S. Nada, and D. M. Sabatini, “Ragulator-rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids,” Cell, vol. 141, no. 2, pp. 290–303, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. G. Juhász, “Interpretation of bafilomycin, pH neutralizing or protease inhibitor treatments in autophagic flux experiments: novel considerations,” Autophagy, vol. 8, no. 12, pp. 1875–1876, 2012. View at Publisher · View at Google Scholar · View at Scopus
  70. E. A. Alemu, T. Lamark, K. M. Torgersen et al., “ATG8 family proteins act as scaffolds for assembly of the ULK complex: sequence requirements for LC3-interacting region (LIR) motifs,” Journal of Biological Chemistry, vol. 287, no. 47, pp. 39275–39290, 2012. View at Publisher · View at Google Scholar · View at Scopus
  71. K. Hegedüs, P. Nagy, Z. Gáspári, and G. Juhász, “The putative HORMA domain protein Atg101 dimerizes and is required for starvation-induced and selective autophagy in Drosophila,” BioMed Research International, vol. 2014, Article ID 470482, 13 pages, 2014. View at Publisher · View at Google Scholar
  72. A. Duran, R. Amanchy, J. F. Linares et al., “P62 is a key regulator of nutrient sensing in the mTORC1 pathway,” Molecular Cell, vol. 44, no. 1, pp. 134–146, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. L. Zhou, H.-F. Wang, H.-G. Ren et al., “Bcl-2-dependent upregulation of autophagy by sequestosome 1/p62 in vitro,” Acta Pharmacologica Sinica, vol. 34, no. 5, pp. 651–656, 2013. View at Publisher · View at Google Scholar · View at Scopus
  74. J. Yan, M. L. Seibenhener, L. Calderilla-Barbosa et al., “SQSTM1/p62 interacts with HDAC6 and regulates deacetylase activity,” PLoS ONE, vol. 8, no. 9, Article ID e76016, 2013. View at Google Scholar
  75. K. Nihira, Y. Miki, K. Ono, T. Suzuki, and H. Sasano, “An inhibition of p62/SQSTM1 caused autophagic cell death of several human carcinoma cells,” Cancer Science, vol. 105, no. 5, pp. 568–575, 2014. View at Google Scholar
  76. P. Low, Á. Varga, K. Pircs et al., “Impaired proteasomal degradation enhances autophagy via hypoxia signaling in Drosophila,” BMC Cell Biology, vol. 14, no. 1, article 29, 2013. View at Publisher · View at Google Scholar · View at Scopus
  77. S. Pankiv, T. Lamark, J.-A. Bruun, A. Øvervatn, G. Bjørkøy, and T. Johansen, “Nucleocytoplasmic shuttling of p62/SQSTM1 and its role in recruitment of nuclear polyubiquitinated proteins to promyelocytic leukemia bodies,” Journal of Biological Chemistry, vol. 285, no. 8, pp. 5941–5953, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. K. Pircs, P. Nagy, A. Varga et al., “Advantages and limitations of different p62-based assays for estimating autophagic activity in Drosophila,” PLoS ONE, vol. 7, no. 8, Article ID e44214, 2012. View at Publisher · View at Google Scholar · View at Scopus
  79. L. Sanz, P. Sanchez, M.-J. Lallena, M. T. Diaz-Meco, and J. Moscat, “The interaction of p62 with RIP links the atypical PKCs to NF-κB activation,” The EMBO Journal, vol. 18, no. 11, pp. 3044–3053, 1999. View at Publisher · View at Google Scholar · View at Scopus
  80. J. Y. Choe, H. Y. Jung, K. Y. Park, and S. K. Kim, “Enhanced p62 expression through impaired proteasomal degradation is involved in caspase-1 activation in monosodium urate crystal-induced interleukin-1beta expression,” Rheumatology, vol. 53, no. 6, pp. 1043–1053, 2014. View at Google Scholar
  81. S. Ohtsuka, Y. Ishii, M. Matsuyama et al., “SQSTM1/p62/A170 regulates the severity of Legionella pneumophila pneumonia by modulating inflammasome activity,” European Journal of Immunology, vol. 44, no. 4, pp. 1084–1092, 2014. View at Google Scholar
