The oxidative folding and misfolding of human leukocyte antigen-B27

Antioxidants and Redox Signaling

Volumn 15, Issue 3, 2011, Pages 669-684

  Antoniou, Antony N ^a   Guiliano, David B ^a   Lenart, Izabela ^a   Burn, Garth ^a   Powis, Simon J ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; CALNEXIN; CALRETICULIN; HLA B27 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEIN P57; TAPASIN;

AUTOIMMUNE DISEASE; B LYMPHOCYTE; BIOSYNTHESIS; DIMERIZATION; HEAVY CHAIN; HUMAN; IMMUNE RESPONSE; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; OXIDATION; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FOLDING; REVIEW; SPONDYLOARTHROPATHY; T LYMPHOCYTE;

BETA 2-MICROGLOBULIN; CYSTEINE; DISULFIDES; HISTOCOMPATIBILITY ANTIGENS CLASS II; HISTOCOMPATIBILITY TESTING; HLA-B27 ANTIGEN; HUMANS; LYMPHOCYTES; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEOSTASIS DEFICIENCIES; SPONDYLARTHROPATHIES;

EID: 79960016957     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2010.3692     Document Type: Review

References (159)

1. Alberts P, Daumke O, Deverson EV, Howard JC, and Knittler MR. Distinct functional properties of the TAP subunits coordinate the nucleotide-dependent transport cycle. Curr Biol 11: 242-251, 2001. (Pubitemid 32185326)
2. Allen RL, O'Callaghan CA, McMichael A, and Bowness P. HLA-B27 forms a novel heavy chain homodimer structure. J Immunol 162: 5045-5048, 1999.
3. Allen RL, Raine T, Haude A, Trowsdale J, and Wilson MJ. Leukocyte receptor complex-encoded immunomodulatory receptors show differing specificity for alternative HLA-B27 structures. J Immunol 167: 5543-5547, 2001. (Pubitemid 33062742)
4. Alvarez I, Marti M, Vazquez J, Camafeita E, Ogueta S, and Lopez de Castro JA. The Cys-67 residue of HLA-B27 in-fluences cell surface stability, peptide specificity, and T-cell antigen presentation. J Biol Chem 276: 48740-48747, 2001.
5. Antoniou AN, Ford S, Alphey M, Osborne A, Elliott T, and Powis SJ. The oxidoreductase ERp57 efficiently reduces partially folded in preference to fully folded MHC class I molecules. EMBO J 21: 2655-2663, 2002. (Pubitemid 34619381)
6. Antoniou AN, Ford S, Pilley ES, Blake N, and Powis SJ. Interactions formed by individually expressed TAP1 and TAP2 polypeptide subunits. Immunology 106: 182-189, 2002. (Pubitemid 34621826)
7. Antoniou AN, Ford S, Taurog JD, Butcher GW, and Powis SJ. Formation of HLA-B27 homodimers and their relation-ship to assembly kinetics. J Biol Chem 279: 8895-8902, 2004. (Pubitemid 38295950)
8. Antoniou AN and Powis SJ. Characterization of the ERp57-tapasin complex by rapid cellular acidification and thiol modification. Antioxid Redox Signal 5: 375-379, 2003. (Pubitemid 37087396)
9. Antoniou AN and Powis SJ. Pathogen evasion strategies for the major histocompatibility complex class I assembly pathway. Immunology 124: 1-12, 2008. (Pubitemid 351537581)
10. Antoniou AN, Powis SJ, and Elliott T. Assembly and export of MHC class I peptide ligands. Curr Opin Immunol 15: 75-81, 2003. (Pubitemid 35454196)
11. Antoniou AN, Santos SG, Campbell EC, Lynch S, Arosa FA, and Powis SJ. ERp57 interacts with conserved cysteine residues in the MHC class I peptide-binding groove. FEBS Lett 581: 1988-1992, 2007. (Pubitemid 46670128)
12. Archer JR and Whelan MA. HLA-B27 and effector T cells: arthritogenic peptide or arthritogenic antigen? Lancet 342: 1307, 1993. (Pubitemid 23338812)
13. Archer JR, Whelan MA, Badakere SS, McLean IL, Archer IV, and Winrow VR. Effect of a free sulphydryl group on expression of HLA-B27 specificity. Scand J Rheumatol Suppl 87: 44-50, 1990.
14. Aslund F, Berndt KD, and Holmgren A. Redox potentials of glutaredoxins and other thiol-disulfide oxidoreductases of the thioredoxin superfamily determined by direct pro-tein-protein redox equilibria. J Biol Chem 272: 30780-30786, 1997. (Pubitemid 27527515)
15. Austin CD, Wen X, Gazzard L, Nelson C, Scheller RH, and Scales SJ. Oxidizing potential of endosomes and lysosomes limits intracellular cleavage of disulfide-based antibody-drug conjugates. Proc Natl Acad SciUS A 102:17987-17992, 2005. (Pubitemid 41798489)
16. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, and Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2: 326-332,2000.
17. Bird LA, Peh CA, Kollnberger S, Elliott T, McMichael AJ, and Bowness P. Lymphoblastoid cells express HLA-B27 homodimers both intracellularly and at the cell surface following endosomal recycling. Eur J Immunol 33: 748-759, 2003. (Pubitemid 36367678)
18. Blanchard N and Shastri N. Coping with loss of perfection in the MHC class I peptide repertoire. Curr Opin Immunol 20: 82-88, 2008.
