Recent technical developments in the study of ER-associated degradation

Current Opinion in Cell Biology

Volumn 29, Issue 1, 2014, Pages 82-91

  Nakatsukasa, Kunio ^a   Kamura, Takumi ^a   Brodsky, Jeffrey L ^b  

^a NAGOYA UNIVERSITY   (Japan)

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CROSS LINKING; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; FLUORESCENCE; GENETIC LINKAGE; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; REVIEW; UBIQUITINATION;

ANIMALS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEINS; UBIQUITINATION;

EID: 84901317040     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2014.04.008     Document Type: Review

References (117)

1. Ellgaard L., Molinari M., Helenius A. Setting the standards: quality control in the secretory pathway. Science 1999, 286:1882-1888.
2. Aridor M. Visiting the ER: the endoplasmic reticulum as a target for therapeutics in traffic related diseases. Adv Drug Deliv Rev 2007, 59:759-781.
3. Hebert D.N., Molinari M. In and out of the ER: protein folding, quality control, degradation, and related human diseases. Physiol Rev 2007, 87:1377-1408.
4. Vembar S.S., Brodsky J.L. One step at a time: endoplasmic reticulum-associated degradation. Nat Rev Mol Cell Biol 2008, 9:944-957.
5. Romisch K. Endoplasmic reticulum-associated degradation. Annu Rev Cell Dev Biol 2005, 21:435-456.
6. Hirsch C., Gauss R., Horn S.C., Neuber O., Sommer T. The ubiquitylation machinery of the endoplasmic reticulum. Nature 2009, 458:453-460.
7. Araki K., Nagata K. Protein folding and quality control in the ER. Cold Spring Harb Perspect Biol 2011, 3:a007526.
8. Hampton R.Y., Sommer T. Finding the will and the way of ERAD substrate retrotranslocation. Curr Opin Cell Biol 2012, 24:460-466.
9. Thibault G., Ng D.T. The endoplasmic reticulum-associated degradation pathways of budding yeast. Cold Spring Harb Perspect Biol 2012, 4.
10. Brodsky J.L. Cleaning up: ER-associated degradation to the rescue. Cell 2012, 151:1163-1167.
11. Claessen J.H., Kundrat L., Ploegh H.L. Protein quality control in the ER: balancing the ubiquitin checkbook. Trends Cell Biol 2012, 22:22-32.
12. Sommer T., Wolf D.H. The ubiquitin-proteasome-system. Biochim Biophys Acta 2014, 1843:1.
13. Gardner R.G., Swarbrick G.M., Bays N.W., Cronin S.R., Wilhovsky S., Seelig L., Kim C., Hampton R.Y. Endoplasmic reticulum degradation requires lumen to cytosol signaling. Transmembrane control of Hrd1p by Hrd3p. J Cell Biol 2000, 151:69-82.
14. Deak P.M., Wolf D.H. Membrane topology and function of Der3/Hrd1p as a ubiquitin-protein ligase (E3) involved in endoplasmic reticulum degradation. J Biol Chem 2001, 276:10663-10669.
15. 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.
16. Nakatsukasa K., Brodsky J.L., Kamura T. A stalled retrotranslocation complex reveals physical linkage between substrate recognition and proteasomal degradation during ER-associated degradation. Mol Biol Cell 2013, 24:1765-1775. S1761-1768.
17. Horn S.C., Hanna J., Hirsch C., Volkwein C., Schutz A., Heinemann U., Sommer T., Jarosch E. Usa1 functions as a scaffold of the HRD-ubiquitin ligase. Mol Cell 2009, 36:782-793.
18. Kim I., Li Y., Muniz P., Rao H. Usa1 protein facilitates substrate ubiquitylation through two separate domains. PLoS One 2009, 4:e7604.
19. Carroll S.M., Hampton R.Y. Usa1p is required for optimal function and regulation of the Hrd1p endoplasmic reticulum-associated degradation ubiquitin ligase. J Biol Chem 2010, 285:5146-5156.
