An insertion mutant in DQA1*0501 restores susceptibility to HLA-DM: Implications for disease associations

Journal of Immunology

Volumn 187, Issue 5, 2011, Pages 2442-2452

  Hou, Tieying ^a   Macmillan, Henriette ^a   Chen, Zhenjun ^b   Keech, Catherine L ^b   Jin, Xi ^a   Sidney, John ^c   Strohman, Michael ^a   Yoon, Taejin ^a   Mellins, Elizabeth D ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HLA DM ANTIGEN; HLA DQA1 ANTIGEN;

ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CELL SURFACE; CONTROLLED STUDY; DISEASE ASSOCIATION; IN VITRO STUDY; MOUSE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SENSITIVITY ANALYSIS; T LYMPHOCYTE;

AMINO ACID SEQUENCE; ANIMALS; ANTIGEN PRESENTATION; CELIAC DISEASE; CELL SEPARATION; FLOW CYTOMETRY; GLIADIN; HLA-D ANTIGENS; HLA-DQ ANTIGENS; HYBRIDOMAS; LYMPHOCYTE ACTIVATION; MICE; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN STRUCTURE, SECONDARY; TRANSFECTION;

EID: 80052679493     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100255     Document Type: Article

References (62)

1. Lundin, K. E., H. A. Gjertsen, H. Scott, L. M. Sollid, and E. Thorsby. 1994. Function of DQ2 and DQ8 as HLA susceptibility molecules in celiac disease. Hum. Immunol. 41: 24-27. (Pubitemid 24319045)
2. Pociot, F., and M. F. McDermott. 2002. Genetics of type 1 diabetes mellitus. Genes Immun. 3: 235-249. (Pubitemid 38967549)
3. Green, P. H., and C. Cellier. 2007. Celiac disease. N. Engl. J. Med. 357: 1731-1743.
4. Johnson, T. C., B. Diamond, L. Memeo, H. Negulescu, Z. Hovhanissyan, V. Verkarre, H. Rotterdam, A. Fasano, S. Caillat-Zucman, E. Grosdidier, et al. 2004. Relationship of HLA-DQ8 and severity of celiac disease: comparison of New York and Parisian cohorts. Clin. Gastroenterol. Hepatol. 2: 888-894. (Pubitemid 39335795)
5. Busch, R., R. C. Doebele, N. S. Patil, A. Pashine, and E. D. Mellins. 2000. Accessory molecules for MHC class II peptide loading. Curr. Opin. Immunol. 12: 99-106. (Pubitemid 30093457)
6. Busch, R., C. H. Rinderknecht, S. Roh, A. W. Lee, J. J. Harding, T. Burster, T. M. Hornell, and E. D. Mellins. 2005. Achieving stability through editing and chaperoning: regulation of MHC class II peptide binding and expression. Immunol. Rev. 207: 242-260. (Pubitemid 41415022)
7. Jones, P. P., D. B. Murphy, D. Hewgill, and H. O. McDevitt. 1979. Detection of a common polypeptide chain in I - A and I - E sub-region immunoprecipitates. Mol. Immunol. 16: 51-60. (Pubitemid 9169395)
8. Machamer, C. E., and P. Cresswell. 1982. Biosynthesis and glycosylation of the invariant chain associated with HLA-DR antigens. J. Immunol. 129: 2564-2569. (Pubitemid 13245523)
9. Bakke, O., and B. Dobberstein. 1990. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 63: 707-716. (Pubitemid 120035044)
10. West, M. A., J. M. Lucocq, and C. Watts. 1994. Antigen processing and class II MHC peptide-loading compartments in human B-lymphoblastoid cells. Nature 369: 147-151. (Pubitemid 24153437)
11. Tulp, A., D. Verwoerd, B. Dobberstein, H. L. Ploegh, and J. Pieters. 1994. Isolation and characterization of the intracellular MHC class II compartment. Nature 369: 120-126. (Pubitemid 24153434)
12. Qiu, Y., X. Xu, A. Wandinger-Ness, D. P. Dalke, and S. K. Pierce. 1994. Separation of subcellular compartments containing distinct functional forms of MHC class II. J. Cell Biol. 125: 595-605. (Pubitemid 24149841)
13. Peters, P. J., J. J. Neefjes, V. Oorschot, H. L. Ploegh, and H. J. Geuze. 1991. Segregation of MHC class II molecules from MHC class I molecules in the Golgi complex for transport to lysosomal compartments. Nature 349: 669-676. (Pubitemid 21912130)
14. Riberdy, J. M., J. R. Newcomb, M. J. Surman, J. A. Barbosa, and P. Cresswell. 1992. HLA-DR molecules from an antigen-processing mutant cell line are associated with invariant chain peptides. Nature 360: 474-477.
