Quality and quantity control at the endoplasmic reticulum

Current Opinion in Cell Biology

Volumn 22, Issue 4, 2010, Pages 437-446

  Hegde, Ramanujan S ^a   Ploegh, Hidde L ^b  

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

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; UBIQUITIN PROTEIN LIGASE;

AUTOPHOSPHORYLATION; CELL SURFACE; CYTOSOL; ENDOPLASMIC RETICULUM; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; QUALITY CONTROL; REVIEW; UBIQUITINATION; ANIMAL; METABOLISM; PHYSIOLOGICAL STRESS; PROTEIN PROCESSING;

ANIMALS; CYTOSOL; ENDOPLASMIC RETICULUM; HUMANS; METABOLIC NETWORKS AND PATHWAYS; PROTEIN PROCESSING, POST-TRANSLATIONAL; STRESS, PHYSIOLOGICAL;

EID: 77955049339     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2010.05.005     Document Type: Review

References (78)

1. Anelli T., Sitia R. Protein quality control in the early secretory pathway. EMBO J 2008, 27:315-327.
2. Hampton R.Y., Garza R.M. Protein quality control as a strategy for cellular regulation: lessons from ubiquitin-mediated regulation of the sterol pathway. Chem Rev 2009, 109:1561-1574.
3. Vembar S.S., Brodsky J.L. One step at a time: endoplasmic reticulum-associated degradation. Nat Rev Mol Cell Biol 2008, 9:944-957.
4. Helenius A., Marquardt T., Braakman I. The endoplasmic reticulum as a protein-folding compartment. Trends Cell Biol 1992, 2:227-231.
5. Helenius A., Aebi M. Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 2004, 73:1019-1049.
6. Hosokawa N., Tremblay L.O., Sleno B., Kamiya Y., Wada I., Nagata K., Kato K., Herscovics A. EDEM1 accelerates the trimming of alpha1,2-linked mannose on the C branch of N-glycans. Glycobiology 2010, 20:567-575.
7. Quan E.M., Kamiya Y., Kamiya D., Denic V., Weibezahn J., Kato K., Weissman J.S. Defining the glycan destruction signal for endoplasmic reticulum-associated degradation. Mol Cell 2008, 32:870-877.
8. Clerc S., Hirsch C., Oggier D.M., Deprez P., Jakob C., Sommer T., Aebi M. Htm1 protein generates the N-glycan signal for glycoprotein degradation in the endoplasmic reticulum. J Cell Biol 2009, 184:159-172.
9. Hosokawa N., Kamiya Y., Kato K. The role of MRH domain-containing lectins in ERAD. Glycobiology 2010, 10.1093/glycob/cwq013.
10. Kamiya Y., Kamiya D., Yamamoto K., Nyfeler B., Hauri H.P., Kato K. Molecular basis of sugar recognition by the human L-type lectins ERGIC-53, VIPL, and VIP36. J Biol Chem 2008, 283:1857-1861.
11. Jakob C.A., Chevet E., Thomas D.Y., Bergeron J.J. Lectins of the ER quality control machinery. Results Probl Cell Differ 2001, 33:1-17.
12. Daniels R., Kurowski B., Johnson A.E., Hebert D.N. N-linked glycans direct the cotranslational folding pathway of influenza hemagglutinin. Mol Cell 2003, 11:79-90.
13. Appenzeller C., Andersson H., Kappeler F., Hauri H.P. The lectin ERGIC-53 is a cargo transport receptor for glycoproteins. Nat Cell Biol 1999, 1:330-334.
14. Mikami K., Yamaguchi D., Tateno H., Hu D., Qin S.Y., Kawasaki N., Yamada M., Matsumoto N., Hirabayashi J., Ito Y., Yamamoto K. The sugar-binding ability of human OS-9 and its involvement in ER-associated degradation. Glycobiology 2010, 20:310-321.
15. Molinari M., Calanca V., Galli C., Lucca P., Paganetti P. Role of EDEM in the release of misfolded glycoproteins from the calnexin cycle. Science 2003, 299:1397-1400.
16. Oda Y., Hosokawa N., Wada I., Nagata K. EDEM as an acceptor of terminally misfolded glycoproteins released from calnexin. Science 2003, 299:1394-1397.
17. Keith N., Parodi A.J., Caramelo J.J. Glycoprotein tertiary and quaternary structures are monitored by the same quality control mechanism. J Biol Chem 2005, 280:18138-18141.