19. Blanco-Gelaz MA, Suarez-Alvarez B, Diaz-Pena R, and Lopez-Larrea C. HLA-B27 polymorphism at position 116 critically influences the association with TAP/tapasin, in-tracellular trafficking and conformational homodimers formation. Mol Immunol 46: 1304-1311, 2009.
20. Boyson JE, Erskine R, Whitman MC, Chiu M, Lau JM, Koopman LA, Valter MM, Angelisova P, Horejsi V, and Strominger JL. Disulfide bond-mediated dimerization of HLA-G on the cell surface. Proc Natl Acad Sci USA 99: 16180-16185, 2002. (Pubitemid 35462769)
21. Breban M, Hacquard-Bouder C, and Falgarone G. Animal models of HLA-B27-associated diseases. Curr Mol Med 4: 31-40, 2004.
22. Breban M, Hammer RE, Richardson JA, and Taurog JD. Transfer of the inflammatory disease of HLA-B27 trans-genic rats by bone marrow engraftment. J Exp Med 178: 1607-1616., 1993. (Pubitemid 23318439)
23. Brewerton DA, Caffrey M, Nicholls A, Walters D, Oates JK, and James DC Reiter's disease and HL-A 27. Lancet 2: 996-998, 1973.
24. Brewerton DA, Hart FD, Nicholls A, Caffrey M, James DC, and Sturrock RD. Ankylosing spondylitis and HL-A 27. Lancet 1: 904-907, 1973.
25. Brown MA. Breakthroughs in genetic studies of ankylosing spondylitis. Rheumatology (Oxford) 47: 132-137, 2008. (Pubitemid 351168219)
26. Burr ML, Cano F, Svobodova S, Boyle LH, Boname JM, and Lehner PJ. HRD1 and UBE2J1 target misfolded MHC class I heavy chains for endoplasmic reticulum-associated degradation. Proc Natl Acad Sci USA 108: 2034-2039, 2011.
27. Burton PR, Clayton DG, Cardon LR, Craddock N, De-loukas P, Duncanson A, Kwiatkowski DP, McCarthy MI, Ouwehand WH, Samani NJ, Todd JA, Donnelly P, Barrett JC, Davison D, Easton D, Evans DM, Leung HT, Marchini JL, Morris AP, Spencer CC, Tobin MD, Attwood AP, Boorman JP, Cant B, Everson U, Hussey JM, Jolley JD, Knight AS, Koch K, Meech E, Nutland S, Prowse CV, Stevens HE, Taylor NC, Walters GR, Walker NM, Wat-kins NA, Winzer T, Jones RW, McArdle WL, Ring SM, Strachan DP, Pembrey M, Breen G, St Clair D, Caesar S, Gordon-Smith K, Jones L, Fraser C, Green EK, Grozeva D, Hamshere ML, Holmans PA, Jones IR, Kirov G, Moskivina V, Nikolov I, O'Donovan MC, Owen MJ, Collier DA, Elkin A, Farmer A, Williamson R, McGuffin P, Young AH, Ferrier IN, Ball SG, Balmforth AJ, Barrett JH, Bishop TD, Iles MM, Maqbool A, Yuldasheva N, Hall AS, Braund PS, Dixon RJ, Mangino M, Stevens S, Thompson JR, Bredin F, Tremelling M, Parkes M, Drummond H, Lees CW, Nimmo ER, Satsangi J, Fisher SA, Forbes A, Lewis CM, Onnie CM, Prescott NJ, San-derson J, Matthew CG, Barbour J, Mohiuddin MK, Tod-hunter CE, Mansfield JC, Ahmad T, Cummings FR, Jewell DP, et al. Association scan of 14,500 nonsynonymous SNPs in four diseases identifies autoimmunity variants. Nat Genet 39: 1329-1337, 2007. (Pubitemid 350041542)
28. Capps GG, Robinson BE, Lewis KD, and Zuniga MC. In vivo dimeric association of class I MHC heavy chains. Possible relationship to class I MHC heavy chain-beta 2-microglobulin dissociation. J Immunol 151: 159-169, 1993. (Pubitemid 23206981)
29. Chambers JE, Jessop CE, and Bulleid NJ. Formation of a major histocompatibility complex class I tapasin disulfide indicates a change in spatial organization of the peptide-loading complex during assembly. J Biol Chem 283 1862-1869. 2008.
30. Colbert RA. HLA-B27 misfolding: a solution to the spon-dyloarthropathy conundrum? [In Process Citation]. Mol Med Today 6: 224-230, 2000.
31. Colbert RA, DeLay ML, Klenk EI, and Layh-Schmitt G From HLA-B27 to spondyloarthritis: a journey through the ER. Immunol Rev 233: 181-202, 2010.
32. Colonna M, Navarro F, Bellon T, Llano M, Garcia P, Sa-maridis J, Angman L, Cella M, and Lopez-Botet M. A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and mye-lomonocytic cells. J Exp Med 186: 1809-1818, 1997. (Pubitemid 27524591)
33. Colonna M, Samaridis J, Cella M, Angman L, Allen RL, O'Callaghan CA, Dunbar R, Ogg GS, Cerundolo V, and Rolink A. Human myelomonocytic cells express an inhibi-tory receptor for classical and nonclassical MHC class I molecules. J Immunol 160: 3096-3100, 1998. (Pubitemid 28164696)
34. Cormier JH, Tamura T, Sunryd JC, and Hebert DN. EDEM1 recognition and delivery of misfolded proteins to the SEL1L-containing ERAD complex. Mol Cell 34: 627-633, 2009.