20. Mehnert M., Sommer T., Jarosch E. Der1 promotes movement of misfolded proteins through the endoplasmic reticulum membrane. Nat Cell Biol 2014, 16:77-86.
21. Gardner R.G., Shearer A.G., Hampton R.Y. In vivo action of the HRD ubiquitin ligase complex: mechanisms of endoplasmic reticulum quality control and sterol regulation. Mol Cell Biol 2001, 21:4276-4291.
22. 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.
23. Stanley A.M., Carvalho P., Rapoport T. Recognition of an ERAD-L substrate analyzed by site-specific in vivo photocrosslinking. FEBS Lett 2011, 585:1281-1286.
24. Buschhorn B.A., Kostova Z., Medicherla B., Wolf D.H. A genome-wide screen identifies Yos9p as essential for ER-associated degradation of glycoproteins. FEBS Lett 2004, 577:422-426.
25. Bhamidipati A., Denic V., Quan E.M., Weissman J.S. Exploration of the topological requirements of ERAD identifies Yos9p as a lectin sensor of misfolded glycoproteins in the ER lumen. Mol Cell 2005, 19:741-751.
26. Kim W., Spear E.D., Ng D.T. Yos9p detects and targets misfolded glycoproteins for ER-associated degradation. Mol Cell 2005, 19:753-764.
27. Szathmary R., Bielmann R., Nita-Lazar M., Burda P., Jakob C.A. Yos9 protein is essential for degradation of misfolded glycoproteins and may function as lectin in ERAD. Mol Cell 2005, 19:765-775.
28. Gauss R., Jarosch E., Sommer T., Hirsch C. A complex of Yos9p and the HRD ligase integrates endoplasmic reticulum quality control into the degradation machinery. Nat Cell Biol 2006, 8:849-854.
29. 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.
30. 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.
31. Ye Y., Meyer H.H., Rapoport T.A. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 2001, 414:652-656.
32. Bays N.W., Wilhovsky S.K., Goradia A., Hodgkiss-Harlow K., Hampton R.Y. HRD4/NPL4 is required for the proteasomal processing of ubiquitinated ER proteins. Mol Biol Cell 2001, 12:4114-4128.
33. Jarosch E., Taxis C., Volkwein C., Bordallo J., Finley D., Wolf D.H., Sommer T. Protein dislocation from the ER requires polyubiquitination and the AAA-ATPase Cdc48. Nat Cell Biol 2002, 4:134-139.
34. Rabinovich E., Kerem A., Frohlich K.U., Diamant N., Bar-Nun S. AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation. Mol Cell Biol 2002, 22:626-634.
35. Ye Y., Meyer H.H., Rapoport T.A. 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 2003, 162:71-84.
36. 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.
37. Kreft S.G., Wang L., Hochstrasser M. Membrane topology of the yeast endoplasmic reticulum-localized ubiquitin ligase Doa10 and comparison with its human ortholog TEB4 (MARCH-VI). J Biol Chem 2006, 281:4646-4653.
38. Swanson R., Locher M., Hochstrasser M. A conserved ubiquitin ligase of the nuclear envelope/endoplasmic reticulum that functions in both ER-associated and Matalpha2 repressor degradation. Genes Dev 2001, 15:2660-2674.
39. Ravid T., Kreft S.G., Hochstrasser M. Membrane and soluble substrates of the Doa10 ubiquitin ligase are degraded by distinct pathways. EMBO J 2006, 25:533-543.
40. Vashist S., Ng D.T. Misfolded proteins are sorted by a sequential checkpoint mechanism of ER quality control. J Cell Biol 2004, 165:41-52.
41. Huyer G., Piluek W.F., Fansler Z., Kreft S.G., Hochstrasser M., Brodsky J.L., Michaelis S. Distinct machinery is required in Saccharomyces cerevisiae for the endoplasmic reticulum-associated degradation of a multispanning membrane protein and a soluble luminal protein. J Biol Chem 2004, 279:38369-38378.