18. Hebert D.N., Garman S.C., Molinari M. The glycan code of the endoplasmic reticulum: asparagine-linked carbohydrates as protein maturation and quality-control tags. Trends Cell Biol 2005, 15:364-370.
19. Okuda-Shimizu Y., Hendershot L.M. Characterization of an ERAD pathway for nonglycosylated BiP substrates, which require Herp. Mol Cell 2007, 28:544-554.
20. Bernasconi R., Galli C., Calanca V., Nakajima T., Molinari M. Stringent requirement for HRD1, SEL1L, and OS-9/XTP3-B for disposal of ERAD-LS substrates. J Cell Biol 2010, 188:223-235.
21. Sato B.K., Schulz D., Do P.H., Hampton R.Y. Misfolded membrane proteins are specifically recognized by the transmembrane domain of the Hrd1p ubiquitin ligase. Mol Cell 2009, 34:212-222.
22. Christianson J.C., Shaler T.A., Tyler R.E., Kopito R.R. OS-9 and GRP94 deliver mutant alpha1-antitrypsin to the Hrd1-SEL1L ubiquitin ligase complex for ERAD. Nat Cell Biol 2008, 10:272-282.
23. Hosokawa N., Wada I., Nagasawa K., Moriyama T., Okawa K., Nagata K. Human XTP3-B forms an endoplasmic reticulum quality control scaffold with the HRD1-SEL1L ubiquitin ligase complex and BiP. J Biol Chem 2008, 283:20914-20924.
24. Lee S.O., Cho K., Cho S., Kim I., Oh C., Ahn K. Protein disulphide isomerase is required for signal peptide peptidase-mediated protein degradation. EMBO J 2010, 29:363-375.
25. Bernardi K.M., Forster M.L., Lencer W.I., Tsai B. Derlin-1 facilitates the retro-translocation of cholera toxin. Mol Biol Cell 2008, 19:877-884.
26. Weitzmann A., Baldes C., Dudek J., Zimmermann R. The heat shock protein 70 molecular chaperone network in the pancreatic endoplasmic reticulum - a quantitative approach. FEBS J 2007, 274:5175-5187.
27. Hirsch C., Gauss R., Horn S.C., Neuber O., Sommer T. The ubiquitylation machinery of the endoplasmic reticulum. Nature 2009, 458:453-460.
28. Carvalho P., Goder V., Rapoport T.A. Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell 2006, 126:361-373.
29. Denic V., Quan E.M., Weissman J.S. A luminal surveillance complex that selects misfolded glycoproteins for ER-associated degradation. Cell 2006, 126:349-359.
30. Gauss R., Sommer T., Jarosch E. The Hrd1p ligase complex forms a linchpin between ER-lumenal substrate selection and Cdc48p recruitment. EMBO J 2006, 25:1827-1835.
31. Kanehara K., Xie W., Ng D.T. Modularity of the Hrd1 ERAD complex underlies its diverse client range. J Cell Biol 2010, 188:707-716.
32. Hebert D.N., Bernasconi R., Molinari M. ERAD substrates: which way out?. Semin Cell Dev Biol 2010, 21:526-532.
33. Ploegh H.L. A lipid-based model for the creation of an escape hatch from the endoplasmic reticulum. Nature 2007, 448:435-438.
34. Brambillasca S., Yabal M., Makarow M., Borgese N. Unassisted translocation of large polypeptide domains across phospholipid bilayers. J Cell Biol 2006, 175:767-777.
35. Nickel W., Rabouille C. Mechanisms of regulated unconventional protein secretion. Nat Rev Mol Cell Biol 2009, 10:148-155.
36. Duran J.M., Anjard C., Stefan C., Loomis W.F., Malhotra V. Unconventional secretion of Acb1 is mediated by autophagosomes. J Cell Biol 2010, 188:527-536.
37. Manjithaya R., Anjard C., Loomis W.F., Subramani S. Unconventional secretion of Pichia pastoris Acb1 is dependent on GRASP protein, peroxisomal functions, and autophagosome formation. J Cell Biol 2010, 188:537-546.
38. Ye Y. Diverse functions with a common regulator: ubiquitin takes command of an AAA ATPase. J Struct Biol 2006, 156:29-40.
39. Ye Y., Shibata Y., Kikkert M., van Voorden S., Wiertz E., Rapoport T.A. Inaugural article: Recruitment of the p97 ATPase and ubiquitin ligases to the site of retrotranslocation at the endoplasmic reticulum membrane. Proc Natl Acad Sci U S A 2005, 102:14132-14138.
