BAG6 regulates the quality control of a polytopic ERAD substrate

Journal of Cell Science

Volumn 127, Issue 13, 2014, Pages 2898-2909

  Payapilly, Aishwarya ^a   High, Stephen ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Degradation; Dominant negative; Endoplasmicreticulum associated degradation; Proteasome; Stabilisation; Ubiquitin

Indexed keywords

BCL 2 ASSOCIATED ANTHANOGENE 6 PROTEIN; CARRIER PROTEINS AND BINDING PROTEINS; UNCLASSIFIED DRUG; BAG6 PROTEIN, HUMAN; CHAPERONE; OPSIN; PROTEASOME; UBIQUITIN;

ARTICLE; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; GENE OVEREXPRESSION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN QUALITY; QUALITY CONTROL; STEADY STATE; UBIQUITINATION; GENETIC TRANSFECTION; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; SITE DIRECTED MUTAGENESIS;

ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; HELA CELLS; HUMANS; MOLECULAR CHAPERONES; MUTAGENESIS, SITE-DIRECTED; OPSINS; PROTEASOME ENDOPEPTIDASE COMPLEX; TRANSFECTION; UBIQUITIN;

EID: 84903780276     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.145565     Document Type: Article

References (41)

1. Adamus, G., Zam, Z. S., Arendt, A., Palczewski, K., McDowell, J. H. and Hargrave, P. A. (1991). Anti-rhodopsin monoclonal antibodies of defined specificity: characterization and application. Vision Res. 31, 17-31.
2. Akahane, T., Sahara, K., Yashiroda, H., Tanaka, K. and Murata, S. (2013). Involvement of Bag6 and the TRC pathway in proteasome assembly. Nat. Commun. 4, 2234.
3. Buchberger, A., Bukau, B. and Sommer, T. (2010). Protein quality control in the cytosol and the endoplasmic reticulum: brothers in arms. Mol. Cell 40, 238-252.
4. Burr, M. L., van den Boomen, D. J. H., Bye, H., Antrobus, R., Wiertz, E. J. and Lehner, P. J. (2013). MHC class I molecules are preferentially ubiquitinated on endoplasmic reticulum luminal residues during HRD1 ubiquitin E3 ligasemediated dislocation. Proc. Natl. Acad. Sci. USA 110, 14290-14295.
5. Claessen, J. H. L. and Ploegh, H. L. (2011). BAT3 guides misfolded glycoproteins out of the endoplasmic reticulum. PLoS ONE 6, e28542.
6. Claessen, J. H., Kundrat, L. and Ploegh, H. L. (2012). Protein quality control in the ER: balancing the ubiquitin checkbook. Trends Cell Biol. 22, 22-32.
7. Clague, M. J., Coulson, J. M. and Urbé, S. (2012). Cellular functions of the DUBs. J. Cell Sci. 125, 277-286.
8. Ernst, R., Claessen, J. H. L., Mueller, B., Sanyal, S., Spooner, E., van der Veen, A. G., Kirak, O., Schlieker, C. D., Weihofen, W. A. and Ploegh, H. L. (2011). Enzymatic blockade of the ubiquitin-proteasome pathway. PLoS Biol. 8, e1000605.
9. Fleig, L., Bergbold, N., Sahasrabudhe, P., Geiger, B., Kaltak, L. and Lemberg, M. K. (2012). Ubiquitin-dependent intramembrane rhomboid protease promotes ERAD of membrane proteins. Mol. Cell 47, 558-569.
10. Ghaemmaghami, S., Huh, W.-K., Bower, K., Howson, R. W., Belle, A., Dephoure, N., O'Shea, E. K. and Weissman, J. S. (2003). Global analysis of protein expression in yeast. Nature 425, 737-741.
11. Goeckeler, J. L. and Brodsky, J. L. (2010). Molecular chaperones and substrate ubiquitination control the efficiency of endoplasmic reticulum-associated degradation. Diabetes Obes. Metab. 12 Suppl. 2, 32-38.
12. Grabbe, C., Husnjak, K. and Dikic, I. (2011). The spatial and temporal organization of ubiquitin networks. Nat. Rev. Mol. Cell Biol. 12, 295-307.
13. Hessa, T., Sharma, A., Mariappan, M., Eshleman, H. D., Gutierrez, E. and Hegde, R. S. (2011). Protein targeting and degradation are coupled for elimination of mislocalized proteins. Nature 475, 394-397.
14. Jiang, W., Wang, S., Xiao, M., Lin, Y., Zhou, L., Lei, Q., Xiong, Y., Guan, K.-L. and Zhao, S. (2011). Acetylation regulates gluconeogenesis by promoting PEPCK1 degradation via recruiting the UBR5 ubiquitin ligase. Mol. Cell 43, 33-44.
15. Jonikas, M. C. M., Collins, S. R. S., Denic, V., Oh, E., Quan, E. M. E., Schmid, V., Weibezahn, J., Schwappach, B., Walter, P., Weissman, J. S. J. et al. (2009). Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science 323, 1693-1697.
16. Kawahara, H., Minami, R. and Yokota, N. (2013). BAG6/BAT3: emerging roles in quality control for nascent polypeptides. J. Biochem. 153, 147-160.
17. Kikukawa, Y., Minami, R., Shimada, M., Kobayashi, M., Tanaka, K., Yokosawa, H. and Kawahara, H. (2005). Unique proteasome subunit Xrpn10c is a specific receptor for the antiapoptotic ubiquitin-like protein Scythe. FEBS J. 272, 6373-6386.
18. Kimura, Y. and Tanaka, K. (2010). Regulatory mechanisms involved in the control of ubiquitin homeostasis. J. Biochem. 147, 793-798.
