Mechanisms for quality control of misfolded transmembrane proteins

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 4, 2012, Pages 1108-1114

  Houck, Scott A ^a   Cyr, Douglas M ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Autophagy; Membrane chaperone; Protein folding; Quality control; Transmembrane protein

Indexed keywords

CHAPERONE; DERLIN 1; ESCHERICHIA COLI PROTEIN; FUNGAL PROTEIN; MEMBRANE PROTEIN; PROTEIN BAP29; PROTEIN BAP31; PROTEIN HRD1; PROTEIN SHR3P; PROTEIN YIDC; TRANSLOCON; TRANSMEMBRANE CONDUCTANCE REGULATOR; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

AUTOPHAGY; BIOACCUMULATION; ENDOPLASMIC RETICULUM; ENZYME SUBSTRATE; ESCHERICHIA COLI; HUMAN; MEMBRANE BIOLOGY; MEMBRANE STRUCTURE; MOLECULAR MODEL; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN DEFECT; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN UNFOLDING; QUALITY CONTROL; REVIEW;

ANIMALS; AUTOPHAGY; HUMANS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; PROTEIN FOLDING; PROTEIN STRUCTURE, QUATERNARY;

EID: 84857648264     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.11.007     Document Type: Review

References (87)

1. J.L. Goeckeler, and J.L. Brodsky Molecular chaperones and substrate ubiquitination control the efficiency of endoplasmic reticulum-associated degradation Diabetes Obes. Metab. 12 Suppl 2 2010 32 38
2. 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
3. P. Maattanen, K. Gehring, J.J. Bergeron, and D.Y. Thomas Protein quality control in the ER: the recognition of misfolded proteins Semin. Cell Dev. Biol. 21 2010 500 511
4. T. Tatsuta Protein quality control in mitochondria J. Biochem. 146 2009 455 461
5. P. Arvan, X. Zhao, J. Ramos-Castaneda, and A. Chang Secretory pathway quality control operating in Golgi, plasmalemmal, and endosomal systems Traffic 3 2002 771 780
6. D.M. Cyr, J. Hohfeld, and C. Patterson Protein quality control: U-box-containing E3 ubiquitin ligases join the fold Trends Biochem. Sci. 27 2002 368 375
7. N. Beglova, and S.C. Blacklow The LDL receptor: how acid pulls the trigger Trends Biochem. Sci. 30 2005 309 317
8. C.R. Sanders, and J.K. Myers Disease-related misassembly of membrane proteins Annu. Rev. Biophys. Biomol. Struct. 33 2004 25 51
9. H.F. Mendes, J. van der Spuy, J.P. Chapple, and M.E. Cheetham Mechanisms of cell death in rhodopsin retinitis pigmentosa: implications for therapy Trends Mol. Med. 11 2005 177 185
10. B.P. O'Sullivan, and S.D. Freedman Cystic fibrosis Lancet 373 2009 1891 1904
11. D.G. Bichet Nephrogenic diabetes insipidus Adv. Chronic Kidney Dis. 13 2006 96 104
12. J.A. Janovick, G. Maya-Nunez, and P.M. Conn Rescue of hypogonadotropic hypogonadism-causing and manufactured GnRH receptor mutants by a specific protein-folding template: misrouted proteins as a novel disease etiology and therapeutic target J. Clin. Endocrinol. Metab. 87 2002 3255 3262
13. S. Shao, and R.S. Hegde Membrane protein insertion at the endoplasmic reticulum Annu. Rev. Cell Dev. Biol. 27 2010 25 26
14. R. Beckmann, D. Bubeck, R. Grassucci, P. Penczek, A. Verschoor, G. Blobel, and J. Frank Alignment of conduits for the nascent polypeptide chain in the ribosome-Sec61 complex Science 278 1997 2123 2126
