Ube2g2-gp78-mediated HERP polyubiquitylation is involved in ER stress recovery

Journal of Cell Science

Volumn 127, Issue 7, 2014, Pages 1417-1427

  Yan, Long ^a   Liu, Weixiao ^a   Zhang, Huihui ^b   Liu, Chao ^a   Shang, Yongliang ^a   Ye, Yihong ^c   Zhang, Xiaodong ^b   Li, Wei ^b  

^a INSTITUTE OF ZOOLOGY   (China)

^b WUHAN UNIVERSITY   (China)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

ER stress recovery; HERP; Trade off; Ube2g2 gp78; Ubiquitin proteasome system

Indexed keywords

CHAPERONE; HOMOCYSTEINE INDUCED ENDOPLASMIC RETICULUM PROTEIN; PROTEASOME; PROTEIN; PROTEIN GP78; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN CONJUGATING ENZYME E2 G2; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; HERPUD1 PROTEIN, HUMAN; HERPUD1 PROTEIN, MOUSE; MEMBRANE PROTEIN; UBE2G2 PROTEIN, HUMAN; UBE2G2 PROTEIN, MOUSE;

ARTICLE; CELL FUNCTION; CELL STRAIN HCT116; CELL STRAIN HEK293; CELL SURVIVAL; CELL VIABILITY; COMPLEX FORMATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; HELA CELL; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR BIOLOGY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION; ANIMAL; CELL CULTURE; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY;

ANIMALS; CELLS, CULTURED; ENDOPLASMIC RETICULUM STRESS; HUMANS; MEMBRANE PROTEINS; MICE; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINATION;

EID: 84897469420     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.135293     Document Type: Article

References (52)