19. Krenciute, G., Liu, S., Yucer, N., Shi, Y., Ortiz, P., Liu, Q., Kim, B. J., Odejimi, A. O., Leng, M., Qin, J. et al. (2013). Nuclear BAG6-UBL4A-GET4 complex mediates DNA damage signaling and cell death. J. Biol. Chem. 288, 20547-20557.
20. Lee, J.-G. and Ye, Y. (2013). Bag6/Bat3/Scythe: a novel chaperone activity with diverse regulatory functions in protein biogenesis and degradation. Bioessays 35, 377-385.
21. Leznicki, P. and High, S. (2012). SGTA antagonizes BAG6-mediated protein triage. Proc. Natl. Acad. Sci. USA 109, 19214-19219.
22. Leznicki, P., Clancy, A., Schwappach, B. and High, S. (2010). Bat3 promotes the membrane integration of tail-anchored proteins. J. Cell Sci. 123, 2170-2178.
23. Leznicki, P., Roebuck, Q. P., Wunderley, L., Clancy, A., Krysztofinska, E. M., Isaacson, R. L., Warwicker, J., Schwappach, B. and High, S. (2013). The association of BAG6 with SGTA and tail-anchored proteins. PLoS ONE 8, e59590.
24. Liu, Y., Soetandyo, N., Lee, J.-G., Liu, L., Xu, Y., Clemons, W. M., Jr and Ye, Y. (2014). USP13 antagonizes gp78 to maintain functionality of a chaperone in ERassociated degradation. Elife 3, e01369.
25. Lynes, E. M. and Simmen, T. (2011). Urban planning of the endoplasmic reticulum (ER): how diverse mechanisms segregate the many functions of the ER. Biochim. Biophys. Acta 1813, 1893-1905.
26. Manchen, S. T. and Hubberstey, A. V. (2001). Human Scythe contains a functional nuclear localization sequence and remains in the nucleus during staurosporine-induced apoptosis. Biochem. Biophys. Res. Commun. 287, 1075-1082.
27. Matiuhin, Y., Kirkpatrick, D. S., Ziv, I., Kim, W., Dakshinamurthy, A., Kleifeld, O., Gygi, S. P., Reis, N. and Glickman, M. H. (2008). Extraproteasomal Rpn10 restricts access of the polyubiquitin-binding protein Dsk2 to proteasome. Mol. Cell 32, 415-425.
28. Minami, R., Hayakawa, A., Kagawa, H., Yanagi, Y., Yokosawa, H. and Kawahara, H. (2010). BAG-6 is essential for selective elimination of defective proteasomal substrates. J. Cell Biol. 190, 637-650.
29. Prelich, G. (2012). Gene overexpression: uses, mechanisms, and interpretation. Genetics 190, 841-854.
30. Ray-Sinha, A., Cross, B. C., Mironov, A., Wiertz, E. and High, S. (2009). Endoplasmic reticulum-associated degradation of a degron-containing polytopic membrane protein. Mol. Membr. Biol. 26, 448-464.
31. Su, V. and Lau, A. F. (2009). Ubiquitin-like and ubiquitin-associated domain proteins: significance in proteasomal degradation. Cell. Mol. Life Sci. 66, 2819-2833.
32. Wang, X. and Terpstra, E. J. M. (2013). Ubiquitin receptors and protein quality control. J. Mol. Cell. Cardiol. 55, 73-84.
33. Wang, Q., Liu, Y., Soetandyo, N., Baek, K., Hegde, R. and Ye, Y. (2011). A ubiquitin ligase-associated chaperone holdase maintains polypeptides in soluble states for proteasome degradation. Mol. Cell 42, 758-770.
34. Wiertz, E. J., Jones, T. R., Sun, L., Bogyo, M., Geuze, H. J. and Ploegh, H. L. (1996a). The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84, 769-779.
35. Wiertz, E. J., Tortorella, D., Bogyo, M., Yu, J., Mothes, W., Jones, T. R., Rapoport, T. A. and Ploegh, H. L. (1996b). Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384, 432-438.
36. Winnefeld, M., Grewenig, A., Schnölzer, M., Spring, H., Knoch, T. A., Gan, E. C., Rommelaere, J. and Cziepluch, C. (2006). Human SGT interacts with Bag-6/Bat-3/Scythe and cells with reduced levels of either protein display persistence of few misaligned chromosomes and mitotic arrest. Exp. Cell Res. 312, 2500-2514.
37. Wu, W., Song, W., Li, S., Ouyang, S., Fok, K. L., Diao, R., Miao, S., Chan, H. C. and Wang, L. (2012). Regulation of apoptosis by Bat3-enhanced YWK-II/APLP2 protein stability. J. Cell Sci. 125, 4219-4229.
38. Xu, Y., Cai, M., Yang, Y., Huang, L. and Ye, Y. (2012). SGTA recognizes a noncanonical ubiquitin-like domain in the Bag6-Ubl4A-Trc35 complex to promote endoplasmic reticulum-associated degradation. Cell Rep. 2, 1633-1644.
39. Xu, Y., Liu, Y., Lee, J.-G. and Ye, Y. (2013). A ubiquitin-like domain recruits an oligomeric chaperone to a retrotranslocation complex in endoplasmic reticulumassociated degradation. J. Biol. Chem. 288, 18068-18076.
40. Yewdell, J. W., Lacsina, J. R., Rechsteiner, M. C. and Nicchitta, C. V. (2011). Out with the old, in with the new? Comparing methods for measuring protein degradation. Cell Biol. Int. 35, 457-462.
41. Yong, S. T. and Wang, X.-F. (2012). A novel, non-apoptotic role for Scythe/BAT3: a functional switch between the pro-and anti-proliferative roles of p21 during the cell cycle. PLoS ONE 7, e38085.