35. Cresswell P and Dawson JR. Dimeric and monomeric forms of HL-A antigens solubilized by detergent. J Immunol 114: 523-525, 1975.
36. Dangoria NS, DeLay ML, Kingsbury DJ, Mear JP, Uchanska-Ziegler B, Ziegler A, and Colbert RA. HLA-B27 misfolding is associated with aberrant intermolecular dis-ulfide bond formation (dimerization) in the endoplasmic reticulum. J Biol Chem 277: 23459-23468, 2002. (Pubitemid 34952180)
37. Degen E, Cohen-Doyle MF, and Williams DB. Efficient dissociation of the p88 chaperone from major histocom-patibility complex class I molecules requires both beta 2-microglobulin and peptide. J Exp Med 175: 1653-1661,1992.
38. Dick TP, Bangia N, Peaper DR, and Cresswell P. Disulfide bond isomerization and the assembly of MHC class I-peptide complexes. Immunity 16: 87-98, 2002. (Pubitemid 34143219)
39. Dong G, Wearsch PA, Peaper DR, Cresswell P, and Re-inisch KM. Insights into MHC class I peptide loading from the structure of the tapasin-ERp57 thiol oxidoreductase heterodimer. Immunity 30: 21-32, 2009.
40. Dong M, Bridges JP, Apsley K, Xu Y, and Weaver TE. ERdj4 and ERdj5 are required for endoplasmic reticulum-associated protein degradation of misfolded surfactant protein C. Mol Biol Cell 19: 2620-2630, 2008.
41. Ellgaard L and Frickel EM. Calnexin, calreticulin, and ERp57: teammates in glycoprotein folding. Cell Biochem Biophys 39: 223-247, 2003. (Pubitemid 41270793)
42. Elliott T and Williams A. The optimization of peptide cargo bound to MHC class I molecules by the peptide-loading complex. Immunol Rev 207: 89-99, 2005. (Pubitemid 41415010)
43. Fabian H, Huser H, Loll B, Ziegler A, Naumann D, and Uchanska-Ziegler B. HLA-B27 heavy chains distinguished by a micropolymorphism exhibit differential flexibility. Arthritis Rheum 62: 978-987, 2010.
44. Fabian H, Huser H, Narzi D, Misselwitz R, Loll B, Ziegler A, Bockmann RA, Uchanska-Ziegler B, and Naumann D. HLA-B27 subtypes differentially associated with disease exhibit conformational differences in solution. J Mol Biol 376: 798-810, 2008.
45. Frenkel Z, Shenkman M, Kondratyev M, and Lederkremer GZ. Separate roles and different routing of calnexin and ERp57 in endoplasmic reticulum quality control revealed by interactions with asialoglycoprotein receptor chains. Mol Biol Cell 15: 2133-2142, 2004. (Pubitemid 38580633)
46. Fussell H, Nesbeth D, Lenart I, Campbell EC, Lynch S, Santos S, Gould K, Powis SJ, and Antoniou AN. Novel detection of in vivo HLA-B27 conformations correlates with ankylosing spondylitis association. Arthritis Rheum 58: 3419-3424, 2008.
47. Galocha B and Lopez de Castro JA. Mutational analysis reveals a complex interplay of peptide binding and multi-ple biological features of HLA-B27. J Biol Chem 285: 39180-39190, 2010.
48. Gao B, Adhikari R, Howarth M, Nakamura K, Gold MC, Hill AB, Knee R, Michalak M, and Elliott T. Assembly and antigen-presenting function of MHC class I molecules in cells lacking the ER chaperone calreticulin. Immunity 16: 99-109, 2002. (Pubitemid 34143220)
49. Garbi N, Tanaka S, Momburg F, and Hammerling GJ. Im-paired assembly of the major histocompatibility complex class I peptide-loading complex in mice deficient in the oxidoreductase ERp57. Nat Immunol 7: 93-102, 2006. (Pubitemid 41823873)
50. Gewurz BE, Gaudet R, Tortorella D, Wang EW, Ploegh HL, and Wiley DC Antigen presentation subverted: structure of the human cytomegalovirus protein US2 bound to the class I molecule HLA-A2. Proc Natl Acad SciUSA 98: 6794-6799, 2001. (Pubitemid 32538296)
51. Gewurz BE, Wang EW, Tortorella D, Schust DJ, and Ploegh HL. Human cytomegalovirus US2 endoplasmic reticulum-lumenal domain dictates association with major histocom-patibility complex class I in a locus-specific manner. J Virol 75: 5197-5204, 2001. (Pubitemid 32448542)
52. Gruda R, Achdout H, Stern-Ginossar N, Gazit R, Betser-Cohen G, Manaster I, Katz G, Gonen-Gross T, Tirosh B, and Mandelboim O. Intracellular cysteine residues in the tail of MHC class I proteins are crucial for extracellular recogni-tion by leukocyte Ig-like receptor 1. J Immunol 179: 3655-3661, 2007.
