Pathogenic Hijacking of ER-Associated Degradation: Is ERAD Flexible?

Molecular Cell

Volumn 59, Issue 3, 2015, Pages 335-344

  Morito, Daisuke ^a,b   Nagata, Kazuhiro ^a,b  

^a KYOTO SANGYO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CHOLERA TOXIN; CYTOLETHAL DISTENDING TOXIN; ENTEROTOXIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PERTUSSIS TOXIN; POLYPEPTIDE; PSEUDOMONAS EXOTOXIN; RICIN; SHIGA TOXIN; TOXIN; VEROTOXIN; PROTEIN; VIRUS PROTEIN;

ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; HOST CELL; NONHUMAN; PATHOGENESIS; PLASTICITY; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN PROCESSING; PROTEIN QUALITY; QUALITY CONTROL; REVIEW; ANIMAL; CHEMISTRY; CYTOSOL; ENDOPLASMIC RETICULUM; HUMAN; METABOLISM; PATHOLOGY; VIROLOGY; VIRUS; VIRUS INFECTION;

ANIMALS; CYTOSOL; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; HUMANS; PROTEINS; PROTEOLYSIS; VIRAL PROTEINS; VIRUS DISEASES; VIRUSES;

EID: 84938573020     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.06.010     Document Type: Review

References (97)