  82. M. W. Wooten, M. L. Seibenhener, V. Mamidipudi, M. T. Diaz-Meco, P. A. Barker, and J. Moscat, “The atypical protein kinase C-interacting protein p62 is a Scaffold for NF-κB activation by nerve growth factor,” Journal of Biological Chemistry, vol. 276, no. 11, pp. 7709–7712, 2001. View at Publisher · View at Google Scholar · View at Scopus
  83. A. Durán, M. Serrano, M. Leitges et al., “The atypical PKC-interacting protein p62 is an important mediator of RANK-activated osteoclastogenesis,” Developmental Cell, vol. 6, no. 2, pp. 303–309, 2004. View at Publisher · View at Google Scholar · View at Scopus
  84. N. Laurin, J. P. Brown, J. Morissette, and V. Raymond, “Recurrent mutation of the gene encoding sequestosome 1 (SQSTM1/p62) in paget disease of bone,” The American Journal of Human Genetics, vol. 70, no. 6, pp. 1582–1588, 2002. View at Publisher · View at Google Scholar · View at Scopus
  85. A. Duran, J. F. Linares, A. S. Galvez et al., “The signaling adaptor p62 is an important NF-κB mediator in tumorigenesis,” Cancer Cell, vol. 13, no. 4, pp. 343–354, 2008. View at Publisher · View at Google Scholar · View at Scopus
  86. A. Takeda-Watanabe, M. Kitada, K. Kanasaki, and D. Koya, “SIRT1 inactivation induces inflammation through the dysregulation of autophagy in human THP-1 cells,” Biochemical and Biophysical Research Communications, vol. 427, no. 1, pp. 191–196, 2012. View at Publisher · View at Google Scholar · View at Scopus
  87. C.-S. Shi, K. Shenderov, N.-N. Huang et al., “Activation of autophagy by inflammatory signals limits IL-1β production by targeting ubiquitinated inflammasomes for destruction,” Nature Immunology, vol. 13, no. 3, pp. 255–263, 2012. View at Publisher · View at Google Scholar · View at Scopus
  88. C.-P. Chang, Y.-C. Su, C.-W. Hu, and H.-Y. Lei, “TLR2-dependent selective autophagy regulates NF-κB lysosomal degradation in hepatoma-derived M2 macrophage differentiation,” Cell Death and Differentiation, vol. 20, no. 3, pp. 515–523, 2013. View at Publisher · View at Google Scholar · View at Scopus
  89. J. Shi, J. Wong, P. Piesik et al., “Cleavage of sequestosome 1/p62 by an enteroviral protease results in disrupted selective autophagy and impaired NFKB signaling,” Autophagy, vol. 9, no. 10, pp. 1591–1603, 2013. View at Google Scholar
  90. K.-I. Fujita and S. M. Srinivasula, “TLR4-mediated autophagy in macrophages is a p62-dependent type of selective autophagy of aggresome-like induced structures (ALIS),” Autophagy, vol. 7, no. 5, pp. 552–554, 2011. View at Publisher · View at Google Scholar · View at Scopus
  91. M. Ponpuak, A. S. Davis, E. A. Roberts et al., “Delivery of cytosolic components by autophagic adaptor protein p62 endows autophagosomes with unique antimicrobial properties,” Immunity, vol. 32, no. 3, pp. 329–341, 2010. View at Publisher · View at Google Scholar · View at Scopus
  92. Z. Jin, Y. Li, R. Pitti et al., “Cullin3-based polyubiquitination and p62-dependent aggregation of caspase-8 mediate extrinsic apoptosis signaling,” Cell, vol. 137, no. 4, pp. 721–735, 2009. View at Publisher · View at Google Scholar · View at Scopus
  93. M. M. Young, Y. Takahashi, O. Khan et al., “Autophagosomal membrane serves as platform for intracellular death-inducing signaling complex (iDISC)-mediated caspase-8 activation and apoptosis,” Journal of Biological Chemistry, vol. 287, no. 15, pp. 12455–12468, 2012. View at Publisher · View at Google Scholar · View at Scopus