15. D. Gorlich, E. Hartmann, S. Prehn, and T.A. Rapoport A protein of the endoplasmic reticulum involved early in polypeptide translocation Nature 357 1992 47 52
16. D. Gorlich, and T.A. Rapoport Protein translocation into proteoliposomes reconstituted from purified components of the endoplasmic reticulum membrane Cell 75 1993 615 630
17. W.R. Skach The expanding role of the ER translocon in membrane protein folding J. Cell Biol. 179 2007 1333 1335
18. T.A. Rapoport, V. Goder, S.U. Heinrich, and K.E. Matlack Membrane-protein integration and the role of the translocation channel Trends Cell Biol. 14 2004 568 575
19. R.S. Hegde, and V.R. Lingappa Membrane protein biogenesis: regulated complexity at the endoplasmic reticulum Cell 91 1997 575 582
20. Y. Kida, F. Morimoto, and M. Sakaguchi Two translocating hydrophilic segments of a nascent chain span the ER membrane during multispanning protein topogenesis J. Cell Biol. 179 2007 1441 1452
21. A.H. Delcour Structure and function of pore-forming beta-barrels from bacteria J. Mol. Microbiol. Biotechnol. 4 2002 1 10
22. R. Chen, and U. Henning A periplasmic protein (Skp) of Escherichia coli selectively binds a class of outer membrane proteins Mol. Microbiol. 19 1996 1287 1294
23. L.K. Tamm, H. Hong, and B. Liang Folding and assembly of beta-barrel membrane proteins Biochim. Biophys. Acta 1666 2004 250 263
24. C. Hirsch, R. Gauss, S.C. Horn, O. Neuber, and T. Sommer The ubiquitylation machinery of the endoplasmic reticulum Nature 458 2009 453 460
25. M. Kikkert, R. Doolman, M. Dai, R. Avner, G. Hassink, S. van Voorden, S. Thanedar, J. Roitelman, V. Chau, and E. Wiertz Human HRD1 is an E3 ubiquitin ligase involved in degradation of proteins from the endoplasmic reticulum J. Biol. Chem. 279 2004 3525 3534
26. R.G. Gardner, G.M. Swarbrick, N.W. Bays, S.R. Cronin, S. Wilhovsky, L. Seelig, C. Kim, and R.Y. Hampton Endoplasmic reticulum degradation requires lumen to cytosol signaling. Transmembrane control of Hrd1p by Hrd3p J. Cell Biol. 151 2000 69 82
27. R. Gauss, T. Sommer, and E. Jarosch The Hrd1p ligase complex forms a linchpin between ER-lumenal substrate selection and Cdc48p recruitment EMBO J. 25 2006 1827 1835
28. S. Fang, M. Ferrone, C. Yang, J.P. Jensen, S. Tiwari, and A.M. Weissman 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. 98 2001 14422 14427
29. Y.H. Yamamoto, T. Kimura, S. Momohara, M. Takeuchi, T. Tani, Y. Kimata, H. Kadokura, and K. Kohno A novel ER J-protein DNAJB12 accelerates ER-associated degradation of membrane proteins including CFTR Cell Struct. Funct. 35 2010 107 116
30. 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 CFTR{Delta}F508 Mol. Biol. Cell 22 2011 301 314
31. T. Ravid, S.G. Kreft, and M. Hochstrasser Membrane and soluble substrates of the Doa10 ubiquitin ligase are degraded by distinct pathways EMBO J. 25 2006 533 543
32. A. Neutzner, M. Neutzner, A.S. Benischke, S.W. Ryu, S. Frank, R.J. Youle, and M. Karbowski A systematic search for endoplasmic reticulum (ER) membrane-associated RING finger proteins identifies Nixin/ZNRF4 as a regulator of calnexin stability and ER homeostasis J. Biol. Chem. 286 2011 8633 8643
33. 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
34. D.N. Sheppard, and M.J. Welsh Structure and function of the CFTR chloride channel Physiol. Rev. 79 1999 S23 S45