53. Hammer GE, Gonzalez F, Champsaur M, Cado D, and Shastri N. The aminopeptidase ERAAP shapes the peptide repertoire displayed by major histocompatibility complex class I molecules. Nat Immunol 7: 103-112, 2006. (Pubitemid 41823874)
54. Hammer GE, Gonzalez F, James E, Nolla H, and Shastri N. In the absence of aminopeptidase ERAAP, MHC class I molecules present many unstable and highly immunogenic peptides. Nat Immunol 8: 101-108, 2007. (Pubitemid 46242364)
55. Hammer RE, Maika SD, Richardson JA, Tang JP, and Taurog JD. Spontaneous inflammatory disease in trans-genic rats expressing HLA-B27 and human beta 2m: an animal model of HLA-B27-associated human disorders. Cell 63: 1099-1112, 1990. (Pubitemid 120034950)
56. Hammond C, Braakman I, and Helenius A. Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control. Proc Natl Acad Sci USA 91: 913-917, 1994. (Pubitemid 24048478)
57. Hammond C and Helenius A. Folding of VSV G protein sequential interaction with BiP and calnexin. Science 266: 456-458, 1994. (Pubitemid 24348968)
58. Harris MR, Yu YY, Kindle CS, Hansen TH, and Solheim JC. Calreticulin and calnexin interact with different protein and glycan determinants during the assembly of MHC class I. J Immunol 160: 5404-5409, 1998. (Pubitemid 28267830)
59. Hebert DN and Molinari M. In and out of the ER: protein folding, quality control, degradation, and related human diseases. Physiol Rev 87: 1377-1408, 2007. (Pubitemid 350041473)
60. Hellman R, Vanhove M, Lejeune A, Stevens FJ, and Hen-dershot LM. The in vivo association of BiP with newly synthesized proteins is dependent on the rate and stability of folding and not simply on the presence of sequences that can bind to BiP. J Cell Biol 144: 21-30, 1999. (Pubitemid 29047008)
61. Hendershot LM. The ER function BiP is a master regulator of ER function. Mt Sinai J Med 71: 289-297, 2004.
62. Holbrook LM, Watkins NA, Simmonds AD, Jones CI, Ouwehand WH, and Gibbins JM. Platelets release novel thiol isomerase enzymes which are recruited to the cell surface following activation. Br J Haematol 148: 627-637, 2010.
63. Howe C, Garstka M, Al-Balushi M, Ghanem E, Antoniou AN, Fritzsche S, Jankevicius G, Kontouli N, Schneeweiss C, Williams A, Elliott T, and Springer S. Calreticulin-dependent recycling in the early secretory pathway mediates optimal peptide loading of MHC class I molecules. EMBO J 28: 3730-3744, 2009.
64. Hughes EA and Cresswell P. The thiol oxidoreductase ERp57 is a component of the MHC class I peptide-loading complex. Curr Biol 8: 709-712, 1998. (Pubitemid 28286279)
65. Hulsmeyer M, Fiorillo MT, Bettosini F, Sorrentino R, Saenger W, Ziegler A, and Uchanska-Ziegler B. Dual, HLA-B27 subtype-dependent conformation of a self-peptide. J Exp Med 199: 271-281, 2004. (Pubitemid 38139247)
66. Hwang C, Sinskey AJ, and Lodish HF. Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257: 1496-1502, 1992.
67. Ioannou Y, Zhang JY, Passam FH, Rahgozar S, Qi JC, Giannakopoulos B, Qi M, Yu P, Yu DM, Hogg PJ, and Krilis SA. Naturally occurring free thiols within beta 2-glycoprotein I in vivo: nitrosylation, redox modification by endothelial cells, and regulation of oxidative stress-induced cell injury. Blood 116: 1961-1970.
68. Jackson MR, Cohen-Doyle MF, Peterson PA, and Williams DB. Regulation of MHC class I transport by the molecular chaperone, calnexin (p88, IP90). Science 263: 384-387, 1994.
69. Jessop CE, Chakravarthi S, Garbi N, Hammerling GJ, Lovell S, and Bulleid NJ. ERp57 is essential for efficient folding of glycoproteins sharing common structural do-mains. EMBO J 26: 28-40, 2007. (Pubitemid 46094697)
70. Johnstone RM, Adam M, Hammond JR, Orr L, and Turbide C. Vesicle formation during reticulocyte maturation. As-sociation of plasma membrane activities with released vesicles (exosomes). J Biol Chem 262: 9412-9420, 1987.
71. Kanaseki T, Blanchard N Hammer GE, Gonzalez F, and Shastri N. ERAAP synergizes with MHC class I molecules to make the final cut in the antigenic peptide precursors in the endoplasmic reticulum. Immunity 25: 795-806, 2006. (Pubitemid 46107289)
72. Kang K, Park B, Oh C, Cho K, and Ahn K. A role for protein disulfide isomerase in the early folding and as-sembly of MHC class I molecules. Antioxid Redox Signal 11: 2553-2561, 2009.
