XDeubiquitinases sharpen substrate discrimination during membrane protein degradation from the ER

Cell

Volumn 154, Issue 3, 2013, Pages

  Zhang, Zai Rong ^a,c   Bonifacino, Juan S ^a   Hegde, Ramanujan S ^b  

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

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE; CD4 ANTIGEN; DEUBIQUITINASE; LIGASE; LIPOSOME; MEMBRANE PROTEIN; POLYUBIQUITIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; VPU PROTEIN;

ARTICLE; CELL FATE; COMPUTER ANALYSIS; CONTROLLED STUDY; DISSOCIATION; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; EXPERIMENTAL STUDY; HUMAN; HUMAN CELL; MOLECULAR RECOGNITION; PRIORITY JOURNAL; QUALITY CONTROL; UBIQUITINATION;

ANTIGENS, CD4; ENDOPEPTIDASES; ENDOPLASMIC RETICULUM; HEK293 CELLS; HELA CELLS; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; LIPOSOMES; MEMBRANE PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 84881150929     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.06.038     Document Type: Article

References (54)

1. J.R. Blount, A.A. Burr, A. Denuc, G. Marfany, and S.V. Todi Ubiquitin-specific protease 25 functions in Endoplasmic Reticulum-associated degradation PLoS One 7 2012 e36542
2. S. Bour, U. Schubert, and K. Strebel The human immunodeficiency virus type 1 Vpu protein specifically binds to the cytoplasmic domain of CD4: implications for the mechanism of degradation J. Virol. 69 1995 1510 1520
3. A. Buchberger, B. Bukau, and T. Sommer Protein quality control in the cytosol and the endoplasmic reticulum: brothers in arms Mol. Cell 40 2010 238 252
4. M.Y. Chen, F. Maldarelli, M.K. Karczewski, R.L. Willey, and K. Strebel Human immunodeficiency virus type 1 Vpu protein induces degradation of CD4 in vitro: the cytoplasmic domain of CD4 contributes to Vpu sensitivity J. Virol. 67 1993 3877 3884
5. F. Chiti, and C.M. Dobson Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75 2006 333 366
6. R.A. DeBose-Boyd Feedback regulation of cholesterol synthesis: sterol-accelerated ubiquitination and degradation of HMG CoA reductase Cell Res. 18 2008 609 621
7. D.M. Duda, L.A. Borg, D.C. Scott, H.W. Hunt, M. Hammel, and B.A. Schulman Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation Cell 134 2008 995 1006
8. R. Ernst, B. Mueller, H.L. Ploegh, and C. Schlieker The otubain YOD1 is a deubiquitinating enzyme that associates with p97 to facilitate protein dislocation from the ER Mol. Cell 36 2009 28 38
9. R. Ernst, J.H. Claessen, B. Mueller, S. Sanyal, E. Spooner, A.G. van der Veen, O. Kirak, C.D. Schlieker, W.A. Weihofen, and H.L. Ploegh Enzymatic blockade of the ubiquitin-proteasome pathway PLoS Biol. 8 2011 e1000605
10. M. Feldman, and F.G. van der Goot Novel ubiquitin-dependent quality control in the endoplasmic reticulum Trends Cell Biol. 19 2009 357 363
11. R.M. Feldman, C.C. Correll, K.B. Kaplan, and R.J. Deshaies A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p Cell 91 1997 221 230
12. R.D. Fons, B.A. Bogert, and R.S. Hegde Substrate-specific function of the translocon-associated protein complex during translocation across the ER membrane J. Cell Biol. 160 2003 529 539
13. M.H. Furman, H.L. Ploegh, and D. Tortorella Membrane-specific, host-derived factors are required for US2- and US11-mediated degradation of major histocompatibility complex class I molecules J. Biol. Chem. 277 2002 3258 3267
14. R.G. Gardner, A.G. Shearer, and R.Y. Hampton In vivo action of the HRD ubiquitin ligase complex: mechanisms of endoplasmic reticulum quality control and sterol regulation Mol. Cell. Biol. 21 2001 4276 4291