40. Lilley B.N., Ploegh H.L. Multiprotein complexes that link dislocation, ubiquitination, and extraction of misfolded proteins from the endoplasmic reticulum membrane. Proc Natl Acad Sci U S A 2005, 102:14296-14301.
41. Ballar P., Shen Y., Yang H., Fang S. The role of a novel p97/valosin-containing protein-interacting motif of gp78 in endoplasmic reticulum-associated degradation. J Biol Chem 2006, 281:35359-35368.
42. Schuberth C., Buchberger A. Membrane-bound Ubx2 recruits Cdc48 to ubiquitin ligases and their substrates to ensure efficient ER-associated protein degradation. Nat Cell Biol 2005, 7:999-1006.
43. Neuber O., Jarosch E., Volkwein C., Walter J., Sommer T. Ubx2 links the Cdc48 complex to ER-associated protein degradation. Nat Cell Biol 2005, 7:993-998.
44. White S.R., Lauring B. AAA+ ATPases: achieving diversity of function with conserved machinery. Traffic 2007, 8:1657-1667.
45. Lee R.J., Liu C.W., Harty C., McCracken A.A., Latterich M., Romisch K., DeMartino G.N., Thomas P.J., Brodsky J.L. Uncoupling retro-translocation and degradation in the ER-associated degradation of a soluble protein. EMBO J 2004, 23:2206-2215.
46. Lipson C., Alalouf G., Bajorek M., Rabinovich E., Atir-Lande A., Glickman M., Bar-Nun S. A proteasomal ATPase contributes to dislocation of endoplasmic reticulum-associated degradation (ERAD) substrates. J Biol Chem 2008, 283:7166-7175.
47. Tirosh B., Furman M.H., Tortorella D., Ploegh H.L. Protein unfolding is not a prerequisite for endoplasmic reticulum-to-cytosol dislocation. J Biol Chem 2003, 278:6664-6672.
48. Schelhaas M., Malmstrom J., Pelkmans L., Haugstetter J., Ellgaard L., Grunewald K., Helenius A. Simian Virus 40 depends on ER protein folding and quality control factors for entry into host cells. Cell 2007, 131:516-529.
49. Ashok A., Hegde R.S. Selective processing and metabolism of disease-causing mutant prion proteins. PLoS Pathog 2009, 5:e1000479.
50. Wang S., Ng D.T. Evasion of endoplasmic reticulum surveillance makes Wsc1p an obligate substrate of Golgi quality control. Mol Biol Cell 2010, 21:1153-1165.
51. DeBose-Boyd R.A. Feedback regulation of cholesterol synthesis: sterol-accelerated ubiquitination and degradation of HMG CoA reductase. Cell Res 2008, 18:609-621.
52. Song B.L., Javitt N.B., DeBose-Boyd R.A. Insig-mediated degradation of HMG CoA reductase stimulated by lanosterol, an intermediate in the synthesis of cholesterol. Cell Metab 2005, 1:179-189.
53. Song B.L., Sever N., DeBose-Boyd R.A. Gp78, a membrane-anchored ubiquitin ligase, associates with Insig-1 and couples sterol-regulated ubiquitination to degradation of HMG CoA reductase. Mol Cell 2005, 19:829-840.
54. Shearer A.G., Hampton R.Y. Lipid-mediated, reversible misfolding of a sterol-sensing domain protein. EMBO J 2005, 24:149-159.
55. Bays N.W., Gardner R.G., Seelig L.P., Joazeiro C.A., Hampton R.Y. Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ER-associated degradation. Nat Cell Biol 2001, 3:24-29.
56. Flury I., Garza R., Shearer A., Rosen J., Cronin S., Hampton R.Y. INSIG: a broadly conserved transmembrane chaperone for sterol-sensing domain proteins. EMBO J 2005, 24:3917-3926.
57. Isaacson M.K., Ploegh H.L. Ubiquitination, ubiquitin-like modifiers, and deubiquitination in viral infection. Cell Host Microbe 2009, 5:559-570.
58. Stagg H.R., Thomas M., van den Boomen D., Wiertz E.J., Drabkin H.A., Gemmill R.M., Lehner P.J. The TRC8 E3 ligase ubiquitinates MHC class I molecules before dislocation from the ER. J Cell Biol 2009, 186:685-692.
59. Loureiro J., Lilley B.N., Spooner E., Noriega V., Tortorella D., Ploegh H.L. Signal peptide peptidase is required for dislocation from the endoplasmic reticulum. Nature 2006, 441:894-897.