73. Kaufman JF, Krangel MS, and Strominger JL. Cysteines in the transmembrane region of major histocompatibility complex antigens are fatty acylated via thioester bonds. J Biol Chem 259: 7230-7238, 1984. (Pubitemid 14077808)
74. Kienast A, Preuss M, Winkler M, and Dick TP. Redox regulation of peptide receptivity of major histocompatibil-ity complex class I molecules by ERp57 and tapasin. Nat Immunol 8: 864-872, 2007. (Pubitemid 47099038)
75. Knittler MR, Alberts P, Deverson EV, and Howard JC. Nucleotide binding by TAP mediates association with peptide and release of assembled MHC class I molecules. Curr Biol 9: 999-1008, 1999. (Pubitemid 29456168)
76. Kollnberger S, Bird L, Sun MY, Retiere C, Braud VM, McMichael A, and Bowness P. Cell-surface expression and immune receptor recognition of HLA-B27 homodimers. Arthritis Rheum 46: 2972-2982, 2002. (Pubitemid 35315891)
77. Kostyu DD, Hannick LI, Traweek JL, Ghanayem M, Heil-pern D, and Dawson DV. HLA class I polymorphism: structure and function and still questions. Hum Immunol 57: 1-18, 1997. (Pubitemid 28023578)
78. Lanier LL. Follow the leader: NK cell receptors for classical and nonclassical MHC class I. Cell 92: 705-707, 1998. (Pubitemid 28155309)
79. Lanier LL. NK cell receptors. Annu Rev Immunol 16: 359-393, 1998. (Pubitemid 28183369)
80. Layh-Schmitt G and Colbert RA. The interleukin-23/inter-leukin-17 axis in spondyloarthritis. Curr Opin Rheumatol 20: 392-397, 2008.
81. Leach MR and Williams DB. Lectin-deficient calnexin is capable of binding class I histocompatibility molecules in vivo and preventing their degradation. J Biol Chem 279: 9072-9079, 2004. (Pubitemid 38295971)
82. Lederkremer GZ. Glycoprotein folding, quality control and ER-associated degradation. Curr Opin Struct Biol 19: 515-523, 2009.
83. Lee S, Park B, Kang K, and Ahn K. Redox-regulated export of the major histocompatibility complex class I-peptide complexes from the endoplasmic reticulum. Mol Biol Cell 20: 3285-3294, 2009.
84. Lehner PJ, Surman MJ, and Cresswell P. Soluble tapasin restores MHC class I expression and function in the tapa-sin-negative cell line.220. Immunity 8: 221-231, 1998. (Pubitemid 28123749)
85. Lewis JW and Elliott T. Evidence for successive peptide binding and quality control stages during MHC class I assembly. Curr Biol 8: 717-720, 1998. (Pubitemid 28286281)
86. Lichterfeld M, Kavanagh DG, Williams KL, Moza B, Mui SK, Miura T, Sivamurthy R, Allgaier R, Pereyra F, Trocha A, Feeney M, Gandhi RT, Rosenberg ES, Altfeld M, Allen TM, Allen R, Walker BD, Sundberg EJ, and Yu XG. A viral CTL escape mutation leading to immunoglobulin-like transcript 4-mediated functional inhibition of myelomono-cytic cells. J Exp Med 204: 2813-2824, 2007. (Pubitemid 350179552)
87. Lindquist JA, Hammerling GJ, and Trowsdale J. ER60/ERp57 forms disulfide-bonded intermediates with MHC class I heavy chain. FASEB J 15: 1448-1450, 2001.
88. Loureiro J, Lilley BN, Spooner E, Noriega V, Tortorella D, and Ploegh HL. Signal peptide peptidase is required for dislocation from the endoplasmic reticulum. Nature 441: 894-897, 2006.
89. Lynch S, Santos SG, Campbell EC, Nimmo AM, Botting C, Prescott A, Antoniou AN, and Powis SJ. NovelMHC class I structures on exosomes. J Immunol 183: 1884-1891, 2009.
90. Ma Y and Hendershot LM. ER chaperone functions during normal and stress conditions. J Chem Neuroanat 28: 51-65, 2004. (Pubitemid 39195252)
91. Maattanen P, Gehring K, Bergeron JJ, and Thomas DY. Protein quality control in the ER: the recognition of mis-folded proteins. Semin Cell Dev Biol 21: 500-511, 2010.
92. Machold RP, Wiertz EJ, Jones TR, and Ploegh HL. The HCMV gene products US11 and US2 differ in their ability to attack allelic forms of murine major histocompatibility complex (MHC) class I heavy chains. J Exp Med 185: 363-366, 1997. (Pubitemid 27078293)
93. Madden DR, Gorga JC, Strominger JL, and Wiley DC The structure of HLA-B27 reveals nonamer self-peptides bound in an extended conformation. Nature 353: 321-325, 1991. (Pubitemid 21912496)
94. Malhotra JD and Kaufman RJ. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal 9: 2277-2293, 2007. (Pubitemid 350059010)
95. Malik P, Klimovitsky P, Deng LW, Boyson JE, and Stro-minger JL. Uniquely conformed peptide-containing beta 2-microglobulin-free heavy chains of HLA-B2705 on the cell surface. J Immunol 169: 4379-4387, 2002. (Pubitemid 35178212)
96. Matlack KE, Misselwitz B, Plath K, and Rapoport TA. BiP acts as a molecular ratchet during posttranslational trans-port of prepro-alpha factor across the ER membrane. Cell 97: 553-564, 1999. (Pubitemid 29256959)
97. Matsuo Y, Masutani H, Son A, Kizaka-Kondoh S, and Yodoi J. Physical and functional interaction of transmem-brane thioredoxin-related protein with major histocom-patibility complex class I heavy chain: redox-based protein quality control and its potential relevance to immune re-sponses. Mol Biol Cell 20: 4552-4562, 2009.
