A Cdc48 "retrochaperone" function is required for the solubility of retrotranslocated, integral membrane Endoplasmic Reticulum-associated Degradation (ERAD-M) substrates

Journal of Biological Chemistry

Volumn 292, Issue 8, 2017, Pages 3112-3128

  Neal, Sonya ^a   Mak, Raymond ^a   Bennett, Eric J ^a   Hampton, Randolph ^a  

^a SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; BIOLOGICAL MEMBRANES; CELL MEMBRANES; CYTOLOGY; MOLECULAR BIOLOGY; PROTEINS; SOLUBILITY;

26 S PROTEASOME; BIOCHEMICAL CONFIRMATION; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATIONS; INTEGRAL MEMBRANE; MEMBRANE PROTEINS; RETROTRANSLOCATION; SUBSTRATE SOLUBILITIES;

SUBSTRATES;

CDC48 PROTEIN; CHAPERONE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; CELL CYCLE PROTEIN; HMG2 PROTEIN, S CEREVISIAE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; SACCHAROMYCES CEREVISIAE PROTEIN; UBIQUITIN;

ARTICLE; BINDING COMPETITION; COMPLEX FORMATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; IN VIVO STUDY; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEOMICS; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; SOLUBILITY; CYTOLOGY; ENDOPLASMIC RETICULUM; METABOLISM; UBIQUITINATION;

ADENOSINE TRIPHOSPHATASES; CELL CYCLE PROTEINS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; HYDROXYMETHYLGLUTARYL COA REDUCTASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SOLUBILITY; UBIQUITIN; UBIQUITINATION;

EID: 85013784737     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.770610     Document Type: Article

References (59)