42. Chen P., Johnson P., Sommer T., Jentsch S., Hochstrasser M. Multiple ubiquitin-conjugating enzymes participate in the in vivo degradation of the yeast MAT alpha 2 repressor. Cell 1993, 74:357-369.
43. Hiller M.M., Finger A., Schweiger M., Wolf D.H. ER degradation of a misfolded luminal protein by the cytosolic ubiquitin-proteasome pathway. Science 1996, 273:1725-1728.
44. 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.
45. Biederer T., Volkwein C., Sommer T. Role of Cue1p in ubiquitination and degradation at the ER surface. Science 1997, 278:1806-1809.
46. Bagola K., von Delbruck M., Dittmar G., Scheffner M., Ziv I., Glickman M.H., Ciechanover A., Sommer T. Ubiquitin binding by a CUE domain regulates ubiquitin chain formation by ERAD E3 ligases. Mol Cell 2013, 50:528-539.
47. Metzger M.B., Liang Y.H., Das R., Mariano J., Li S., Li J., Kostova Z., Byrd R.A., Ji X., Weissman A.M. A structurally unique E2-binding domain activates ubiquitination by the ERAD E2, Ubc7p, through multiple mechanisms. Mol Cell 2013, 50:516-527.
48. Kikkert M., Doolman R., Dai M., Avner R., Hassink G., van Voorden S., Thanedar S., Roitelman J., Chau V., Wiertz E. Human HRD1 is an E3 ubiquitin ligase involved in degradation of proteins from the endoplasmic reticulum. J Biol Chem 2004, 279:3525-3534.
49. Fang S., Ferrone M., Yang C., Jensen J.P., Tiwari S., Weissman A.M. The tumor autocrine motility factor receptor, gp78, is a ubiquitin protein ligase implicated in degradation from the endoplasmic reticulum. Proc Natl Acad Sci U S A 2001, 98:14422-14427.
50. Hassink G., Kikkert M., van Voorden S., Lee S.J., Spaapen R., van Laar T., Coleman C.S., Bartee E., Fruh K., Chau V., et al. TEB4 is a C4HC3 RING finger-containing ubiquitin ligase of the endoplasmic reticulum. Biochem J 2005, 388:647-655.
51. Mueller B., Lilley B.N., Ploegh H.L. SEL1L, the homologue of yeast Hrd3p, is involved in protein dislocation from the mammalian ER. J Cell Biol 2006, 175:261-270.
52. Lilley B.N., Ploegh H.L. A membrane protein required for dislocation of misfolded proteins from the ER. Nature 2004, 429:834-840.
53. Ye Y., Shibata Y., Yun C., Ron D., Rapoport T.A. A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature 2004, 429:841-847.
54. Greenblatt E.J., Olzmann J.A., Kopito R.R. Derlin-1 is a rhomboid pseudoprotease required for the dislocation of mutant alpha-1 antitrypsin from the endoplasmic reticulum. Nat Struct Mol Biol 2011, 18:1147-1152.
55. Kokame K., Agarwala K.L., Kato H., Miyata T. Herp, a new ubiquitin-like membrane protein induced by endoplasmic reticulum stress. J Biol Chem 2000, 275:32846-32853.
56. Schulze A., Standera S., Buerger E., Kikkert M., van Voorden S., Wiertz E., Koning F., Kloetzel P.M., Seeger M. The ubiquitin-domain protein HERP forms a complex with components of the endoplasmic reticulum associated degradation pathway. J Mol Biol 2005, 354:1021-1027.
57. Christianson J.C., Olzmann J.A., Shaler T.A., Sowa M.E., Bennett E.J., Richter C.M., Tyler R.E., Greenblatt E.J., Harper J.W., Kopito R.R. Defining human ERAD networks through an integrative mapping strategy. Nat Cell Biol 2012, 14:93-105.