98. McCracken AA and Brodsky JL. Assembly of ER-associated protein degradation in vitro: dependence on cytosol, cal-nexin, and ATP. J Cell Biol 132: 291-298, 1996. (Pubitemid 26052565)
99. McLean L, Perrett D, Winrow VR, and Archer JR. Status of an unpaired thiol group on the HLA-B27 epitope. Clin Exp Immunol 77: 417-421, 1989. (Pubitemid 19234392)
100. Mear JP, Schreiber KL, Munz C, Zhu X, Stevanovic S, Rammensee HG, Rowland-Jones SL, and Colbert RA. Misfolding of HLA-B27 as a result of its B pocket suggests a novel mechanism for its role in susceptibility to spondy-loarthropathies. J Immunol 163: 6665-6670, 1999.
101. Merino E, Galocha B, Vazquez MN, and Lopez de Castro JA. Disparate folding and stability of the ankylosing spondylitis-associated HLA-B*1403 and B*2705 proteins. Arthritis Rheum 58: 3693-3704, 2008.
102. Merino E, Montserrat V, Paradela A, and Lopez de Castro JA. Two HLA-B14 subtypes (B*1402 and B*1403) differen-tially associated with ankylosing spondylitis differ sub-stantially in peptide specificity but have limited peptide and T-cell epitope sharing with HLA-B27. J Biol Chem 280: 35868-35880, 2005. (Pubitemid 41633854)
103. Molinari M, Calanca V, Galli C, Lucca P, and Paganetti P. Role of EDEM in the release of misfolded glycoproteins from the calnexin cycle. Science 299: 1397-1400, 2003. (Pubitemid 36254653)
104. Morrice NA and Powis SJ. A role for the thiol-dependent reductase ERp57 in the assembly of MHC class I molecules. Curr Biol 8: 713-716, 1998. (Pubitemid 28286280)
105. Nejentsev S, Howson JM, Walker NM, Szeszko J, Field SF, Stevens HE, Reynolds P, Hardy M, King E, Masters J, Hulme J, Maier LM, Smyth D, Bailey R, Cooper JD, Ribas G, Campbell RD, Clayton DG, and Todd JA. Localization of type 1 diabetes susceptibility to the MHC class I genes HLA-B and HLA-A. Nature 450: 887-892, 2007. (Pubitemid 350231332)
106. Netzer N, Goodenbour JM, David A, Dittmar KA, Jones RB, Schneider JR, Boone D, Eves EM, Rosner MR, Gibbs JS, Embry A, Dolan B, Das S, Hickman HD, Berglund P, Bennink JR, Yewdell JW, and Pan T. Innate immune and chemically triggered oxidative stress modifies translational fidelity. Nature 462: 522-526, 2009.
107. Nossner E and Parham P. Species-specific differences in chaperone interaction of human and mouse major histo-compatibility complex class I molecules. J Exp Med 181: 327-337, 1995.
108. Oda Y, Hosokawa N, Wada I, and Nagata K. EDEM as an acceptor of terminally misfolded glycoproteins released from calnexin. Science 299: 1394-1397, 2003. (Pubitemid 36254652)
109. Oliver JD, Roderick HL, Llewellyn DH, and High S. ERp57 functions as a subunit of specific complexes formed with the ER lectins calreticulin and calnexin. Mol Biol Cell 10: 2573-2582, 1999. (Pubitemid 29393511)
110. Otero JH, Lizak B, and Hendershot LM. Life and death of a BiP substrate. Semin Cell Dev Biol 21: 472-478, 2010.
111. Park B, Kim Y, Shin J, Lee S, Cho K, Fruh K, and Ahn K. Human cytomegalovirus inhibits tapasin-dependent peptide loading and optimization of the MHC class I peptide cargo for immune evasion. Immunity 20: 71-85, 2004. (Pubitemid 38134295)
112. Park B, Lee S, Kim E, and Ahn K. A single polymorphic residue within the peptide-binding cleft of MHC class I molecules determines spectrum of tapasin dependence. J Immunol 170: 961-968, 2003. (Pubitemid 36070550)
113. Park B, Lee S, Kim E, Cho K, Riddell SR, Cho S, and Ahn K. Redox regulation facilitates optimal peptide selection by MHC class I during antigen processing. Cell 127: 369-382, 2006. (Pubitemid 44572373)
114. Peaper DR and Cresswell P. The redox activity of ERp57 is not essential for its functions in MHC class I peptide loading. Proc Natl Acad Sci USA 105: 10477-10482, 2008.
115. Peaper DR, Wearsch PA, and Cresswell P. Tapasin and ERp57 form a stable disulfide-linked dimer within the MHC class I peptide-loading complex. EMBO J 24: 3613-3623, 2005. (Pubitemid 41509368)
116. Peh CA, Burrows SR, Barnden M, Khanna R, Cresswell P, Moss DJ, and McCluskey J. HLA-B27 restricted antigen presentation in the absence of tapasin reveals polymor-phism in mechanisms of HLA class I peptide loading. Im-munity 8: 531-542, 1998. (Pubitemid 28264744)
117. Pollock S, Kozlov G, Pelletier MF, Trempe JF, Jansen G, Sitnikov D, Bergeron JJ, Gehring K, Ekiel I, and Thomas DY. Specific interaction of ERp57 and calnexin determined by NMR spectroscopy and an ER two-hybrid system EMBO J 23: 1020-1029, 2004. (Pubitemid 38436867)
118. Powis SJ, Nesbeth D, Lenart I, Fussell H, Lamb T, Gould K, and Antoniou AN. Rapid acidification and alkylation: re-dox analysis of the MHC class I pathway. J Immunol Methods 340: 81-85, 2009.
