Selenoprotein S-dependent selenoprotein K binding to p97(VCP) protein is essential for endoplasmic reticulum-associated degradation

Journal of Biological Chemistry

Volumn 290, Issue 50, 2015, Pages 29941-29952

  Lee, Jea Hwang ^a   Park, Ki Jun ^a   Jang, Jun Ki ^a   Jeon, Yeong Ha ^a   Ko, Kwan Young ^a   Kwon, Joon Hyun ^a,c   Lee, Seung Rock ^b   Kim, Ick Young ^a  

^a Korea University   (South Korea)

^b Chonnam National University Medical School   (South Korea)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; BIOLOGICAL MEMBRANES; CELL MEMBRANES; PROTEINS;

CO-PRECIPITATED; CYTOSOLIC; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATIONS; HEK293 CELLS; MEMBRANE PROTEINS; N2A CELLS; REGULATORY MECHANISM; SELENOPROTEINS;

MEMBRANES;

ADENOSINE TRIPHOSPHATASE; CDC48 PROTEIN; CELL CYCLE PROTEIN; MEMBRANE PROTEIN; PROTEIN BINDING; SELENOPROTEIN; SELENOPROTEIN K, MOUSE; VIMP PROTEIN, HUMAN;

ANIMAL; CELL LINE; ENDOPLASMIC RETICULUM; HUMAN; METABOLISM; MOUSE;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CELL CYCLE PROTEINS; CELL LINE; ENDOPLASMIC RETICULUM; HUMANS; MEMBRANE PROTEINS; MICE; PROTEIN BINDING; SELENOPROTEINS;

EID: 84949662465     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.680215     Document Type: Article

References (50)