1. Abujarour R.J., Dalal S., Hanson P.I., Draper R.K. p97 Is in a complex with cholera toxin and influences the transport of cholera toxin and related toxins to the cytoplasm. J.Biol. Chem. 2005, 280:15865-15871.
2. Araki K., Nagata K. Protein folding and quality control in the ER. Cold Spring Harb. Perspect. Biol. 2011, 3:a007526.
3. 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.
4. 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.
5. Blom D., Hirsch C., Stern P., Tortorella D., Ploegh H.L. A glycosylated type I membrane protein becomes cytosolic when peptide: N-glycanase is compromised. EMBO J. 2004, 23:650-658.
6. Boname J.M., Stevenson P.G. MHC class I ubiquitination by a viral PHD/LAP finger protein. Immunity 2001, 15:627-636.
7. Boname J.M., Bloor S., Wandel M.P., Nathan J.A., Antrobus R., Dingwell K.S., Thurston T.L., Smith D.L., Smith J.C., Randow F., Lehner P.J. Cleavage by signal peptide peptidase is required for the degradation of selected tail-anchored proteins. J.Cell Biol. 2014, 205:847-862.
8. Burr M.L., Cano F., Svobodova S., Boyle L.H., Boname J.M., Lehner P.J. HRD1 and UBE2J1 target misfolded MHC class I heavy chains for endoplasmic reticulum-associated degradation. Proc. Natl. Acad. Sci. USA 2011, 108:2034-2039.
9. Burr M.L., van den Boomen D.J., Bye H., Antrobus R., Wiertz E.J., Lehner P.J. MHC class I molecules are preferentially ubiquitinated on endoplasmic reticulum luminal residues during HRD1 ubiquitin E3 ligase-mediated dislocation. Proc. Natl. Acad. Sci. USA 2013, 110:14290-14295.
10. 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.
11. 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.
12. Christianson J.C., Ye Y. Cleaning up in the endoplasmic reticulum: ubiquitin in charge. Nat. Struct. Mol. Biol. 2014, 21:325-335.
13. 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.
14. 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.
15. Crough T., Khanna R. Immunobiology of human cytomegalovirus: from bench to bedside. Clin. Microbiol. Rev. 2009, 22:76-98.
16. Day P.J., Owens S.R., Wesche J., Olsnes S., Roberts L.M., Lord J.M. An interaction between ricin and calreticulin that may have implications for toxin trafficking. J.Biol. Chem. 2001, 276:7202-7208.
17. 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.
18. Ebrahimi B., Dutia B.M., Roberts K.L., Garcia-Ramirez J.J., Dickinson P., Stewart J.P., Ghazal P., Roy D.J., Nash A.A. Transcriptome profile of murine gammaherpesvirus-68 lytic infection. J.Gen. Virol. 2003, 84:99-109.
19. Ellgaard L., Ruddock L.W. The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep. 2005, 6:28-32.
20. Eshraghi A., Dixon S.D., Tamilselvam B., Kim E.J., Gargi A., Kulik J.C., Damoiseaux R., Blanke S.R., Bradley K.A. Cytolethal distending toxins require components of the ER-associated degradation pathway for host cell entry. PLoS Pathog. 2014, 10:e1004295.
21. Geiger R., Andritschke D., Friebe S., Herzog F., Luisoni S., Heger T., Helenius A. BAP31 and BiP are essential for dislocation of SV40 from the endoplasmic reticulum to the cytosol. Nat. Cell Biol. 2011, 13:1305-1314.
22. Greenblatt E.J., Olzmann J.A., Kopito R.R. Derlin-1 is a rhomboid pseudoprotease required for the dislocation of mutant α-1 antitrypsin from the endoplasmic reticulum. Nat. Struct. Mol. Biol. 2011, 18:1147-1152.
23. Hagiwara M., Maegawa K., Suzuki M., Ushioda R., Araki K., Matsumoto Y., Hoseki J., Nagata K., Inaba K. Structural basis of an ERAD pathway mediated by the ER-resident protein disulfide reductase ERdj5. Mol. Cell 2011, 41:432-444.
24. Hartl F.U., Hayer-Hartl M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 2002, 295:1852-1858.
25. Hebert D.N., Bernasconi R., Molinari M. ERAD substrates: which way out?. Semin. Cell Dev. Biol. 2010, 21:526-532.
26. Hegde N.R., Chevalier M.S., Wisner T.W., Denton M.C., Shire K., Frappier L., Johnson D.C. The role of BiP in endoplasmic reticulum-associated degradation of major histocompatibility complex class I heavy chain induced by cytomegalovirus proteins. J.Biol. Chem. 2006, 281:20910-20919.
27. Helenius A., Aebi M. Intracellular functions of N-linked glycans. Science 2001, 291:2364-2369.
28. Helenius A., Aebi M. Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 2004, 73:1019-1049.
29. Herr R.A., Harris J., Fang S., Wang X., Hansen T.H. Role of the RING-CH domain of viral ligase mK3 in ubiquitination of non-lysine and lysine MHC I residues. Traffic 2009, 10:1301-1317.
30. Hershko A., Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 1998, 67:425-479.
31. Hirsch C., Blom D., Ploegh H.L. A role for N-glycanase in the cytosolic turnover of glycoproteins. EMBO J. 2003, 22:1036-1046.
32. Inoue T., Moore P., Tsai B. How viruses and toxins disassemble to enter host cells. Annu. Rev. Microbiol. 2011, 65:287-305.