58. Bernasconi R., Galli C., Kokame K., Molinari M. Autoadaptive ER-associated degradation defines a preemptive unfolded protein response pathway. Mol Cell 2013, 52:783-793.
59. Schnell D.J., Hebert D.N. Protein translocons: multifunctional mediators of protein translocation across membranes. Cell 2003, 112:491-505.
60. Chin J.W., Cropp T.A., Anderson J.C., Mukherji M., Zhang Z., Schultz P.G. An expanded eukaryotic genetic code. Science 2003, 301:964-967.
61. Shiota T., Mabuchi H., Tanaka-Yamano S., Yamano K., Endo T. In vivo protein-interaction mapping of a mitochondrial translocator protein Tom22 at work. Proc Natl Acad Sci U S A 2011, 108:15179-15183.
62. Carvalho P., Stanley A.M., Rapoport T.A. Retrotranslocation of a misfolded luminal ER protein by the ubiquitin-ligase Hrd1p. Cell 2010, 143:579-591.
63. Sai X., Kokame K., Shiraishi H., Kawamura Y., Miyata T., Yanagisawa K., Komano H. The ubiquitin-like domain of Herp is involved in Herp degradation, but not necessary for its enhancement of amyloid beta-protein generation. FEBS Lett 2003, 553:151-156.
64. Hori O., Ichinoda F., Yamaguchi A., Tamatani T., Taniguchi M., Koyama Y., Katayama T., Tohyama M., Stern D.M., Ozawa K., et al. Role of Herp in the endoplasmic reticulum stress response. Genes Cells 2004, 9:457-469.
65. Miura H., Hashida K., Sudo H., Awa Y., Takarada-Iemata M., Kokame K., Takahashi T., Matsumoto M., Kitao Y., Hori O. Deletion of Herp facilitates degradation of cytosolic proteins. Genes Cells 2010, 15:843-853.
66. Merulla J., Fasana E., Solda T., Molinari M. Specificity and regulation of the endoplasmic reticulum-associated degradation machinery. Traffic 2013, 14:767-777.
67. Bernasconi R., Molinari M. ERAD and ERAD tuning: disposal of cargo and of ERAD regulators from the mammalian ER. Curr Opin Cell Biol 2011, 23:176-183.
68. Travers K.J., Patil C.K., Wodicka L., Lockhart D.J., Weissman J.S., Walter P. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 2000, 101:249-258.
69. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007, 8:519-529.
70. Mori K. Signalling pathways in the unfolded protein response: development from yeast to mammals. J Biochem 2009, 146:743-750.
71. Schuck S., Prinz W.A., Thorn K.S., Voss C., Walter P. Membrane expansion alleviates endoplasmic reticulum stress independently of the unfolded protein response. J Cell Biol 2009, 187:525-536.
72. Yorimitsu T., Nair U., Yang Z., Klionsky D.J. Endoplasmic reticulum stress triggers autophagy. J Biol Chem 2006, 281:30299-30304.
73. 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.
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. Ogata M., Hino S., Saito A., Morikawa K., Kondo S., Kanemoto S., Murakami T., Taniguchi M., Tanii I., Yoshinaga K., et al. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 2006, 26:9220-9231.
76. Bernales S., Schuck S., Walter P. ER-phagy: selective autophagy of the endoplasmic reticulum. Autophagy 2007, 3:285-287.
77. Kouroku Y., Fujita E., Tanida I., Ueno T., Isoai A., Kumagai H., Ogawa S., Kaufman R.J., Kominami E., Momoi T. ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 2007, 14:230-239.
78. Ding W.X., Ni H.M., Gao W., Hou Y.F., Melan M.A., Chen X., Stolz D.B., Shao Z.M., Yin X.M. Differential effects of endoplasmic reticulum stress-induced autophagy on cell survival. J Biol Chem 2007, 282:4702-4710.
79. Okuda-Shimizu Y., Hendershot L.M. Characterization of an ERAD pathway for nonglycosylated BiP substrates, which require Herp. Mol Cell 2007, 28:544-554.
80. 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.
81. 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.