1. Kleizen, B., and Braakman, I. (2004) Protein folding and quality control in the endoplasmic reticulum. Curr. Opin. Cell Biol. 16, 343-349
2. Ellgaard, L., and Helenius, A. (2003) Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 4, 181-191
3. Römisch, K. (2005) Endoplasmic reticulum-associated degradation. Annu. Rev. Cell Dev. Biol. 21, 435-456
4. Kostova, Z., and Wolf, D. H. (2003) For whom the bell tolls: protein quality control of the endoplasmic reticulum and the ubiquitin-proteasome connection. EMBO J. 22, 2309-2317
5. Kaufman, R. J. (2002) Orchestrating the unfolded protein response in health and disease. J. Clin. Invest. 110, 1389-1398
6. Fu, S., Yang, L., Li, P., Hofmann, O., Dicker, L., Hide, W., Lin, X., Watkins, S. M., Ivanov, A. R., and Hotamisligil, G. S. (2011) Aberrant lipid metabolism disrupts calcium homeostasis causing liver endoplasmic reticulum stress in obesity. Nature 473, 528-531
7. Doroudgar, S., Völkers, M., Thuerauf, D. J., Khan, M., Mohsin, S., Respress, J. L., Wang, W., Gude, N., Müller, O. J., Wehrens, X. H., Sussman, M. A., and Glembotski, C. C. (2015) Hrd1 and ER-associated protein degradation, ERAD, are critical elements of the adaptive ER stress response in cardiac myocytes. Circ. Res. 117, 536-546
8. Yamanaka, K., Sasagawa, Y., and Ogura, T. (2012) Recent advances in p97/VCP/Cdc48 cellular functions. Biochim. Biophys. Acta 1823, 130-137
9. Ye, Y., Meyer, H. H., and Rapoport, T. A. (2001) The AAA ATPase Cdc48/ p97 and its partners transport proteins from the ER into the cytosol. Nature 414, 652-656
10. Meyer, H., Bug, M., and Bremer, S. (2012) Emerging functions of the VCP/p97 AAA-ATPase in the ubiquitin system. Nat. Cell Biol. 14, 117-123
11. Ewens, C. A., Kloppsteck, P., Förster, A., Zhang, X., and Freemont, P. S. (2010) Structural and functional implications of phosphorylation and acetylation in the regulation of the AAA+protein p97. Biochem. Cell Biol. 88, 41-48
12. Lee, J. H., Kwon, J. H., Jeon, Y. H., Ko, K. Y., Lee, S.-R., and Kim, I. Y. (2014) Pro-178 and Pro-183 of selenoprotein S Are essential residues for interaction with p97 (VCP) during endoplasmic reticulum-associated degradation. J. Biol. Chem. 289, 13758-13768
13. Ballar, P., Shen, Y., Yang, H., and Fang, S. (2006) The role of a novel p97/valosin-containing protein-interacting motif of gp78 in endoplasmic reticulum-associated degradation. J. Biol. Chem. 281, 35359-35368
14. Ballar, P., Pabuccuoglu, A., and Kose, F. A. (2011) Different p97/VCP complexes function in retrotranslocation step of mammalian ER-associated degradation (ERAD). Int. J. Biochem. Cell Biol. 43, 613-621
15. Wójcik, C., Rowicka, M., Kudlicki, A., Nowis, D., McConnell, E., Kujawa, M., and DeMartino, G. N. (2006) Valosin-containing protein (p97) is a regulator of endoplasmic reticulum stress and of the degradation of N-end rule and ubiquitin-fusion degradation pathway substrates in mammalian cells. Mol. Biol. Cell 17, 4606-4618
16. Lilley, B. N., and Ploegh, H. L. (2005) Multiprotein complexes that link dislocation, ubiquitination, and extraction of misfolded proteins from the endoplasmic reticulum membrane. Proc. Natl. Acad. Sci. U.S.A. 102, 14296-14301
17. Shchedrina, V. A., Zhang, Y., Labunskyy, V. M., Hatfield, D. L., and Gladyshev, V. N. (2010) Structure-function relations, physiological roles, and evolution of mammalian ER-resident selenoproteins. Antioxid. Redox Signal. 12, 839-849
18. Lee, J. J., Park, J. K., Jeong, J., Jeon, H., Yoon, J. B., Kim, E. E., and Lee, K. J. (2013) Complex of Fas-associated factor 1 (FAF1) with valosin-containing protein (VCP)-Npl4-Ufd1 and polyubiquitinated proteins promotes endoplasmic reticulum-associated degradation (ERAD). J. Biol. Chem. 288, 6998-7011
19. Yang, M., Omura, S., Bonifacino, J. S., and Weissman, A. M. (1998) Novel aspects of degradation of T cell receptor subunits from the endoplasmic reticulum (ER) in T cells: importance of oligosaccharide processing, ubiquitination, and proteasome-dependent removal from ER membranes. J. Exp. Med. 187, 835-846
20. Zhong, X., Shen, Y., Ballar, P., Apostolou, A., Agami, R., and Fang, S. (2004) AAA ATPase p97/valosin-containing protein interacts with gp78, a ubiquitin ligase for endoplasmic reticulum-associated degradation. J. Biol. Chem. 279, 45676-45684
21. Kryukov, G. V., Castellano, S., Novoselov, S. V., Lobanov, A. V., Zehtab, O., Guigó, R., and Gladyshev, V. N. (2003) Characterization of mammalian selenoproteomes. Science 300, 1439-1443
22. Arnér, E. S. (2010) Selenoproteins: what unique properties can arise with selenocysteine in place of cysteine? Exp. Cell Res. 316, 1296-1303
23. Christensen, L. C., Jensen, N. W., Vala, A., Kamarauskaite, J., Johansson, L., Winther, J. R., Hofmann, K., Teilum, K., and Ellgaard, L. (2012) The human selenoprotein VCP-interacting membrane protein (VIMP) is nonglobular and harbors a reductase function in an intrinsically disordered region. J. Biol. Chem. 287, 26388-26399
24. Shchedrina, V. A., Everley, R. A., Zhang, Y., Gygi, S. P., Hatfield, D. L., and Gladyshev, V. N. (2011) Selenoprotein K binds multiprotein complexes and is involved in the regulation of endoplasmic reticulum homeostasis. J. Biol. Chem. 286, 42937-42948