33. Jiang M., Abend J.R., Tsai B., Imperiale M.J. Early events during BK virus entry and disassembly. J.Virol. 2009, 83:1350-1358.
34. Kida Y., Morimoto F., Sakaguchi M. Two translocating hydrophilic segments of a nascent chain span the ER membrane during multispanning protein topogenesis. J.Cell Biol. 2007, 179:1441-1452.
35. 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.
36. Kothe M., Ye Y., Wagner J.S., De Luca H.E., Kern E., Rapoport T.A., Lencer W.I. Role of p97 AAA-ATPase in the retrotranslocation of the cholera toxin A1 chain, a non-ubiquitinated substrate. J.Biol. Chem. 2005, 280:28127-28132.
37. 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.
38. Li S., Spooner R.A., Allen S.C., Guise C.P., Ladds G., Schnöder T., Schmitt M.J., Lord J.M., Roberts L.M. Folding-competent and folding-defective forms of ricin A chain have different fates after retrotranslocation from the endoplasmic reticulum. Mol. Biol. Cell 2010, 21:2543-2554.
39. Lilley B.N., Ploegh H.L. A membrane protein required for dislocation of misfolded proteins from the ER. Nature 2004, 429:834-840.
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. USA 2005, 102:14296-14301.
41. Lilley B.N., Gilbert J.M., Ploegh H.L., Benjamin T.L. Murine polyomavirus requires the endoplasmic reticulum protein Derlin-2 to initiate infection. J.Virol. 2006, 80:8739-8744.
42. Lindwasser O.W., Chaudhuri R., Bonifacino J.S. Mechanisms of CD4 downregulation by the Nef and Vpu proteins of primate immunodeficiency viruses. Curr. Mol. Med. 2007, 7:171-184.
43. Loureiro J., Ploegh H.L. Antigen presentation and the ubiquitin-proteasome system in host-pathogen interactions. Adv. Immunol. 2006, 92:225-305.
44. 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.
45. Lybarger L., Wang X., Harris M.R., Virgin H.W., Hansen T.H. Virus subversion of the MHC class I peptide-loading complex. Immunity 2003, 18:121-130.
46. Magadán J.G., Bonifacino J.S. Transmembrane domain determinants of CD4 Downregulation by HIV-1 Vpu. J.Virol. 2012, 86:757-772.
47. Magadán J.G., Pérez-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 Pathog. 2010, 6:e1000869.
48. 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.
49. Marsh M., Helenius A. Virus entry: open sesame. Cell 2006, 124:729-740.
50. Mayor T. Navigating the ERAD interaction network. Nat. Cell Biol. 2012, 14:46-47.
51. Mehnert M., Sommer T., Jarosch E. Der1 promotes movement of misfolded proteins through the endoplasmic reticulum membrane. Nat. Cell Biol. 2014, 16:77-86.
52. Meinecke M., Cizmowski C., Schliebs W., Krüger V., Beck S., Wagner R., Erdmann R. The peroxisomal importomer constitutes a large and highly dynamic pore. Nat. Cell Biol. 2010, 12:273-277.
53. Meusser B., Sommer T. Vpu-mediated degradation of CD4 reconstituted in yeast reveals mechanistic differences to cellular ER-associated protein degradation. Mol. Cell 2004, 14:247-258.
54. Moore P., He K., Tsai B. Establishment of an invitro transport assay that reveals mechanistic differences in cytosolic events controlling cholera toxin and T-cell receptor α retro-translocation. PLoS ONE 2013, 8:e75801.
55. 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.
56. 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. S1-S8.
57. Nery F.C., Armata I.A., Farley J.E., Cho J.A., Yaqub U., Chen P., da Hora C.C., Wang Q., Tagaya M., Klein C., et al. TorsinA participates in endoplasmic reticulum-associated degradation. Nat. Commun. 2011, 2:393.
58. Ninagawa S., Okada T., Sumitomo Y., Kamiya Y., Kato K., Horimoto S., Ishikawa T., Takeda S., Sakuma T., Yamamoto T., Mori K. EDEM2 initiates mammalian glycoprotein ERAD by catalyzing the first mannose trimming step. J.Cell Biol. 2014, 206:347-356.
59. Oda Y., Hosokawa N., Wada I., Nagata K. EDEM as an acceptor of terminally misfolded glycoproteins released from calnexin. Science 2003, 299:1394-1397.
60. Oda Y., Okada T., Yoshida H., Kaufman R.J., Nagata K., Mori K. Derlin-2 and Derlin-3 are regulated by the mammalian unfolded protein response and are required for ER-associated degradation. J.Cell Biol. 2006, 172:383-393.
61. Otero J.H., Lizák B., Hendershot L.M. Life and death of a BiP substrate. Semin. Cell Dev. Biol. 2010, 21:472-478.
62. Peaper D.R., Cresswell P. Regulation of MHC class I assembly and peptide binding. Annu. Rev. Cell Dev. Biol. 2008, 24:343-368.
63. Petris G., Casini A., Sasset L., Cesaratto F., Bestagno M., Cereseto A., Burrone O.R. CD4 and BST-2/tetherin proteins retro-translocate from endoplasmic reticulum to cytosol as partially folded and multimeric molecules. J.Biol. Chem. 2014, 289:1-12.
64. Rabinovich E., Kerem A., Fröhlich 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.
65. Rapoport T.A. Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 2007, 450:663-669.