119. Ramos M and Lopez de Castro JA. HLA-B27 and the pathogenesis of spondyloarthritis. Tissue Antigens 60: 191-205, 2002. (Pubitemid 35398822)
120. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, and Geuze HJ. B lymphocytes se-crete antigen-presenting vesicles. J Exp Med 183: 1161-1172, 1996.
121. Ruddock LW and Molinari M. N-glycan processing in ER quality control. J Cell Sci 119: 4373-4380, 2006. (Pubitemid 44830636)
122. Sadasivan B, Lehner PJ, Ortmann B, Spies T, and Cresswell P. Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Im-munity 5: 103-114, 1996. (Pubitemid 26301087)
123. Sadasivan BK, Cariappa A, Waneck GL, and Cresswell P. Assembly, peptide loading, and transport of MHC class I molecules in a calnexin-negative cell line. Cold Spring Harb Symp Quant Biol 60: 267-275, 1995. (Pubitemid 26202037)
124. Saleki K, Hartigan N, Lith M, Bulleid N and Benham AM. Differential oxidation of HLA-B2704 and HLA-B2705 in lymphoblastoid and transfected adherent cells. Antioxid Redox Signal 8: 292-299, 2006. (Pubitemid 43741300)
125. Santos SG, Campbell EC, Lynch S, Wong V, Antoniou AN, and Powis SJ. MHC class I-ERp57-tapasin interactions within the peptide-loading complex. J Biol Chem 282: 17587-17593, 2007. (Pubitemid 47100280)
126. Santos SG, Lynch S, Campbell EC, Antoniou AN, and Po-wis SJ. Induction of HLA-B27 heavy chain homodimer formation after activation in dendritic cells. Arthritis Res Ther 10: R100, 2008.
127. Santos SG, Powis SJ, and Arosa FA. Misfolding of major histocompatibility complex class I molecules in activated T cells allows cis-interactions with receptors and signaling molecules and is associated with tyrosine phosphorylation. J Biol Chem 279: 53062-53070, 2004. (Pubitemid 40051806)
128. Savina A, Jancic C, Hugues S, Guermonprez P, Vargas P, Moura IC, Lennon-Dumenil AM, Seabra MC, Raposo G, and Amigorena S. NOX2 controls phagosomal pH to reg-ulate antigen processing during crosspresentation by den-dritic cells. Cell 126: 205-218, 2006. (Pubitemid 44026552)
129. Schlosstein L, Terasaki PI, Bluestone R, and Pearson CM. High association of an HL-A antigen, W27, with ankylosing spondylitis. N Engl J Med 288: 704-706, 1973.
130. Scott JE and Dawson JR. MHC class I expression and transport in a calnexin-deficient cell line. J Immunol 155: 143-148, 1995.
131. Serwold T, Gonzalez F, Kim J, Jacob R, and Shastri N. ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature 419: 480-483, 2002.
132. Smith JA, Barnes MD, Hong D, DeLay ML, Inman RD, and Colbert RA. Gene expression analysis of macrophages de-rived from ankylosing spondylitis patients reveals inter-feron-gamma dysregulation. Arthritis Rheum 58: 1640-1649, 2008. (Pubitemid 351847516)
133. Smith JA, Turner MJ, DeLay ML, Klenk EI, Sowders DP, and Colbert RA. Endoplasmic reticulum stress and the unfolded protein response are linked to synergistic IFN-beta induction via X-box binding protein 1. Eur J Immunol 38: 1194-1203, 2008.
134. Solda T, Galli C, Kaufman RJ, and Molinari M. Substrate-specific requirements for UGT1-dependent release from calnexin. Mol Cell 27: 238-249, 2007. (Pubitemid 47058298)
135. Sorgjerd K, Ghafouri B, Jonsson BH, Kelly JW, Blond SY, and Hammarstrom P. Retention of misfolded mutant transthyretin by the chaperone BiP/GRP78 mitigates amyloidogenesis. J Mol Biol 356: 469-482, 2006. (Pubitemid 43099984)
136. Stagg HR, Thomas M, van den Boomen D, Wiertz EJ, Drabkin HA, Gemmill RM, and Lehner PJ. The TRC8 E3 ligase ubiquitinates MHC class I molecules before disloca-tion from the ER. J Cell Biol 186: 685-692, 2009.
137. Stam NJ, Spits H, and Ploegh HL. Monoclonal antibodies raised against denatured HLA-B locus heavy chains permit biochemical characterization of certain HLA-C locus products. J Immunol 137: 2299-2306, 1986. (Pubitemid 16020728)
138. Stronge VS, Saito Y, Ihara Y, and Williams DB. Relationship between calnexin and BiP in suppressing aggregation and promoting refolding of protein and glycoprotein substrates. J Biol Chem 276: 39779-39787, 2001.
139. Taurog JD. The mystery of HLA-B27: if it isn't one thing, it's another. Arthritis Rheum 56: 2478-2481, 2007. (Pubitemid 47237266)
140. Taurog JD, Dorris ML, Satumtira N, Tran TM, Sharma R, Dressel R, van den Brandt J, and Reichardt HM. Spondy-larthritis in HLA-B27/human beta2-microglobulin-transgenic rats is not prevented by lack of CD8. Arthritis Rheum 60:1977-1984, 2009.
