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BioMed Research International
Volume 2015 (2015), Article ID 319454, 13 pages
http://dx.doi.org/10.1155/2015/319454
Research Article

Prohibitin: A Novel Molecular Player in KDEL Receptor Signalling

1Department of Cellular and Translational Pharmacology, Fondazione Mario Negri Sud, 66030 Santa Maria Imbaro, Italy
2Department of Cell Biology & Signalling, The FIRC Institute of Molecular Oncology (IFOM), 20139 Milan, Italy
3Proteomic Core Facility, Fondazione Mario Negri Sud, 66030 Santa Maria Imbaro, Italy
4Institute of Protein Biochemistry, National Research Council and Telethon Institute of Genetics and Medicine, 80131 Naples, Italy

Received 5 December 2014; Accepted 14 April 2015

Academic Editor: Christian Appenzeller-Herzog

Copyright © 2015 Monica Giannotta 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. M. J. Lewis and H. R. B. Pelham, “A human homologue of the yeast HDEL receptor,” Nature, vol. 348, no. 6297, pp. 162–163, 1990. View at Publisher · View at Google Scholar · View at Scopus
  2. M. J. Lewis and H. R. B. Pelham, “Sequence of a second human KDEL receptor,” Journal of Molecular Biology, vol. 226, no. 4, pp. 913–916, 1992. View at Publisher · View at Google Scholar · View at Scopus
  3. V. W. Hsu, N. Shah, and R. D. Klausner, “A brefeldin A-like phenotype is induced by the overexpression of a human ERD-2-like protein, ELP-1,” Cell, vol. 69, no. 4, pp. 625–635, 1992. View at Publisher · View at Google Scholar · View at Scopus
  4. J. E. Collins, C. L. Wright, C. A. Edwards et al., “A genome annotation-driven approach to cloning the human ORFeome,” Genome Biology, vol. 5, no. 10, p. R84, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. J. C. Semenza, K. G. Hardwick, N. Dean, and H. R. B. Pelham, “ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway,” Cell, vol. 61, no. 7, pp. 1349–1357, 1990. View at Publisher · View at Google Scholar · View at Scopus
  6. A. A. Scheel and H. R. B. Pelham, “Identification of amino acids in the binding pocket of the human KDEL receptor,” The Journal of Biological Chemistry, vol. 273, no. 4, pp. 2467–2472, 1998. View at Publisher · View at Google Scholar · View at Scopus
  7. F. M. Townsley, D. W. Wilson, and H. R. B. Pelham, “Mutational analysis of the human KDEL receptor: distinct structural requirements for Golgi retention, ligand binding and retrograde transport,” The EMBO Journal, vol. 12, no. 7, pp. 2821–2829, 1993. View at Google Scholar · View at Scopus
  8. K. Yamamoto, H. Hamada, H. Shinkai, Y. Kohno, H. Koseki, and T. Aoe, “The KDEL receptor modulates the endoplasmic reticulum stress response through mitogen-activated protein kinase signaling cascades,” The Journal of Biological Chemistry, vol. 278, no. 36, pp. 34525–34532, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. P. Wang, B. Li, L. Zhou, E. Fei, and G. Wang, “The KDEL receptor induces autophagy to promote the clearance of neurodegenerative disease-related proteins,” Neuroscience, vol. 190, pp. 43–55, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. T. Pulvirenti, M. Giannotta, M. Capestrano et al., “A traffic-activated Golgi-based signalling circuit coordinates the secretory pathway,” Nature Cell Biology, vol. 10, no. 8, pp. 912–922, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Giannotta, C. Ruggiero, M. Grossi et al., “The KDEL receptor couples to Gαq/11 to activate Src kinases and regulate transport through the Golgi,” The EMBO Journal, vol. 31, no. 13, pp. 2869–2881, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. D. T. Browman, M. B. Hoegg, and S. M. Robbins, “The SPFH domain-containing proteins: more than lipid raft markers,” Trends in Cell Biology, vol. 17, no. 8, pp. 394–402, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. I. Chowdhury, W. E. Thompson, and K. Thomas, “Prohibitins role in cellular survival through Ras-Raf-MEK-ERK pathway,” Journal of Cellular Physiology, vol. 229, no. 8, pp. 998–1004, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Mishra, S. R. Ande, and B. L. G. Nyomba, “The role of prohibitin in cell signaling,” The FEBS Journal, vol. 277, no. 19, pp. 3937–3946, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. I. Chowdhury, W. Xu, J. K. Stiles et al., “Apoptosis of rat granulosa cells after staurosporine and serum withdrawal is suppressed by adenovirus-directed overexpression of prohibitin,” Endocrinology, vol. 148, no. 1, pp. 206–217, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. C.