35. S.H. Cheng, R.J. Gregory, J. Marshall, S. Paul, D.W. Souza, G.A. White, C.R. O'Riordan, and A.E. Smith Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis Cell 63 1990 827 834
36. J.R. Riordan, J.M. Rommens, B. Kerem, N. Alon, R. Rozmahel, Z. Grzelczak, J. Zielenski, S. Lok, N. Plavsic, J.L. Chou, M.L. Drumm, M.C. Iannuzzi, F.S. Collins, and L. Tsui Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA Science 245 1989 1066 1073
37. J.L. Bobadilla, M. Macek Jr., J.P. Fine, and P.M. Farrell Cystic fibrosis: a worldwide analysis of CFTR mutations-correlation with incidence data and application to screening Hum. Mutat. 19 2002 575 606
38. K. Du, M. Sharma, and G.L. Lukacs The DeltaF508 cystic fibrosis mutation impairs domain-domain interactions and arrests post-translational folding of CFTR Nat. Struct. Mol. Biol. 12 2005 17 25
39. G.C. Meacham, Z. Lu, S. King, E. Sorscher, A. Tousson, and D.M. Cyr The Hdj-2/Hsc70 chaperone pair facilitates early steps in CFTR biogenesis EMBO J. 18 1999 1492 1505
40. J.M. Younger, H.Y. Ren, L. Chen, C.Y. Fan, A. Fields, C. Patterson, and D.M. Cyr A foldable CFTR{Delta}F508 biogenic intermediate accumulates upon inhibition of the Hsc70-CHIP E3 ubiquitin ligase J. Cell Biol. 167 2004 1075 1085
41. J.M. Younger, L. Chen, H.Y. Ren, M.F. Rosser, E.L. Turnbull, C.Y. Fan, C. Patterson, and D.M. Cyr Sequential quality-control checkpoints triage misfolded cystic fibrosis transmembrane conductance regulator Cell 126 2006 571 582
42. F. Sun, R. Zhang, X. Gong, X. Geng, P.F. Drain, and R.A. Frizzell Derlin-1 promotes the efficient degradation of the cystic fibrosis transmembrane conductance regulator (CFTR) and CFTR folding mutants J. Biol. Chem. 281 2006 36856 36863
43. D.E. Grove, M.F. Rosser, H.Y. Ren, A.P. Naren, and D.M. Cyr Mechanisms for rescue of correctable folding defects in CFTRDelta F508 Mol. Biol. Cell 20 2009 4059 4069
44. F.U. Hartl, and M. Hayer-Hartl Molecular chaperones in the cytosol: from nascent chain to folded protein Science 295 2002 1852 1858
45. J.U. Bowie Membrane protein folding: how important are hydrogen bonds? Curr. Opin. Struct. Biol. 21 2011 42 49
46. M. Tector, and F.U. Hartl An unstable transmembrane segment in the cystic fibrosis transmembrane conductance regulator EMBO J. 18 1999 6290 6298
47. B.C. Cross, and S. High Dissecting the physiological role of selective transmembrane-segment retention at the ER translocon J. Cell Sci. 122 2009 1768 1777
48. S. Tamborero, M. Vilar, L. Martinez-Gil, A.E. Johnson, and I. Mingarro Membrane insertion and topology of the translocating chain-associating membrane protein (TRAM) J. Mol. Biol. 406 2011 571 582
49. H. Do, D. Falcone, J. Lin, D.W. Andrews, and A.E. Johnson The cotranslational integration of membrane proteins into the phospholipid bilayer is a multistep process Cell 85 1996 369 378
50. S.U. Heinrich, W. Mothes, J. Brunner, and T.A. Rapoport The Sec61p complex mediates the integration of a membrane protein by allowing lipid partitioning of the transmembrane domain Cell 102 2000 233 244
51. J.C. Samuelson, M. Chen, F. Jiang, I. Moller, M. Wiedmann, A. Kuhn, G.J. Phillips, and R.E. Dalbey YidC mediates membrane protein insertion in bacteria Nature 406 2000 637 641
52. S. Nagamori, I.N. Smirnova, and H.R. Kaback Role of YidC in folding of polytopic membrane proteins J. Cell Biol. 165 2004 53 62