15. R.M. Garza, B.K. Sato, and R.Y. Hampton In vitro analysis of Hrd1p-mediated retrotranslocation of its multispanning membrane substrate 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase J. Biol. Chem. 284 2009 14710 14722
16. A.D. Gillon, C.F. Latham, and E.A. Miller Vesicle-mediated ER export of proteins and lipids Biochim. Biophys. Acta 1821 2012 1040 1049
17. D.E. Grove, C.Y. Fan, H.Y. Ren, and D.M. Cyr The endoplasmic reticulum-associated Hsp40 DNAJB12 and Hsc70 cooperate to facilitate RMA1 E3-dependent degradation of nascent CFTRDeltaF508 Mol. Biol. Cell 22 2011 301 314
18. R.Y. Hampton ER-associated degradation in protein quality control and cellular regulation Curr. Opin. Cell Biol. 14 2002 476 482
19. U. Hassiepen, U. Eidhoff, G. Meder, J.F. Bulber, A. Hein, U. Bodendorf, E. Lorthiois, and B. Martoglio A sensitive fluorescence intensity assay for deubiquitinating proteases using ubiquitin-rhodamine110-glycine as substrate Anal. Biochem. 371 2007 201 207
20. M. Higy, T. Junne, and M. Spiess Topogenesis of membrane proteins at the endoplasmic reticulum Biochemistry 43 2004 12716 12722
21. C. Hirsch, R. Gauss, S.C. Horn, O. Neuber, and T. Sommer The ubiquitylation machinery of the endoplasmic reticulum Nature 458 2009 453 460
22. M.K. Isaacson, and H.L. Ploegh Ubiquitination, ubiquitin-like modifiers, and deubiquitination in viral infection Cell Host Microbe 5 2009 559 570
23. S. Ishikura, A.M. Weissman, and J.S. Bonifacino Serine residues in the cytosolic tail of the T-cell antigen receptor alpha-chain mediate ubiquitination and endoplasmic reticulum-associated degradation of the unassembled protein J. Biol. Chem. 285 2010 23916 23924
24. G.Z. Lederkremer, and M.H. Glickman A window of opportunity: timing protein degradation by trimming of sugars and ubiquitins Trends Biochem. Sci. 30 2005 297 303
25. T. Li, N.P. Pavletich, B.A. Schulman, and N. Zheng High-level expression and purification of recombinant SCF ubiquitin ligases Methods Enzymol. 398 2005 125 142
26. M.K. Malleshaiah, V. Shahrezaei, P.S. Swain, and S.W. Michnick The scaffold protein Ste5 directly controls a switch-like mating decision in yeast Nature 465 2010 101 105
27. J.G. Magadán, and J.S. Bonifacino Transmembrane domain determinants of CD4 Downregulation by HIV-1 Vpu J. Virol. 86 2012 757 772
28. J.G. Magadán, F.J. Pérez-Victoria, R. Sougrat, Y. Ye, K. Strebel, and J.S. Bonifacino Multilayered mechanism of CD4 downregulation by HIV-1 Vpu involving distinct ER retention and ERAD targeting steps PLoS Pathog. 6 2010 e1000869
29. F. Margottin, S.P. Bour, H. Durand, L. Selig, S. Benichou, V. Richard, D. Thomas, K. Strebel, and R. Benarous A novel human WD protein, h-beta TrCp, that interacts with HIV-1 Vpu connects CD4 to the ER degradation pathway through an F-box motif Mol. Cell 1 1998 565 574
30. M. Mariappan, A. Mateja, M. Dobosz, E. Bove, R.S. Hegde, and R.J. Keenan The mechanism of membrane-associated steps in tail-anchored protein insertion Nature 477 2011 61 66
31. G.C. Meacham, C. Patterson, W. Zhang, J.M. Younger, and D.M. Cyr The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation Nat. Cell Biol. 3 2001 100 105
32. M.S. Melikova, K.A. Kondratov, and E.S. Kornilova Two different stages of epidermal growth factor (EGF) receptor endocytosis are sensitive to free ubiquitin depletion produced by proteasome inhibitor MG132 Cell Biol. Int. 30 2006 31 43
33. B. Meusser, and T. Sommer Vpu-mediated degradation of CD4 reconstituted in yeast reveals mechanistic differences to cellular ER-associated protein degradation Mol. Cell 14 2004 247 258