25. Liu, J., Srinivasan, P., Pham, D. N., and Rozovsky, S. (2012) Expression and purification of the membrane enzyme selenoprotein K. Protein Expr. Purif. 86, 27-34
26. Gao, Y., Feng, H. C., Walder, K., Bolton, K., Sunderland, T., Bishara, N., Quick, M., Kantham, L., and Collier, G. R. (2004) Regulation of the selenoprotein SelS by glucose deprivation and endoplasmic reticulum stress: SelS is a novel glucose-regulated protein. FEBS Lett. 563, 185-190
27. Du, S., Zhou, J., Jia, Y., and Huang, K. (2010) SelK is a novel ER stressregulated protein and protects HepG2 cells from ER stress agent-induced apoptosis. Arch. Biochem. Biophys. 502, 137-143
28. Kim, K. H., Gao, Y., Walder, K., Collier, G. R., Skelton, J., and Kissebah, A. H. (2007) SEPS1 protects RAW264.7 cells from pharmacological ER stress agent-induced apoptosis. Biochem. Biophys. Res. Commun. 354, 127-132
29. Min, K. W., Hwang, J. W., Lee, J. S., Park, Y., Tamura, T. A., and Yoon, J. B. (2003) TIP120A associates with cullins and modulates ubiquitin ligase activity. J. Biol. Chem. 278, 15905-15910
30. Jeon, Y. H., Park, Y. H., Kwon, J. H., Lee, J. H., and Kim, I. Y. (2013) Inhibition of 14-3-3 binding to Rictor of mTORC2 for Akt phosphorylation at Ser473 is regulated by selenoprotein W. Biochim. Biophys. Acta 1833, 2135-2142
31. Jeon, Y. H., Park, Y. H., Lee, J. H., Hong, J. H., and Kim, I. Y. (2014) Selenoprotein W enhances skeletal muscle differentiation by inhibiting TAZ binding to 14-3-3 protein. Biochim. Biophys. Acta 1843, 1356-1364
32. Kim, K. S., Choi, H. W., Yoon, H. E., and Kim, I. Y. (2010) Reactive oxygen species generated by NADPH oxidase 2 and 4 are required for chondrogenic differentiation. J. Biol. Chem. 285, 40294-40302
33. Kwon, J. H., Lee, J. H., Kim, K. S., Chung, Y. W., and Kim, I. Y. (2012) Regulation of cytosolic phospholipase A2 phosphorylation by proteolytic cleavage of annexin A1 in activated mast cells. J. Immunol. 188, 5665-5673
34. Kim, S. J., Cho, J., Song, E. J., Kim, S. J., Kim, H. M., Lee, K. E., Suh, S. W., and Kim, E. E. (2014) Structural basis for ovarian tumor domain-containing protein 1 (OTU1) binding to p97/valosin-containing protein (VCP). J. Biol. Chem. 289, 12264-12274
35. Park, Y. H., Jeon, Y. H., and Kim, I. Y. (2012) Selenoprotein W promotes cell cycle recovery from G2 arrest through the activation of CDC25B. Biochim. Biophys. Acta 1823, 2217-2226
36. Du, S., Liu, H., and Huang, K. (2010) Influence of SelS gene silence on β-mercaptoethanol-mediated endoplasmic reticulum stress and cell apoptosis in HepG2 cells. Biochim. Biophys. Acta 1800, 511-517
37. Rabinovich, E., Kerem, A., Fröhlich, K. U., Diamant, N., and Bar-Nun, S. (2002) AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation. Mol. Cell. Biol. 22, 626-634
38. Ye, Y., Meyer, H. H., and Rapoport, T. A. (2003) Function of the p97-Ufd1-Npl4 complex in retrotranslocation from the ER to the cytosol: dual recognition of nonubiquitinated polypeptide segments and polyubiquitin chains. J. Cell Biol. 162, 71-84
39. Turanov, A. A., Shchedrina, V. A., Everley, R. A., Lobanov, A. V., Yim, S. H., Marino, S. M., Gygi, S. P., Hatfield, D. L., and Gladyshev, V. N. (2014) Selenoprotein S is involved in maintenance and transport of multiprotein complexes. Biochem. J. 462, 555-565
40. Liu, J., and Rozovsky, S. (2013) Contribution of selenocysteine to the peroxidase activity of selenoprotein S. Biochemistry 52, 5514-5516
41. Marciniak, S. J., and Ron, D. (2006) Endoplasmic reticulum stress signaling in disease. Physiol. Rev. 86, 1133-1149
42. Ye, Y., Shibata, Y., Yun, C., Ron, D., and Rapoport, T. A. (2004) A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature 429, 841-847
43. Labunskyy, V. M., Hatfield, D. L., and Gladyshev, V. N. (2014) Selenoproteins: molecular pathways and physiological roles. Physiol. Rev. 94, 739-777
44. Kondo, H., Rabouille, C., Newman, R., Levine, T. P., Pappin, D., Freemont, P., and Warren, G. (1997) p47 is a cofactor for p97-mediated membrane fusion. Nature 388, 75-78
45. Meyer, H. H., Shorter, J. G., Seemann, J., Pappin, D., and Warren, G. (2000) A complex of mammalian ufd1 and npl4 links the AAA-ATPase, p97, to ubiquitin and nuclear transport pathways. EMBO J. 19, 2181-2192
46. Lemus, L., and Goder, V. (2014) Regulation of endoplasmic reticulumassociated protein degradation (ERAD) by ubiquitin. Cells 3, 824-847
47. Kögel, D., Schomburg, R., Schürmann, T., Reimertz, C., König, H. G., Poppe, M., Eckert, A., Müller, W. E., and Prehn, J. H. (2003) The amyloid precursor protein protects PC12 cells against endoplasmic reticulum stress-induced apoptosis. J. Neurochem. 87, 248-256
48. Noda, C., Kimura, H., Arasaki, K., Matsushita, M., Yamamoto, A., Wakana, Y., Inoue, H., and Tagaya, M. (2014) Valosin-containing proteininteracting membrane protein (VIMP) links the endoplasmic reticulum with microtubules in concert with cytoskeleton-linking membrane protein (CLIMP)-63. J. Biol. Chem. 289, 24304-24313
49. Kim, C. Y., and Kim, K. H. (2013) Dexamethasone-induced selenoprotein S degradation is required for adipogenesis. J. Lipid Res. 54, 2069-2082
50. Verma, S., Hoffmann, F. W., Kumar, M., Huang, Z., Roe, K., Nguyen-Wu, E., Hashimoto, A. S., and Hoffmann, P. R. (2011) Selenoprotein K knockout mice exhibit deficient calcium flux in immune cells and impaired immune responses. J. Immunol. 186, 2127-2137