53. A. Kuhn, R. Stuart, R. Henry, and R.E. Dalbey The Alb3/Oxa1/YidC protein family: membrane-localized chaperones facilitating membrane protein insertion? Trends Cell Biol. 13 2003 510 516
54. M.E. Haque, L.L. Spremulli, and C.J. Fecko Identification of protein-protein and protein-ribosome interacting regions of the C-terminal tail of human mitochondrial inner membrane protein Oxa1L J. Biol. Chem. 285 2010 34991 34998
55. J. Kota, and P.O. Ljungdahl Specialized membrane-localized chaperones prevent aggregation of polytopic proteins in the ER J. Cell Biol. 168 2005 79 88
56. J. Kota, C.F. Gilstring, and P.O. Ljungdahl Membrane chaperone Shr3 assists in folding amino acid permeases preventing precocious ERAD J. Cell Biol. 176 2007 617 628
57. K. Kanehara, W. Xie, and D.T. Ng Modularity of the Hrd1 ERAD complex underlies its diverse client range J. Cell Biol. 188 2010 707 716
58. 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
59. E.J. Greenblatt, J.A. Olzmann, and R.R. Kopito Derlin-1 is a rhomboid pseudoprotease required for the dislocation of mutant alpha-1 antitrypsin from the endoplasmic reticulum Nat. Struct. Mol. Biol. 18 2011 1147 1152
60. W.W. Schamel, S. Kuppig, B. Becker, K. Gimborn, H.P. Hauri, and M. Reth A high-molecular-weight complex of membrane proteins BAP29/BAP31 is involved in the retention of membrane-bound IgD in the endoplasmic reticulum Proc. Natl. Acad. Sci. U. S. A. 100 2003 9861 9866
61. W.G. Annaert, B. Becker, U. Kistner, M. Reth, and R. Jahn Export of cellubrevin from the endoplasmic reticulum is controlled by BAP31 J. Cell Biol. 139 1997 1397 1410
62. E. Szczesna-Skorupa, and B. Kemper BAP31 is involved in the retention of cytochrome P450 2C2 in the endoplasmic reticulum J. Biol. Chem. 281 2006 4142 4148
63. L.G. Nijtmans, L. de Jong, M. Artal Sanz, P.J. Coates, J.A. Berden, J.W. Back, A.O. Muijsers, H. van der Spek, and L.A. Grivell Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins EMBO J. 19 2000 2444 2451
64. R.R. Kopito Aggresomes, inclusion bodies and protein aggregation Trends Cell Biol. 10 2000 524 530
65. M. Bucciantini, E. Giannoni, F. Chiti, F. Baroni, L. Formigli, J. Zurdo, N. Taddei, G. Ramponi, C.M. Dobson, and M. Stefani Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases Nature 416 2002 507 511
66. M. Stefani, and C.M. Dobson Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution J. Mol. Med. (Berl) 81 2003 678 699
67. H. Snyder, K. Mensah, C. Theisler, J. Lee, A. Matouschek, and B. Wolozin Aggregated and monomeric alpha-synuclein bind to the S6' proteasomal protein and inhibit proteasomal function J. Biol. Chem. 278 2003 11753 11759
68. K. Liberek, A. Lewandowska, and S. Zietkiewicz Chaperones in control of protein disaggregation EMBO J. 27 2008 328 335
69. S. Pankiv, T.H. Clausen, T. Lamark, A. Brech, J.A. Bruun, H. Outzen, A. Overvatn, G. Bjorkoy, and T. Johansen p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy J. Biol. Chem. 282 2007 24131 24145
70. Z. Yang, and D.J. Klionsky Eaten alive: a history of macroautophagy Nat. Cell Biol. 12 2010 814 822
71. J.A. Johnston, C.L. Ward, and R.R. Kopito Aggresomes: a cellular response to misfolded proteins J. Cell Biol. 143 1998 1883 1898