34. K. Nakatsukasa, G. Huyer, S. Michaelis, and J.L. Brodsky Dissecting the ER-associated degradation of a misfolded polytopic membrane protein Cell 132 2008 101 112
35. M. Nomaguchi, M. Fujita, and A. Adachi Role of HIV-1 Vpu protein for virus spread and pathogenesis Microbes Infect. 10 2008 960 967
36. N.W. Pierce, G. Kleiger, S.O. Shan, and R.J. Deshaies Detection of sequential polyubiquitylation on a millisecond timescale Nature 462 2009 615 619
37. M. Rape, S.K. Reddy, and M.W. Kirschner The processivity of multiubiquitination by the APC determines the order of substrate degradation Cell 124 2006 89 103
38. M.C. Rodrigo-Brenni, and D.O. Morgan Sequential E2s drive polyubiquitin chain assembly on APC targets Cell 130 2007 127 139
39. A. Saha, and R.J. Deshaies Multimodal activation of the ubiquitin ligase SCF by Nedd8 conjugation Mol. Cell 32 2008 21 31
40. B.K. Sato, D. Schulz, P.H. Do, and R.Y. Hampton Misfolded membrane proteins are specifically recognized by the transmembrane domain of the Hrd1p ubiquitin ligase Mol. Cell 34 2009 212 222
41. U. Schubert, and K. Strebel Differential activities of the human immunodeficiency virus type 1-encoded Vpu protein are regulated by phosphorylation and occur in different cellular compartments J. Virol. 68 1994 2260 2271
42. U. Schubert, L.C. Antón, I. Bacík, J.H. Cox, S. Bour, J.R. Bennink, M. Orlowski, K. Strebel, and J.W. Yewdell CD4 glycoprotein degradation induced by human immunodeficiency virus type 1 Vpu protein requires the function of proteasomes and the ubiquitin-conjugating pathway J. Virol. 72 1998 2280 2288
43. C.E. Shamu, C.M. Story, T.A. Rapoport, and H.L. Ploegh The pathway of US11-dependent degradation of MHC class I heavy chains involves a ubiquitin-conjugated intermediate J. Cell Biol. 147 1999 45 58
44. A.S. Sharma, M. Mariappan, S. Appathurai, and R.S. Hegde In vitro dissection of protein translocation into the mammalian endoplasmic reticulum Methods Mol. Biol. 619 2010 339 363
45. S.K. Singh, L. Möckel, P. Thiagarajan-Rosenkranz, M. Wittlich, D. Willbold, and B.W. Koenig Mapping the interaction between the cytoplasmic domains of HIV-1 viral protein U and human CD4 with NMR spectroscopy FEBS J. 279 2012 3705 3714
46. W.R. Skach Cellular mechanisms of membrane protein folding Nat. Struct. Mol. Biol. 16 2009 606 612
47. M.E. Sowa, E.J. Bennett, S.P. Gygi, and J.W. Harper Defining the human deubiquitinating enzyme interaction landscape Cell 138 2009 389 403
48. X. Tian, N.S. Isamiddinova, R.J. Peroutka, S.J. Goldenberg, M.R. Mattern, B. Nicholson, and C. Leach Characterization of selective ubiquitin and ubiquitin-like protease inhibitors using a fluorescence-based multiplex assay format Assay Drug Dev. Technol. 9 2011 165 173
49. N.B. Trunnell, A.C. Poon, S.Y. Kim, and J.E. Ferrell Jr. Ultrasensitivity in the Regulation of Cdc25C by Cdk1 Mol. Cell 41 2011 263 274
50. S.S. Vembar, and J.L. Brodsky One step at a time: endoplasmic reticulum-associated degradation Nat. Rev. Mol. Cell Biol. 9 2008 944 957
51. K.H. Ventii, and K.D. Wilkinson Protein partners of deubiquitinating enzymes Biochem. J. 414 2008 161 175
52. F. Wang, A. Whynot, M. Tung, and V. Denic The mechanism of tail-anchored protein insertion into the ER membrane Mol. Cell 43 2011 738 750
53. D.H. Wolf, and A. Stolz The Cdc48 machine in endoplasmic reticulum associated protein degradation Biochim. Biophys. Acta 1823 2012 117 124
54. K. Wu, J. Kovacev, and Z.Q. Pan Priming and extending: a UbcH5/Cdc34 E2 handoff mechanism for polyubiquitination on a SCF substrate Mol. Cell 37 2010 784 796