1. Ackerman, D. and Gems, D. (2012). Insulin/IGF-1 and hypoxia signaling act in concert to regulate iron homeostasis in Caenorhabditis elegans. PLoS Genet. 8, e1002498.
2. Bennett, A. F. and Lenski, R. E. (2007). An experimental test of evolutionary trade-offs during temperature adaptation. Proc. Natl. Acad. Sci. USA 104 Suppl. 1, 8649-8654.
3. Cao, J., Wang, J., Qi, W., Miao, H. H., Wang, J., Ge, L., DeBose-Boyd, R. A., Tang, J. J., Li, B. L. and Song, B. L. (2007). Ufd1 is a cofactor of gp78 and plays a key role in cholesterol metabolism by regulating the stability of HMGCoA reductase. Cell Metab. 6, 115-128.
4. Carroll, S. M. and Hampton, R. Y. (2010). Usa1p is required for optimal function and regulation of the Hrd1p endoplasmic reticulum-associated degradation ubiquitin ligase. J. Biol. Chem. 285, 5146-5156.
5. Carvalho, P., Stanley, A. M. and Rapoport, T. A. (2010). Retrotranslocation of a misfolded luminal ER protein by the ubiquitin-ligase Hrd1p. Cell 143, 579-591.
6. Casanueva, M. O., Burga, A. and Lehner, B. (2012). Fitness trade-offs and environmentallyinducedmutationbufferingin isogenicC. elegans.Science335,82-85.
7. Chau, V., Tobias, J. W., Bachmair, A., Marriott, D., Ecker, D. J., Gonda, D. K. and Varshavsky, A. (1989). A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243, 1576-1583.
8. Chen, B., Mariano, J., Tsai, Y. C., Chan, A. H., Cohen, M. and Weissman, A. M. (2006). The activity of a human endoplasmic reticulum-associated degradation E3, gp78, requires its Cue domain, RING finger, and an E2-binding site. Proc. Natl. Acad. Sci. USA 103, 341-346.
9. Donaldson, K. M., Yin, H., Gekakis, N., Supek, F. and Joazeiro, C. A. (2003). Ubiquitin signals protein trafficking via interaction with a novel ubiquitin binding domain in the membrane fusion regulator, Vps9p. Curr. Biol. 13, 258-262.
10. Ellgaard, L. and Helenius, A. (2001). ER quality control: towards an understanding at the molecular level. Curr. Opin. Cell Biol. 13, 431-437.
11. Fang, S., Ferrone, M., Yang, C., Jensen, J. P., Tiwari, S. and Weissman, A. M. (2001). The tumor autocrine motility factor receptor, gp78, is a ubiquitin protein ligase implicated in degradation from the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 98, 14422-14427.
12. Hori, O., Ichinoda, F., Yamaguchi, A., Tamatani, T., Taniguchi, M., Koyama, Y., Katayama, T., Tohyama, M., Stern, D. M., Ozawa, K. et al. (2004). Role of Herp in the endoplasmic reticulum stress response. Genes Cells 9, 457-469.
13. Ibarra, R. U., Edwards, J. S. and Palsson, B. O. (2002). Escherichia coli K-12 undergoes adaptive evolution to achieve in silico predicted optimal growth. Nature 420, 186-189.
14. Jarosch, E., Taxis, C., Volkwein, C., Bordallo, J., Finley, D., Wolf, D. H. and Sommer, T. (2002). Protein dislocation from the ER requires polyubiquitination and the AAA-ATPase Cdc48. Nat. Cell Biol. 4, 134-139.
15. Jin, J., Li, X., Gygi, S. P. and Harper, J. W. (2007). Dual E1 activation systems for ubiquitin differentially regulate E2 enzyme charging. Nature 447, 1135-1138.
16. Kamura, T., Sato, S., Iwai, K., Czyzyk-Krzeska, M., Conaway, R. C. and Conaway, J. W. (2000). Activation of HIF1 alpha ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex. Proc. Natl. Acad. Sci. USA 97, 10430-10435.
17. Kaufman, R. J. (1999). Stress signaling form the lumen of endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13, 1211-1233.
18. Kim, T. Y., Kim, E., Yoon, S. K. and Yoon, J. B. (2008). Herp enhances ERassociated protein degradation by recruiting ubiquilins. Biochem. Biophys. Res. Commun. 369, 741-746.
19. Kny, M., Standera, S., Hartmann-Petersen, R., Kloetzel, P. M. and Seeger, M. (2011). Herp regulates Hrd1-mediated ubiquitylation in a ubiquitin-like domaindependent manner. J. Biol. Chem. 286, 5151-5156.
20. Kokame, K., Agarwala, K. L., Kato, H. and Miyata, T. (2000). Herp, a new ubiquitin-like membrane protein induced by endoplasmic reticulum stress. J. Biol. Chem. 275, 32846-32853.
21. Kokame, K., Kato, H. and Miyata, T. (2001). Identification of ERSE-II, a new cisacting element responsible for the ATF6-dependent mammalian unfolded protein response. J. Biol. Chem. 276, 9199-9205.
22. Kostova, Z., Tsai, Y. C. and Weissman, A. M. (2007). Ubiquitin ligases, critical mediators of endoplasmic reticulum-associated degradation. Semin. Cell Dev. Biol. 18, 770-779.
23. Li, W., Tu, D., Brunger, A. T. and Ye, Y. (2007). A ubiquitin ligase transfers preformed polyubiquitin chains from a conjugating enzyme to a substrate. Nature 446, 333-337.
24. Li, W., Tu, D., Li, L., Wollert, T., Ghirlando, R., Brunger, A. T. and Ye, Y. (2009). Mechanistic insights into active site-associated polyubiquitination by the ubiquitin-conjugating enzyme Ube2g2. Proc. Natl. Acad. Sci. USA 106, 3722- 3727.
25. Majmundar, A. J., Wong, W. J. and Simon, M. C. (2010). Hypoxia-inducible factors and the response to hypoxic stress. Mol. Cell 40, 294-309.