66. Redmann V., Oresic K., Tortorella L.L., Cook J.P., Lord M., Tortorella D. Dislocation of ricin toxin A chains in human cells utilizes selective cellular factors. J.Biol. Chem. 2011, 286:21231-21238.
67. Ruggiano A., Foresti O., Carvalho P. Quality control: ER-associated degradation: protein quality control and beyond. J.Cell Biol. 2014, 204:869-879.
68. Schelhaas M., Malmström J., Pelkmans L., Haugstetter J., Ellgaard L., Grünewald 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.
69. Schmitz A., Herrgen H., Winkeler A., Herzog V. Cholera toxin isexported from microsomes by the Sec61p complex. J.Cell Biol. 2000, 148:1203-1212.
70. Shimizu Y., Okuda-Shimizu Y., Hendershot L.M. Ubiquitylation of an ERAD substrate occurs on multiple types of amino acids. Mol. Cell 2010, 40:917-926.
71. Simpson J.C., Roberts L.M., Römisch K., Davey J., Wolf D.H., Lord J.M. Ricin A chain utilises the endoplasmic reticulum-associated protein degradation pathway to enter the cytosol of yeast. FEBS Lett. 1999, 459:80-84.
72. Slominska-Wojewodzka M., Gregers T.F., Wälchli S., Sandvig K. EDEM is involved in retrotranslocation of ricin from the endoplasmic reticulum to the cytosol. Mol. Biol. Cell 2006, 17:1664-1675.
73. Soetandyo N., Ye Y. The p97 ATPase dislocates MHC class I heavy chain in US2-expressing cells via a Ufd1-Npl4-independent mechanism. J.Biol. Chem. 2010, 285:32352-32359.
74. Spooner R.A., Lord J.M. Ricin trafficking in cells. Toxins (Basel) 2015, 7:49-65.
75. Spooner R.A., Smith D.C., Easton A.J., Roberts L.M., Lord J.M. Retrograde transport pathways utilised by viruses and protein toxins. Virol. J. 2006, 3:26.
76. 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.
77. Stein A., Ruggiano A., Carvalho P., Rapoport T.A. Key steps in ERAD of luminal ER proteins reconstituted with purified components. Cell 2014, 158:1375-1388.
78. Strebel K. HIV accessory proteins versus host restriction factors. Curr. Op. Vir. 2013, 3:692-699.
79. Taylor M., Navarro-Garcia F., Huerta J., Burress H., Massey S., Ireton K., Teter K. Hsp90 is required for transfer of the cholera toxin A1 subunit from the endoplasmic reticulum to the cytosol. J.Biol. Chem. 2010, 285:31261-31267.
80. Tsai B., Qian M. Cellular entry of polyomaviruses. Curr. Top. Microbiol. Immunol. 2010, 343:177-194.
81. Ushioda R., Hoseki J., Araki K., Jansen G., Thomas D.Y., Nagata K. ERdj5 is required as a disulfide reductase for degradation of misfolded proteins in the ER. Science 2008, 321:569-572.
82. van de Weijer M.L., Bassik M.C., Luteijn R.D., Voorburg C.M., Lohuis M.A., Kremmer E., Hoeben R.C., LeProust E.M., Chen S., Hoelen H., et al. A high-coverage shRNA screen identifies TMEM129 as an E3 ligase involved in ER-associated protein degradation. Nat. Commun. 2014, 5:3832.
83. van den Boomen D.J., Timms R.T., Grice G.L., Stagg H.R., Skødt K., Dougan G., Nathan J.A., Lehner P.J. TMEM129 is a Derlin-1 associated ERAD E3 ligase essential for virus-induced degradation of MHC-I. Proc. Natl. Acad. Sci. USA 2014, 111:11425-11430.
84. Vembar S.S., Brodsky J.L. One step at a time: endoplasmic reticulum-associated degradation. Nat. Rev. Mol. Cell Biol. 2008, 9:944-957.
85. 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 invitro system. Cell 2007, 129:943-955.
86. Walczak C.P., Ravindran M.S., Inoue T., Tsai B. A cytosolic chaperone complexes with dynamic membrane J-proteins and mobilizes a nonenveloped virus out of the endoplasmic reticulum. PLoS Pathog. 2014, 10:e1004007.
87. Walter P., Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 2011, 334:1081-1086.
88. 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.
89. 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.
90. Wernick N.L., Chinnapen D.J., Cho J.A., Lencer W.I. Cholera toxin: an intracellular journey into the cytosol by way of the endoplasmic reticulum. Toxins (Basel) 2010, 2:310-325.
91. Wiertz E.J., Jones T.R., Sun L., Bogyo M., Geuze H.J., Ploegh H.L. The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 1996, 84:769-779.
92. Wiertz E.J., Tortorella D., Bogyo M., Yu J., Mothes W., Jones T.R., Rapoport T.A., Ploegh H.L. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 1996, 384:432-438.
93. Williams J.M., Inoue T., Banks L., Tsai B. The ERdj5-Sel1L complex facilitates cholera toxin retrotranslocation. Mol. Biol. Cell 2013, 24:785-795.
94. 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.
95. 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.
96. Ye Y., Shibata Y., Kikkert M., van Voorden S., Wiertz E., Rapoport T.A. Recruitment of the p97 ATPase and ubiquitin ligases to the site of retrotranslocation at the endoplasmic reticulum membrane. Proc. Natl. Acad. Sci. USA 2005, 102:14132-14138.
97. 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.