-F. Chiu, M.-Y. Ho, J.-M. Peng et al., “Raf activation by Ras and promotion of cellular metastasis require phosphorylation of prohibitin in the raft domain of the plasma membrane,” Oncogene, vol. 32, no. 6, pp. 777–787, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. L. G. J. Nijtmans, M. Artal Sanz, L. A. Grivell, and P. J. Coates, “The mitochondrial PHB complex: roles in mitochondrial respiratory complex assembly, ageing and degenerative disease,” Cellular and Molecular Life Sciences, vol. 59, no. 1, pp. 143–155, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. V. Emerson, D. Holtkotte, T. Pfeiffer et al., “Identification of the cellular prohibitin 1/prohibitin 2 heterodimer as an interaction partner of the C-terminal cytoplasmic domain of the HIV-1 glycoprotein,” Journal of Virology, vol. 84, no. 3, pp. 1355–1365, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. K. Rajalingam and T. Rudel, “Ras-Raf signaling needs prohibitin,” Cell Cycle, vol. 4, no. 11, pp. 1503–1505, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. Y.-J. Wang, X.-L. Guo, S.-A. Li et al., “Prohibitin is involved in the activated internalization and degradation of protease-activated receptor 1,” Biochimica et Biophysica Acta: Molecular Cell Research, vol. 1843, no. 7, pp. 1393–1401, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. E. K.-H. Han, T. McGonigal, C. Butler, V. L. Giranda, and Y. Luo, “Characterization of Akt overexpression in MiaPaCa-2 cells: prohibitin is an Akt substrate both in vitro and in cells,” Anticancer Research, vol. 28, no. 2, pp. 957–963, 2008. View at Google Scholar · View at Scopus
  22. S. R. Ande, Y. Gu, B. L. G. Nyomba, and S. Mishra, “Insulin induced phosphorylation of prohibitin at tyrosine114 recruits Shp1,” Biochimica et Biophysica Acta—Molecular Cell Research, vol. 1793, no. 8, pp. 1372–1378, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. V. Sánchez-Quiles, E. Santamaría, V. Segura, L. Sesma, J. Prieto, and F. J. Corrales, “Prohibitin deficiency blocks proliferation and induces apoptosis in human hepatoma cells: molecular mechanisms and functional implications,” Proteomics, vol. 10, no. 9, pp. 1609–1620, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Aoe, E. Cukierman, A. Lee, D. Cassel, P. J. Peters, and V. W. Hsu, “The KDEL receptor, ERD2, regulates intracellular traffic by recruiting a GTPase-activating protein for ARF1,” EMBO Journal, vol. 16, no. 24, pp. 7305–7316, 1997. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Cancino, A. Capalbo, A. Di Campli et al., “Control systems of membrane transport at the interface between the endoplasmic reticulum and the Golgi,” Developmental Cell, vol. 30, no. 3, pp. 280–294, 2014. View at Publisher · View at Google Scholar
  26. J. Lippincott-Schwartz, J. G. Donaldson, A. Schweizer et al., “Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway,” Cell, vol. 60, no. 5, pp. 821–836, 1990. View at Publisher · View at Google Scholar · View at Scopus
  27. L. G. J. Nijtmans, L. de Jong, M. A. Sanz et al., “Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins,” The EMBO Journal, vol. 19, no. 11, pp. 2444–2451, 2000. View at Publisher · View at Google Scholar · View at Scopus
  28. N. Dean and H. R. B. Pelham, “Recycling of proteins from the Golgi compartment to the ER in yeast,” Journal of Cell Biology, vol. 111, no. 2, pp. 369–377, 1990. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Capitani and M. Sallese, “The KDEL receptor: new functions for an old protein,” FEBS Letters, vol. 583, no. 23, pp. 3863–3871, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. H. R. B. Pelham, “The retention signal for soluble proteins of the endoplasmic reticulum,” Trends in Biochemical Sciences, vol. 15, no. 12, pp. 483–486, 1990. View at Publisher · View at Google Scholar · View at Scopus