26. Meloche, S. and Roux, P. P. (2012). F-box proteins elongate translation during stress recovery. Sci. Signal. 5, pe25
27. Mizushima, N. and Komatsu, M. (2011). Autophagy: renovation of cells and tissues. Cell 147, 728-741.
28. Mizushima, N., Yoshimori, T. and Levine, B. (2010). Methods in mammalian autophagy research. Cell 140, 313-326.
29. Monaghan, P., Metcalfe, N. B. and Torres, R. (2009). Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol. Lett. 12, 75-92.
30. Nogalska, A., Engel, W. K., McFerrin, J., Kokame, K., Komano, H. and Askanas, V. (2006). Homocysteine-induced endoplasmic reticulum protein (Herp) is up-regulated in sporadic inclusion-body myositis and in endoplasmic reticulum stress-induced cultured human muscle fibers. J. Neurochem. 96, 1491-1499.
31. Novak, M., Pfeiffer, T., Lenski, R. E., Sauer, U. and Bonhoeffer, S. (2006). Experimental tests for an evolutionary trade-off between growth rate and yield in E. coli. Am. Nat. 168, 242-251.
32. Okuda-Shimizu, Y. and Hendershot, L. M. (2007). Characterization of an ERAD pathway for nonglycosylated BiP substrates, which require Herp. Mol. Cell 28, 544-554.
33. Pickart, C. M. (2001). Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70, 503-533.
34. Qian, S. B., McDonough, H., Boellmann, F., Cyr, D. M. and Patterson, C. (2006). CHIP-mediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature 440, 551-555.
35. Roobol, A., Carden, M. J., Newsam, R. J. and Smales, C. M. (2009). Biochemical insights into the mechanisms central to the response of mammalian cells to cold stress and subsequent rewarming. FEBS J. 276, 286-302.
36. Rubel, C. E., Schisler, J. C., Hamlett, E. D., DeKroon, R. M., Gautel, M., Alzate, O. and Patterson, C. (2013). Diggin' on u(biquitin): a novel method for the identification of physiological E3 ubiquitin ligase substrates. Cell Biochem. Biophys. 67, 127-138.
37. Rubenstein, E. M., Kreft, S. G., Greenblatt, W., Swanson, R. and Hochstrasser, M. (2012). Aberrant substrate engagement of the ER translocon triggers degradation by the Hrd1 ubiquitin ligase. J. Cell Biol. 197, 761-773.
38. Rutkowski, D. T. and Kaufman, R. J. (2004). A trip to the ER: coping with stress. Trends Cell Biol. 14, 20-28.
39. Sai, X., Kawamura, Y., Kokame, K., Yamaguchi, H., Shiraishi, H., Suzuki, R., Suzuki, T., Kawaichi, M., Miyata, T., Kitamura, T. et al. (2002). Endoplasmic reticulum stress-inducible protein, Herp, enhances presenilin-mediated generation of amyloid beta-protein. J. Biol. Chem. 277, 12915-12920.
40. Sai, X., Kokame, K., Shiraishi, H., Kawamura, Y., Miyata, T., Yanagisawa, K. and Komano, H. (2003). The ubiquitin-like domain of Herp is involved in Herp degradation, but not necessary for its enhancement of amyloid β-protein generation. FEBS Lett. 553, 151-156.
41. Schröder, M. and Kaufman, R. J. (2005). The mammalian unfolded protein response. Annu. Rev. Biochem. 74, 739-789.
42. Schulze, A., Standera, S., Buerger, E., Kikkert, M., van Voorden, S., Wiertz, E., Koning, F., Kloetzel, P. M. and Seeger, M. (2005). The ubiquitin-domain protein HERP forms a complex with components of the endoplasmic reticulum associated degradation pathway. J. Mol. Biol. 354, 1021-1027.
43. Shen, X., Zhang, K. and Kaufman, R. J. (2004). The unfolded protein response - a stress signaling pathway of the endoplasmic reticulum. J. Chem. Neuroanat. 28, 79-92.
44. Shih, S. C., Prag, G., Francis, S. A., Sutanto, M. A., Hurley, J. H. and Hicke, L. (2003). A ubiquitin-binding motif required for intramolecular monoubiquitylation, the CUE domain. EMBO J. 22, 1273-1281.
45. Shmueli, A., Tsai, Y. C., Yang, M., Braun, M. A. and Weissman, A. M. (2009). Targeting of gp78 for ubiquitin-mediated proteasomal degradation by Hrd1: cross-talk between E3s in the endoplasmic reticulum. Biochem. Biophys. Res. Commun. 390, 758-762.
46. Shoval, O., Sheftel, H., Shinar, G., Hart, Y., Ramote, O., Mayo, A., Dekel, E., Kavanagh, K. and Alon, U. (2012). Evolutionary trade-offs, Pareto optimality and the geometry of phenotype space. Science 336, 1157-1160.
47. Spriggs, K. A., Bushell, M. and Willis, A. E. (2010). Translational regulation of gene expression during conditions of cell stress. Mol. Cell 40, 228-237.
48. Tuvia, S., Taglicht, D., Erez, O., Alroy, I., Alchanati, I., Bicoviski, V., Dori- Bachash, M., Ben-Avraham, D. and Reiss, Y. (2007). The ubiquitin E3 ligase POSH regulates calcium homeostasis through spatial control of Herp. J. Cell Biol. 177, 51-61.
49. Ye, Y. and Rape, M. (2009). Building ubiquitin chains: E2 enzymes at work. Nat. Rev. Mol. Cell Biol. 10, 755-764.
50. 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.
51. 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.
52. Zhang, P., Zhao, Y., Zhu, X., Sedwick, D., Zhang, X. and Wang, Z. (2011). Cross-talk between phospho-STAT3 and PLCγ1 plays plays a critical role in colorectal tumorigenesis. Mol. Cancer Res. 9, 1418-1428.