1. Foresti, O., Ruggiano, A., Hannibal-Bach, H. K., Ejsing, C. S., and Carvalho, P. (2013) Sterol homeostasis requires regulated degradation of squalene monooxygenase by the ubiquitin ligase Doa10/Teb4. Elife 2, e00953
2. Hampton, R. Y., and Garza, R. M. (2009) Protein quality control as a strategy for cellular regulation: lessons from ubiquitin-mediated regulation of the sterol pathway. Chem. Rev. 109, 1561-1574
3. Bays, N. W., Gardner, R. G., Seelig, L. P., Joazeiro, C. A., and Hampton, R. Y. (2001) Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ER-associated degradation. Nat. Cell Biol. 3, 24-29
4. 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. U.S.A. 103, 341-346
5. Swanson, R., Locher, M., and Hochstrasser, M. (2001) A conserved ubiquitin ligase of the nuclear envelope/endoplasmic reticulum that functions in both ER-associated and Matα2 repressor degradation. Genes Dev. 15, 2660-2674
6. Richly, H., Rape, M., Braun, S., Rumpf, S., Hoege, C., and Jentsch, S. (2005) A series of ubiquitin binding factors connects CDC48/p97 to substrate multiubiquitylation and proteasomal targeting. Cell 120, 73-84
7. Plemper, R. K., Egner, R., Kuchler, K., and Wolf, D. H. (1998) Endoplasmic reticulum degradation of a mutated ATP-binding cassette transporter Pdr5 proceeds in a concerted action of Sec61 and the proteasome. J. Biol. Chem. 273, 32848-32856
8. Vashist, S., and Ng, D. T. (2004) Misfolded proteins are sorted by a sequential checkpoint mechanism of ER quality control. J. Cell Biol. 165, 41-52
9. Jo, Y., and Debose-Boyd, R. A. (2010) Control of cholesterol synthesis through regulated ER-associated degradation of HMG CoA reductase. Crit. Rev. Biochem. Mol. Biol. 45, 185-198
10. Zhang, Y., Nijbroek, G., Sullivan, M. L., McCracken, A. A., Watkins, S. C., Michaelis, S., and Brodsky, J. L. (2001) Hsp70 molecular chaperone facilitates endoplasmic reticulum-associated protein degradation of cystic fibrosis transmembrane conductance regulator in yeast. Mol. Biol. Cell 12, 1303-1314
11. Carvalho, P., Goder, V., and Rapoport, T. A. (2006) Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell 126, 361-373
12. Bordallo, J., Plemper, R. K., Finger, A., and Wolf, D. H. (1998) Der3p/Hrd1p is required for endoplasmic reticulum-associated degradation of misfolded luminal and integral membrane proteins. Mol. Biol. Cell. 9, 209-222
13. Hampton, R. Y., Gardner, R. G., and Rine, J. (1996) Role of 26S proteasome and HRD genes in the degradation of 3-hydroxy-3-methylglutaryl-CoA reductase, an integral endoplasmic reticulum membrane protein. Mol. Biol. Cell. 7, 2029-2044
14. Hampton, R. Y., and Sommer, T. (2012) Finding the will and the way of ERAD substrate retrotranslocation. Curr. Opin. Cell Biol. 24, 460-466
15. Hiller, M. M., Finger, A., Schweiger, M., and Wolf, D. H. (1996) ER degradation of a misfolded luminal protein by the cytosolic ubiquitin-proteasome pathway. Science 273, 1725-1728
16. Garza, R. M., Sato, B. K., and Hampton, R. Y. (2009) In vitro analysis of Hrd1p-mediated retrotranslocation of its multispanning membrane substrate 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase. J. Biol. Chem. 284, 14710-14722
17. Nakatsukasa, K., Huyer, G., Michaelis, S., and Brodsky, J. L. (2008) Dissecting the ER-associated degradation of a misfolded polytopic membrane protein. Cell 132, 101-112
18. Baldridge, R. D., and Rapoport, T. A. (2016) Autoubiquitination of the Hrd1 ligase triggers protein retrotranslocation in ERAD. Cell 166, 394-407
19. Xia, D., Tang, W. K., and Ye, Y. (2016) Structure and function of the AAA+ ATPase p97/Cdc48p. Gene 583, 64-77
20. Braun, S., Matuschewski, K., Rape, M., Thoms, S., and Jentsch, S. (2002) Role of the ubiquitin-selective CDC48(UFD1/NPL4)chaperone (segregase) in ERAD of OLE1 and other substrates. EMBO J. 21, 615-621
21. 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
22. Bays, N. W., Wilhovsky, S. K., Goradia, A., Hodgkiss-Harlow, K., and Hampton, R. Y. (2001) HRD4/NPL4 is required for the proteasomal processing of ubiquitinated ER proteins. Mol. Biol. Cell. 12, 4114-4128
23. Pye, V. E., Dreveny, I., Briggs, L. C., Sands, C., Beuron, F., Zhang, X., and Freemont, P. S. (2006) Going through the motions: the ATPase cycle of p97. J. Struct. Biol. 156, 12-28
24. 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. 077114:21-9525
25. Balch, W. E., Morimoto, R. I., Dillin, A., and Kelly, J. W. (2008) Adapting proteostasis for disease intervention. Science 319, 916-919
26. Vangala, J. R., Sotzny, F., Krüger, E., Deshaies, R. J., and Radhakrishnan, S. K. (2016) Nrf1 can be processed and activated in a proteasome-independent manner. Curr. Biol. 26, R834-R835
27. Nakatsukasa, K., and Kamura, T. (2016) Subcellular fractionation analysis of the extraction of ubiquitinated polytopic membrane substrate during ER-associated degradation. PLoS ONE 11, e0148327
28. Ploegh, H. L. (2007) A lipid-based model for the creation of an escape hatch from the endoplasmic reticulum. Nature 448, 435-438
29. Hartman, I. Z., Liu, P., Zehmer, J. K., Luby-Phelps, K., Jo, Y., Anderson, R. G., and DeBose-Boyd, R. A. (2010) Sterol-induced dislocation of 3-hydroxy-3-methylglutaryl coenzyme A reductase from endoplasmic reticulum membranes into the cytosol through a subcellular compartment resembling lipid droplets. J. Biol. Chem. 285, 19288-19298
30. 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