  94. J. R. Kovacs, C. Li, Q. Yang et al., “Autophagy promotes T-cell survival through degradation of proteins of the cell death machinery,” Cell Death and Differentiation, vol. 19, no. 1, pp. 144–152, 2012. View at Publisher · View at Google Scholar · View at Scopus
  95. S. Huang, K. Okamoto, C. Yu, and F. A. Sinicrope, “p62/sequestosome-1 up-regulation promotes ABT-263-induced caspase-8 aggregation/activation on the autophagosome,” Journal of Biological Chemistry, vol. 288, no. 47, pp. 33654–33666, 2013. View at Google Scholar
  96. M. Komatsu, H. Kurokawa, S. Waguri et al., “The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1,” Nature Cell Biology, vol. 12, no. 3, pp. 213–223, 2010. View at Publisher · View at Google Scholar · View at Scopus
  97. A. Jain, T. Lamark, E. Sjøttem et al., “p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription,” Journal of Biological Chemistry, vol. 285, no. 29, pp. 22576–22591, 2010. View at Publisher · View at Google Scholar · View at Scopus
  98. T. Ishii, K. Itoh, S. Takahashi et al., “Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages,” Journal of Biological Chemistry, vol. 275, no. 21, pp. 16023–16029, 2000. View at Publisher · View at Google Scholar · View at Scopus
  99. K. Taguchi, N. Fujikawa, M. Komatsu et al., “Keap1 degradation by autophagy for the maintenance of redox homeostasis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 34, pp. 13561–13566, 2012. View at Publisher · View at Google Scholar · View at Scopus
  100. S. H. Bae, S. H. Sung, S. Y. Oh et al., “Sestrins activate Nrf2 by promoting p62-dependent autophagic degradation of keap1 and prevent oxidative liver damage,” Cell Metabolism, vol. 17, no. 1, pp. 73–84, 2013. View at Publisher · View at Google Scholar · View at Scopus
  101. Y. Ichimura, S. Waguri, Y.-S. Sou et al., “Phosphorylation of p62 activates the Keap1-Nrf2 pathway during selective autophagy,” Molecular Cell, vol. 51, no. 5, pp. 618–631, 2013. View at Publisher · View at Google Scholar · View at Scopus
  102. G. Nalepa, M. Rolfe, and J. W. Harper, “Drug discovery in the ubiquitin: proteasome system,” Nature Reviews Drug Discovery, vol. 5, no. 7, pp. 596–613, 2006. View at Publisher · View at Google Scholar · View at Scopus
  103. T. Ravid and M. Hochstrasser, “Diversity of degradation signals in the ubiquitin-proteasome system,” Nature Reviews Molecular Cell Biology, vol. 9, no. 9, pp. 679–689, 2008. View at Publisher · View at Google Scholar · View at Scopus
  104. S. P. Tully, T. M. Stitt, R. D. Caldwell, B. J. Hardock, R. M. Hanson, and P. Maslak, “Interactive web-based pointillist visualization of hydrogenic orbitals using jmol,” Journal of Chemical Education, vol. 90, no. 1, pp. 129–131, 2013. View at Publisher · View at Google Scholar · View at Scopus
  105. S. Vijay-kumar, C. E. Bugg, and W. J. Cook, “Structure of ubiquitin refined at 1.8 Å resolution,” Journal of Molecular Biology, vol. 194, no. 3, pp. 531–544, 1987. View at Google Scholar · View at Scopus
  106. C. Otomo, Z. Metlagel, G. Takaesu, and T. Otomo, “Structure of the human ATG12~ATG5 conjugate required for LC3 lipidation in autophagy,” Nature Structural and Molecular Biology, vol. 20, no. 1, pp. 59–66, 2013. View at Publisher · View at Google Scholar · View at Scopus
  107. K. Sugawara, N. N. Suzuki, Y. Fujioka, N. Mizushima, Y. Ohsumi, and F. Inagaki, “The crystal structure of microtubule-associated protein light chain 3, a mammalian homologue of Saccharomyces cerevisiae Atg8,” Genes to Cells, vol. 9, no. 7, pp. 611–618, 2004. View at Publisher · View at Google Scholar · View at Scopus