82. 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.
83. Bernardi K.M., Williams J.M., Kikkert M., van Voorden S., Wiertz E.J., Ye Y., Tsai B. The E3 ubiquitin ligases Hrd1 and gp78 bind to and promote cholera toxin retro-translocation. Mol Biol Cell 2010, 21:140-151.
84. Iida Y., Fujimori T., Okawa K., Nagata K., Wada I., Hosokawa N. SEL1L protein critically determines the stability of the HRD1-SEL1L endoplasmic reticulum-associated degradation (ERAD) complex to optimize the degradation kinetics of ERAD substrates. J Biol Chem 2011, 286:16929-16939.
85. Groisman B., Shenkman M., Ron E., Lederkremer G.Z. Mannose trimming is required for delivery of a glycoprotein from EDEM1 to XTP3-B and to late endoplasmic reticulum-associated degradation steps. J Biol Chem 2011, 286:1292-1300.
86. Jonikas M.C., Collins S.R., Denic V., Oh E., Quan E.M., Schmid V., Weibezahn J., Schwappach B., Walter P., Weissman J.S., et al. Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science 2009, 323:1693-1697.
87. Brown M.S., Goldstein J.L. Multivalent feedback regulation of HMG CoA reductase, a control mechanism coordinating isoprenoid synthesis and cell growth. J Lipid Res 1980, 21:505-517.
88. Hampton R.Y., Rine J. Regulated degradation of HMG-CoA reductase, an integral membrane protein of the endoplasmic reticulum, in yeast. J Cell Biol 1994, 125:299-312.
89. Hampton R.Y. Proteolysis and sterol regulation. Annu Rev Cell Dev Biol 2002, 18:345-378.
90. Jo Y., Debose-Boyd R.A. Control of cholesterol synthesis through regulated ER-associated degradation of HMG CoA reductase. Crit Rev Biochem Mol Biol 2010, 45:185-198.
91. Foresti O., Ruggiano A., Hannibal-Bach H.K., Ejsing C.S., Carvalho P. Sterol homeostasis requires regulated degradation of squalene monooxygenase by the ubiquitin ligase Doa10/Teb4. Elife 2013, 2:e00953.
92. Chen X., Tukachinsky H., Huang C.H., Jao C., Chu Y.R., Tang H.Y., Mueller B., Schulman S., Rapoport T.A., Salic A. Processing and turnover of the Hedgehog protein in the endoplasmic reticulum. J Cell Biol 2011, 192:825-838.
93. Tyler R.E., Pearce M.M., Shaler T.A., Olzmann J.A., Greenblatt E.J., Kopito R.R. Unassembled CD147 is an endogenous endoplasmic reticulum-associated degradation substrate. Mol Biol Cell 2012, 23:4668-4678.
94. Horimoto S., Ninagawa S., Okada T., Koba H., Sugimoto T., Kamiya Y., Kato K., Takeda S., Mori K. The unfolded protein response transducer ATF6 represents a novel transmembrane-type endoplasmic reticulum-associated degradation substrate requiring both mannose trimming and SEL1L protein. J Biol Chem 2013, 288:31517-31527.
95. McCracken A.A., Brodsky J.L. Assembly of ER-associated protein degradation in vitro: dependence on cytosol, calnexin, and ATP. J Cell Biol 1996, 132:291-298.
96. Werner E.D., Brodsky J.L., McCracken A.A. Proteasome-dependent endoplasmic reticulum-associated protein degradation: an unconventional route to a familiar fate. Proc Natl Acad Sci U S A 1996, 93:13797-13801.
97. Pilon M., Schekman R., Romisch K. Sec61p mediates export of a misfolded secretory protein from the endoplasmic reticulum to the cytosol for degradation. EMBO J 1997, 16:4540-4548.
98. 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.
99. Wahlman J., DeMartino G.N., Skach W.R., Bulleid N.J., Brodsky J.L., Johnson A.E. Real-time fluorescence detection of ERAD substrate retrotranslocation in a mammalian in vitro system. Cell 2007, 129:943-955.