72. J.A. Olzmann, L. Li, and L.S. Chin Aggresome formation and neurodegenerative diseases: therapeutic implications Curr. Med. Chem. 15 2008 47 60
73. L.S. Chin, J.A. Olzmann, and L. Li Parkin-mediated ubiquitin signalling in aggresome formation and autophagy Biochem. Soc. Trans. 38 2010 144 149
74. L. Fu, and E. Sztul ER-associated complexes (ERACs) containing aggregated cystic fibrosis transmembrane conductance regulator (CFTR) are degraded by autophagy Eur. J. Cell Biol. 88 2009 215 226
75. M.S. Gelman, E.S. Kannegaard, and R.R. Kopito A principal role for the proteasome in endoplasmic reticulum-associated degradation of misfolded intracellular cystic fibrosis transmembrane conductance regulator J. Biol. Chem. 277 2002 11709 11714
76. E. Fujita, Y. Kouroku, A. Isoai, H. Kumagai, A. Misutani, C. Matsuda, Y.K. Hayashi, and T. Momoi Two endoplasmic reticulum-associated degradation (ERAD) systems for the novel variant of the mutant dysferlin: ubiquitin/proteasome ERAD(I) and autophagy/lysosome ERAD(II) Hum. Mol. Genet. 16 2007 618 629
77. M. Lu, F. Echeverri, and B.D. Moyer Endoplasmic reticulum retention, degradation, and aggregation of olfactory G-protein coupled receptors Traffic 4 2003 416 433
78. V. Kirkin, D.G. McEwan, I. Novak, and I. Dikic A role for ubiquitin in selective autophagy Mol. Cell 34 2009 259 269
79. T.P. Yao The role of ubiquitin in autophagy-dependent protein aggregate processing Genes Cancer 1 2010 779 786
80. G. Bjorkoy, T. Lamark, A. Brech, H. Outzen, M. Perander, A. Overvatn, H. Stenmark, and T. Johansen p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death J. Cell Biol. 171 2005 603 614
81. A. Iwata, B.E. Riley, J.A. Johnston, and R.R. Kopito HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin J. Biol. Chem. 280 2005 40282 40292
82. V. Kirkin, T. Lamark, Y.S. Sou, G. Bjorkoy, J.L. Nunn, J.A. Bruun, E. Shvets, D.G. McEwan, T.H. Clausen, P. Wild, I. Bilusic, J.P. Theurillat, A. Overvatn, T. Ishii, Z. Elazar, M. Komatsu, I. Dikic, and T. Johansen A role for NBR1 in autophagosomal degradation of ubiquitinated substrates Mol. Cell 33 2009 505 516
83. B.E. Riley, S.E. Kaiser, T.A. Shaler, A.C. Ng, T. Hara, M.S. Hipp, K. Lage, R.J. Xavier, K.Y. Ryu, K. Taguchi, M. Yamamoto, K. Tanaka, N. Mizushima, M. Komatsu, and R.R. Kopito Ubiquitin accumulation in autophagy-deficient mice is dependent on the Nrf2-mediated stress response pathway: a potential role for protein aggregation in autophagic substrate selection J. Cell Biol. 191 2010 537 552
84. J. Zhao, J.J. Brault, A. Schild, P. Cao, M. Sandri, S. Schiaffino, S.H. Lecker, and A.L. Goldberg FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells Cell Metab. 6 2007 472 483
85. T. Kawaguchi, K. Miyazawa, S. Moriya, T. Ohtomo, X.F. Che, M. Naito, M. Itoh, and A. Tomoda Combined treatment with bortezomib plus bafilomycin A1 enhances the cytocidal effect and induces endoplasmic reticulum stress in U266 myeloma cells: crosstalk among proteasome, autophagy-lysosome and ER stress Int. J. Oncol. 38 2011 643 654
86. K.B. Kruse, J.L. Brodsky, and A.A. McCracken 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 17 2006 203 212
87. D.H. Perlmutter Alpha-1-antitrypsin deficiency: importance of proteasomal and autophagic degradative pathways in disposal of liver disease-associated protein aggregates Annu. Rev. Med. 62 2011 333 345