31. Garza, R. M., Tran, P. N., and Hampton, R. Y. (2009) Geranylgeranyl pyrophosphate is a potent regulator of HRD-dependent 3-hydroxy-3-methylglutaryl-CoA reductase degradation in yeast. J. Biol. Chem. 284, 35368-35380
32. Ito, H., Fukuda, Y., Murata, K., and Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168
33. Rao, H., and Sastry, A. (2002) Recognition of specific ubiquitin conjugates is important for the proteolytic functions of the ubiquitin-associated domain proteins Dsk2 and Rad23. J. Biol. Chem. 277, 11691-11695
34. Wilkinson, C. R., Seeger, M., Hartmann-Petersen, R., Stone, M., Wallace, M., Semple, C., and Gordon, C. (2001) Proteins containing the UBA domain are able to bind to multi-ubiquitin chains. Nat. Cell Biol. 3, 939-943
35. 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
36. Doolman, R., Leichner, G. S., Avner, R., and Roitelman, J. (2004) Ubiquitin is conjugated by membrane ubiquitin ligase to three sites, including the N terminus, in transmembrane region of mammalian 3-hydroxy-3-methylglutaryl coenzyme A reductase: implications for sterol-regulated enzyme degradation. J. Biol. Chem. 279, 38184-38193
37. Claypool, S. M., McCaffery, J. M., and Koehler, C. M. (2006) Mitochondrial mislocalization and altered assembly of a cluster of Barth syndrome mutant tafazzins. J. Cell Biol. 174, 379-390
38. Mateja, A., Paduch, M., Chang, H.-Y., Szydlowska, A., Kossiakoff, A. A., Hegde, R. S., and Keenan, R. J. (2015) Protein targeting. Structure of the Get3 targeting factor in complex with its membrane protein cargo. Science 347, 1152-1155
39. Flierman, D., Ye, Y., Dai, M., Chau, V., and Rapoport, T. A. (2003) Polyubiquitin serves as a recognition signal, rather than a ratcheting molecule, during retrotranslocation of proteins across the endoplasmic reticulum membrane. J. Biol. Chem. 278, 34774-34782
40. Pye, V. E., Beuron, F., Keetch, C. A., McKeown, C., Robinson, C. V., Meyer, H. H., Zhang, X., and Freemont, P. S. (2007) Structural insights into the p97-Ufd1-Npl4 complex. Proc. Natl. Acad. Sci. U.S.A. 104, 467-472
41. Wu, X., Li, L., and Jiang, H. (2016) Doa1 targets ubiquitinated substrates for mitochondria-associated degradation. J. Cell Biol. 213, 49-63
42. Ramadan, K., Bruderer, R., Spiga, F. M., Popp, O., Baur, T., Gotta, M., and Meyer, H. H. (2007) Cdc48/p97 promotes reformation of the nucleus by extracting the kinase Aurora B from chromatin. Nature 450, 1258-1262
43. Wilcox, A. J., and Laney, J. D. (2009) A ubiquitin-selective AAA-ATPase mediates transcriptional switching by remodelling a repressor-promoter DNA complex. Nat. Cell Biol. 11, 1481-1486
44. Catt, K., and Tregear, G. W. (1967) Solid-phase radioimmunoassay in antibody-coated tubes. Science 158, 1570-1572
45. Jo, Y., Hartman, I. Z., and DeBose-Boyd, R. A. (2013) Ancient ubiquitous protein-1 mediates sterol-induced ubiquitination of 3-hydroxy-3-methylglutaryl CoA reductase in lipid droplet-associated endoplasmic reticulum membranes. Mol. Biol. Cell. 24, 169-183
46. Gallagher, P. S., Clowes Candadai, S. V., and Gardner, R. G. (2014) The requirement for Cdc48/p97 in nuclear protein quality control degradation depends on the substrate and correlates with substrate insolubility. J. Cell Sci. 127, 1980-1991
47. Xu, Y., Anderson, D. E., and Ye, Y. (2016) The HECT domain ubiquitin ligase HUWE1 targets unassembled soluble proteins for degradation. Cell Discov. 2, 16040
48. Song, C., Wang, Q., and Li, C. C. (2007) Characterization of the aggregation-prevention activity of p97/valosin-containing protein. Biochemistry 46, 14889-14898
49. Stein, A., Ruggiano, A., Carvalho, P., and Rapoport, T. (2014) Key steps in ERAD of luminal ER proteins reconstituted with purified components. Cell 158, 1375-1388
50. Finley, D. (2009) Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78, 477-513
51. Ernst, R., Mueller, B., Ploegh, H. L., and Schlieker, C. (2009) The otubain YOD1 is a deubiquitinating enzyme that associates with p97 to facilitate protein dislocation from the ER. Mol. Cell 36, 28-38
52. Casson, J., McKenna, M., and High, S. (2016) On the road to nowhere: cross-talk between post-translational protein targeting and cytosolic quality control. Biochem. Soc. Trans. 44, 796-801
53. Zhang, T., Xu, Y., Liu, Y., and Ye, Y. (2015) gp78 functions downstream of Hrd1 to promote degradation of misfolded proteins of the endoplasmic reticulum. Mol. Biol. Cell 26, 4438-4450
54. Rodrigo-Brenni, M. C., Gutierrez, E., and Hegde, R. S. (2014) Cytosolic quality control of mislocalized proteins requires RNF126 recruitment to Bag6. Mol. Cell. 55, 227-237
55. Hampton, R. Y., and Rine, J. (1994) Regulated degradation of HMG-CoA reductase, an integral membrane protein of the endoplasmic reticulum, in yeast. J. Cell Biol. 125, 299-312
56. Gardner, R., Cronin, S., Leader, B., Rine, J., Hampton, R., and Leder, B. (1998) Sequence determinants for regulated degradation of yeast 3-hydroxy-3-methylglutaryl-CoA reductase, an integral endoplasmic reticulum membrane protein. Mol. Biol. Cell 9, 2611-2626
57. Sato, B. K., Schulz, D., Do, P. H., and Hampton, R. Y. (2009) Misfolded membrane proteins are specifically recognized by the transmembrane domain of the Hrd1p ubiquitin ligase. Mol. Cell 34, 212-222
58. Sato, B., K., and Hampton, R. Y. (2006) Yeast Derlin Dfm1 interacts with Cdc48 and functions in ER homeostasis. Yeast 10.1002/yea.1407
59. Vashistha, N., Neal, S. E., Singh, A., Carroll, S. M., and Hampton, R. Y. (2016) Direct and essential function for Hrd3 in ER-associated degradation. Proc. Natl. Acad. Sci. U.S.A. 113, 5934-5939