60. Mueller B., Klemm E.J., Spooner E., Claessen J.H., Ploegh H.L. SEL1L nucleates a protein complex required for dislocation of misfolded glycoproteins. Proc Natl Acad Sci U S A 2008, 105:12325-12330.
61. Margottin F., Bour S.P., Durand H., Selig L., Benichou S., Richard V., Thomas D., Strebel K., Benarous R. 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 1998, 1:565-574.
62. Binette J., Dube M., Mercier J., Halawani D., Latterich M., Cohen E.A. Requirements for the selective degradation of CD4 receptor molecules by the human immunodeficiency virus type 1 Vpu protein in the endoplasmic reticulum. Retrovirology 2007, 4:75.
63. Magadan J.G., Perez-Victoria F.J., Sougrat R., Ye Y., Strebel K., Bonifacino J.S. Multilayered mechanism of CD4 downregulation by HIV-1 Vpu involving distinct ER retention and ERAD targeting steps. PLoS Path 2010, 6:e1000869.
64. Wang X., Ye Y., Lencer W., Hansen T.H. The viral E3 ubiquitin ligase mK3 uses the Derlin/p97 endoplasmic reticulum-associated degradation pathway to mediate down-regulation of major histocompatibility complex class I proteins. J Biol Chem 2006, 281:8636-8644.
65. Wang X., Herr R.A., Chua W.J., Lybarger L., Wiertz E.J., Hansen T.H. Ubiquitination of serine, threonine, or lysine residues on the cytoplasmic tail can induce ERAD of MHC-I by viral E3 ligase mK3. J Cell Biol 2007, 177:613-624.
66. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007, 8:519-529.
67. Harding H.P., Zhang Y., Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 1999, 397:271-274.
68. Hollien J., Lin J.H., Li H., Stevens N., Walter P., Weissman J.S. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 2009, 186:323-331.
69. Han D., Lerner A.G., Vande Walle L., Upton J.P., Xu W., Hagen A., Backes B.J., Oakes S.A., Papa F.R. IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 2009, 138:562-575.
70. Iqbal J., Dai K., Seimon T., Jungreis R., Oyadomari M., Kuriakose G., Ron D., Tabas I., Hussain M.M. IRE1beta inhibits chylomicron production by selectively degrading MTP mRNA. Cell Metab 2008, 7:445-455.
71. Kang S.W., Rane N.S., Kim S.J., Garrison J.L., Taunton J., Hegde R.S. Substrate-specific translocational attenuation during ER stress defines a pre-emptive quality control pathway. Cell 2006, 127:999-1013.
72. Orsi A., Fioriti L., Chiesa R., Sitia R. Conditions of endoplasmic reticulum stress favor the accumulation of cytosolic prion protein. J Biol Chem 2006, 281:30431-30438.
73. Spear E.D., Ng D.T. Stress tolerance of misfolded carboxypeptidase Y requires maintenance of protein trafficking and degradative pathways. Mol Biol Cell 2003, 14:2756-2767.
74. Kamimoto T., Shoji S., Hidvegi T., Mizushima N., Umebayashi K., Perlmutter D.H., Yoshimori T. Intracellular inclusions containing mutant alpha1-antitrypsin Z are propagated in the absence of autophagic activity. J Biol Chem 2006, 281:4467-4476.
75. Kruse K.B., Brodsky J.L., McCracken A.A. Characterization of an ERAD gene as VPS30/ATG6 reveals two alternative and functionally distinct protein quality control pathways: one for soluble Z variant of human alpha-1 proteinase inhibitor (A1PiZ) and another for aggregates of A1PiZ. Mol Biol Cell 2006, 17:203-212.
76. Bernales S., McDonald K.L., Walter P. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol 2006, 4:e423.
77. Jonikas M.C., Collins S.R., Denic V., Oh E., Quan E.M., Schmid V., Weibezahn J., Schwappach B., Walter P., Weissman J.S., Schuldiner M. Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science 2009, 323:1693-1697.
78. Kamhi-Nesher S., Shenkman M., Tolchinsky S., Fromm S.V., Ehrlich R., Lederkremer G.Z. A novel quality control compartment derived from the endoplasmic reticulum. Mol Biol Cell 2001, 12:1711-1723.