  31. M. J. Lewis and H. R. B. Pelham, “Ligand-induced redistribution of a human KDEL receptor from the Golgi complex to the endoplasmic reticulum,” Cell, vol. 68, no. 2, pp. 353–364, 1992. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Satoh, K. Hirayoshi, S.-I. Yokota, N. Hosokawa, and K. Nagata, “Intracellular interaction of collagen-specific stress protein HSP47 with newly synthesized procollagen,” Journal of Cell Biology, vol. 133, no. 2, pp. 469–483, 1996. View at Publisher · View at Google Scholar · View at Scopus
  33. V. Saudek, “Cystinosin, MPDU1, SWEETs and KDELR belong to a well-defined protein family with putative function of cargo receptors involved in vesicle trafficking,” PLoS ONE, vol. 7, no. 2, Article ID e30876, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. D. C. Yee, M. A. Shlykov, Å. Västermark et al., “The transporter-opsin-G protein-coupled receptor (TOG) superfamily,” FEBS Journal, vol. 280, no. 22, pp. 5780–5800, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. Zhai, W. H. M. Heijne, D. W. Smith, and M. H. Saier Jr., “Homologues of archaeal rhodopsins in plants, animals and fungi: structural and functional predications for a putative fungal chaperone protein,” Biochimica et Biophysica Acta—Biomembranes, vol. 1511, no. 2, pp. 206–223, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. M. L. Villasmil and J. T. Nickels Jr., “Determination of the membrane topology of Arv1 and the requirement of the ER luminal region for Arv1 function in Saccharomyces cerevisiae,” FEMS Yeast Research, vol. 11, no. 6, pp. 524–527, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. D. A. Stroud, S. Oeljeklaus, S. Wiese et al., “Composition and topology of the endoplasmic reticulum-mitochondria encounter structure,” Journal of Molecular Biology, vol. 413, no. 4, pp. 743–750, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. F. Faulhammer, G. Konrad, B. Brankatschk, S. Tahirovic, A. Knödler, and P. Mayinger, “Cell growth-dependent coordination of lipid signaling and glycosylation is mediated by interactions between Sac1p and Dpm1p,” Journal of Cell Biology, vol. 168, no. 2, pp. 185–191, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. Z. Zheng and J. Zou, “The initial step of the glycerolipid pathway: identification of glycerol 3-phosphate/dihydroxyacetone phosphate dual substrate acyltransferases in Saccharomyces cerevisiae,” The Journal of Biological Chemistry, vol. 276, no. 45, pp. 41710–41716, 2001. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Schuldiner, S. R. Collins, N. J. Thompson et al., “Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile,” Cell, vol. 123, no. 3, pp. 507–519, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. I. Majoul, M. Straub, S. W. Hell, R. Duden, and H.-D. Söling, “KDEL-cargo regulates interactions between proteins involved in COPI vesicle traffic: measurements in living cells using FRET,” Developmental Cell, vol. 1, no. 1, pp. 139–153, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. H. Kojima, H. Hashimoto, and K. Yoda, “Interaction among the subunits of Golgi membrane mannosyltransferase complexes of the yeast Saccharomyces cerevisiae,” Bioscience, Biotechnology and Biochemistry, vol. 63, no. 11, pp. 1970–1976, 1999. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Zhao, J. Du, B. Xiong, H. Xu, and L. Jiang, “ESCRT components regulate the expression of the ER/Golgi calcium pump gene PMR1 through the Rim101/Nrg1 pathway in budding yeast,” Journal of Molecular Cell Biology, vol. 5, no. 5, pp. 336–344, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. G. Polier, J. Neumann, F. Thuaud et al., “The natural anticancer compounds rocaglamides inhibit the Raf-MEK-ERK pathway by targeting prohibitin 1 and 2,” Chemistry and Biology, vol. 19, no. 9, pp. 1093–1104, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. P. Marra, T. Maffucci, T. Daniele et al., “The GM130 and GRASP65 golgi proteins cycle through and define a subdomain of the intermediate compartment,” Nature Cell Biology, vol. 3, no. 12, pp. 1101–1113, 2001. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Shevchenko, “Evaluation of the efficiency of in-gel digestion of proteins by peptide isotopic labeling and MALDI mass spectrometry,” Analytical Biochemistry, vol. 296, no. 2, pp. 279–283, 2001. View at Publisher · View at Google Scholar · View at Scopus