100. Gusarova V., Caplan A.J., Brodsky J.L., Fisher E.A. Apoprotein B degradation is promoted by the molecular chaperones hsp90 and hsp70. J Biol Chem 2001, 276:24891-24900.
101. Schmitz A., Herrgen H., Winkeler A., Herzog V. Cholera toxin is exported from microsomes by the Sec61p complex. J Cell Biol 2000, 148:1203-1212.
102. Moore P., He K., Tsai B. Establishment of an in vitro transport assay that reveals mechanistic differences in cytosolic events controlling cholera toxin and T-cell receptor alpha retro-translocation. PLoS One 2013, 8:e75801.
103. Sato S., Ward C.L., Kopito R.R. Cotranslational ubiquitination of cystic fibrosis transmembrane conductance regulator in vitro. J Biol Chem 1998, 273:7189-7192.
104. Xiong X., Chong E., Skach W.R. Evidence that endoplasmic reticulum (ER)-associated degradation of cystic fibrosis transmembrane conductance regulator is linked to retrograde translocation from the ER membrane. J Biol Chem 1999, 274:2616-2624.
105. Oberdorf J., Carlson E.J., Skach W.R. Uncoupling proteasome peptidase and ATPase activities results in cytosolic release of an ER polytopic protein. J Cell Sci 2006, 119:303-313.
106. Carlson E.J., Pitonzo D., Skach W.R. p97 functions as an auxiliary factor to facilitate TM domain extraction during CFTR ER-associated degradation. EMBO J 2006, 25:4557-4566.
107. Garza R.M., Sato B.K., Hampton R.Y. In vitro analysis of Hrd1p-mediated retrotranslocation of its multispanning membrane substrate 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase. J Biol Chem 2009, 284:14710-14722.
108. Elsabrouty R., Jo Y., Dinh T.T., DeBose-Boyd R.A. Sterol-induced dislocation of 3-hydroxy-3-methylglutaryl coenzyme A reductase from membranes of permeabilized cells. Mol Biol Cell 2013, 24:3300-3308.
109. Nakatsukasa K., Huyer G., Michaelis S., Brodsky J.L. Dissecting the ER-associated degradation of a misfolded polytopic membrane protein. Cell 2008, 132:101-112.
110. Zhang Z.R., Bonifacino J.S., Hegde R.S. Deubiquitinases sharpen substrate discrimination during membrane protein degradation from the ER. Cell 2013, 154:609-622.
111. Shamu C.E., Flierman D., Ploegh H.L., Rapoport T.A., Chau V. Polyubiquitination is required for US11-dependent movement of MHC class I heavy chain from endoplasmic reticulum into cytosol. Mol Biol Cell 2001, 12:2546-2555.
112. Furman M.H., Ploegh H.L., Tortorella D. Membrane-specific, host-derived factors are required for US2- and US11-mediated degradation of major histocompatibility complex class I molecules. J Biol Chem 2002, 277:3258-3267.
113. Cabantous S., Terwilliger T.C., Waldo G.S. Protein tagging and detection with engineered self-assembling fragments of green fluorescent protein. Nat Biotechnol 2005, 23:102-107.
114. Zhong Y., Fang S. Live cell imaging of protein dislocation from the endoplasmic reticulum. J Biol Chem 2012, 287:28057-28066.
115. Grotzke J.E., Lu Q., Cresswell P. Deglycosylation-dependent fluorescent proteins provide unique tools for the study of ER-associated degradation. Proc Natl Acad Sci U S A 2013, 110:3393-3398.
116. Xu C., Wang S., Thibault G., Ng D.T. Futile protein folding cycles in the ER are terminated by the unfolded protein O-mannosylation pathway. Science 2013, 340:978-981.
117. Hipp M.S., Bersuker K., Kopito R.R. Live-cell imaging of ubiquitin-proteasome system function. Methods Mol Biol 2012, 832:463-472.