141. Taurog JD, Maika SD, Satumtira N, Dorris ML, McLean IL, Yanagisawa H, Sayad A, Stagg AJ, Fox GM, Le O'Brien A, Rehman M, Zhou M, Weiner AL, Splawski JB, Richardson JA, and Hammer RE. Inflammatory disease in HLA-B27 transgenic rats. Immunol Rev 169: 209-223, 1999. (Pubitemid 29338734)
142. Tector M and Salter RD. Calnexin influences folding of human class I histocompatibility proteins but not their as-sembly with beta 2-microglobulin. J Biol Chem 270: 19638-19642, 1995.
143. Tector M, Zhang Q, and Salter RD. Beta 2-microglobulin and calnexin can independently promote folding and disulfide bond formation in class I histocompatibility pro-teins. Mol Immunol 34: 401-408, 1997. (Pubitemid 27368336)
144. Tirosh B, Furman MH, Tortorella D, and Ploegh HL. Protein unfolding is not a prerequisite for endoplasmic reticulum-to-cytosol dislocation. J Biol Chem 278: 6664-6672, 2003. (Pubitemid 36800652)
145. Tortorella D, Story CM, Huppa JB, Wiertz EJ, Jones TR, Bacik I, Bennink JR, Yewdell JW, and Ploegh HL. Disloca-tion of type I membrane proteins from the ER to the cytosol is sensitive to changes in redox potential [published erra-tum appears in J Cell Biol 1999 May 3;145(3):following 642]. J Cell Biol 142: 365-376, 1998.
146. Tran TM, Dorris ML, Satumtira N, Richardson JA, Hammer RE, Shang J, and Taurog JD. Additional human beta2-microglobulin curbs HLA-B27 misfolding and promotes arthritis and spondylitis without colitis in male HLA-B27-transgenic rats. Arthritis Rheum 54: 1317-1327, 2006. (Pubitemid 43672945)
147. Tran TM, Satumtira N, Dorris ML, May E, Wang A, Furuta E, and Taurog JD. HLA-B27 in transgenic rats forms dis-ulfide-linked heavy chain oligomers and multimers that bind to the chaperone BiP. JImmunol 172: 5110-5119, 2004. (Pubitemid 38456440)
148. Turner MJ, Delay ML, Bai S, Klenk E, and Colbert RA. HLA-B27 up-regulation causes accumulation of misfolded heavy chains and correlates with the magnitude of the unfolded protein response in transgenic rats: implications for the pathogenesis of spondylarthritis-like disease. Ar-thritis Rheum 56: 215-223, 2006. (Pubitemid 46106195)
149. Turner MJ, Sowders DP, DeLay ML, Mohapatra R, Bai S, Smith JA, Brandewie JR, Taurog JD, and Colbert RA. HLA-B27 misfolding in transgenic rats is associated with acti-vation of the unfolded protein response. J Immunol 175: 2438-2448, 2005. (Pubitemid 41113854)
150. Ushioda R, Hoseki J, Araki K, Jansen G, Thomas DY, and Nagata K. ERdj5 is required as a disulfide reductase for degradation of misfolded proteins in the ER. Science 321: 569-572, 2008.
151. Vassilakos A, Cohen-Doyle MF, Peterson PA, Jackson MR, and Williams DB. The molecular chaperone calnexin facil-itates folding and assembly of class I histocompatibility molecules. EMBO J 15: 1495-1506, 1996. (Pubitemid 26112371)
152. Vembar SS and Brodsky JL. One step at a time: endoplas-mic reticulum-associated degradation. Nat Rev Mol Cell Biol 9: 944-957, 2008.
153. Wearsch PA and Cresswell P. Selective loading of high-affinity peptides onto major histocompatibility complex class I molecules by the tapasin-ERp57 heterodimer. Nat Immunol 8: 873-881, 2007. (Pubitemid 47099039)
154. Whelan MA and Archer JR. Chemical reactivity of an HLA-B27 thiol group. Eur J Immunol 23: 3278-3285, 1993. (Pubitemid 23353779)
155. Williams AP, Peh CA, Purcell AW, McCluskey J, and Elliott T. Optimization of the MHC class I peptide cargo is de-pendent on tapasin. Immunity 16: 509-520, 2002. (Pubitemid 34442576)
156. Williams DB. Beyond lectins: the calnexin/calreticulin chaperone system of the endoplasmic reticulum. J Cell Sci 119: 615-623, 2006.
157. Zhang K, Shen X, Wu J, Sakaki K, Saunders T, Rutkowski DT, Back SH, and Kaufman RJ. Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell 124: 587-599, 2006. (Pubitemid 43199443)
158. Zhang Y, Baig E, and Williams DB. Functions of ERp57 in the folding and assembly of major histocompatibility complex class I molecules. J Biol Chem 281: 14622-14631, 2006. (Pubitemid 43855166)
159. Zhang Y, Kozlov G, Pocanschi CL, Brockmeier U, Ireland BS, Maattanen P, Howe C, Elliott T, Gehring K, and Wil-liams DB. ERp57 does not require interactions with cal-nexin and calreticulin to promote assembly of class I histocompatibility molecules, and it enhances peptide loading independently of its redox activity. J Biol Chem 284: 10160-10173, 2009.