15. Sette, A., S. Ceman, R. T. Kubo, K. Sakaguchi, E. Appella, D. F. Hunt, T. A. Davis, H. Michel, J. Shabanowitz, R. Rudersdorf, et al. 1992. Invariant chain peptides in most HLA-DR molecules of an antigen-processing mutant. Science 258: 1801-1804. (Pubitemid 23087349)
16. Denzin, L. K., and P. Cresswell. 1995. HLA-DM induces CLIP dissociation from MHC class II alpha beta dimers and facilitates peptide loading. Cell 82: 155-165.
17. Sherman, M. A., D. A. Weber, and P. E. Jensen. 1995. DM enhances peptide binding to class II MHC by release of invariant chain-derived peptide. Immunity 3: 197-205.
18. Sloan, V. S., P. Cameron, G. Porter, M. Gammon, M. Amaya, E. Mellins, and D. M. Zaller. 1995. Mediation by HLA-DM of dissociation of peptides from HLA-DR. Nature 375: 802-806.
19. Fallang, L. E., S. Roh, A. Holm, E. Bergseng, T. Yoon, B. Fleckenstein, A. Bandyopadhyay, E. D. Mellins, and L. M. Sollid. 2008. Complexes of two cohorts of CLIP peptides and HLA-DQ2 of the autoimmune DR3-DQ2 haplotype are poor substrates for HLA-DM. J. Immunol. 181: 5451-5461.
20. Denzin, L. K., N. F. Robbins, C. Carboy-Newcomb, and P. Cresswell. 1994. Assembly and intracellular transport of HLA-DM and correction of the class II antigen-processing defect in T2 cells. Immunity 1: 595-606.
21. Salter, R. D., D. N. Howell, and P. Cresswell. 1985. Genes regulating HLA class I antigen expression in T-B lymphoblast hybrids. Immunogenetics 21: 235-246. (Pubitemid 15117182)
22. De Kauwe, A. L., Z. Chen, R. P. Anderson, C. L. Keech, J. D. Price, O. Wijburg, D. C. Jackson, J. Ladhams, J. Allison, and J. McCluskey. 2009. Resistance to celiac disease in humanized HLA-DR3-DQ2-transgenic mice expressing specific anti-gliadin CD4+ T cells. J. Immunol. 182: 7440-7450.
23. Kim, C. Y., H. Quarsten, E. Bergseng, C. Khosla, and L. M. Sollid. 2004. Structural basis for HLA-DQ2-mediated presentation of gluten epitopes in celiac disease. Proc. Natl. Acad. Sci. USA 101: 4175-4179. (Pubitemid 38405902)
24. Doebele, R. C., R. Busch, H. M. Scott, A. Pashine, and E. D. Mellins. 2000. Determination of the HLA-DM interaction site on HLA-DR molecules. Immunity 13: 517-527.
25. Pashine, A., R. Busch, M. P. Belmares, J. N. Munning, R. C. Doebele, M. Buckingham, G. P. Nolan, and E. D. Mellins. 2003. Interaction of HLA-DR with an acidic face of HLA-DM disrupts sequence-dependent interactions with peptides. Immunity 19: 183-192. (Pubitemid 37011333)
26. Fallang, L. E., E. Bergseng, K. Hotta, A. Berg-Larsen, C. Y. Kim, and L. M. Sollid. 2009. Differences in the risk of celiac disease associated with HLA-DQ2.5 or HLA-DQ2.2 are related to sustained gluten antigen presentation. Nat. Immunol. 10: 1096-1101.
27. Belmares, M. P., R. Busch, K. W. Wucherpfennig, H. M. McConnell, and E. D. Mellins. 2002. Structural factors contributing to DM susceptibility of MHC class II/peptide complexes. J. Immunol. 169: 5109-5117. (Pubitemid 35217180)
28. Koonce, C. H., G. Wutz, E. J. Robertson, A. B. Vogt, H. Kropshofer, and E. K. Bikoff. 2003. DM loss in k haplotype mice reveals isotype-specific chaperone requirements. J. Immunol. 170: 3751-3761. (Pubitemid 36359245)
29. Kropshofer, H., S. O. Arndt, G. Moldenhauer, G. J. Hämmerling, and A. B. Vogt. 1997. HLA-DM acts as a molecular chaperone and rescues empty HLA-DR molecules at lysosomal pH. Immunity 6: 293-302. (Pubitemid 27148596)
30. Lovitch, S. B., Z. Pu, and E. R. Unanue. 2006. Amino-terminal flanking residues determine the conformation of a peptide-class II MHC complex. J. Immunol. 176: 2958-2968.
31. Albert, L. J., B. Ghumman, and T. H. Watts. 1996. Effect of HLA-DM transfection on hen egg lysozyme presentation by T2.Ak cells. J. Immunol. 157: 2247-2255. (Pubitemid 126450433)
32. Fallas, J. L., H. M. Tobin, O. Lou, D. Guo, D. B. Sant'Angelo, and L. K. Denzin. 2004. Ectopic expression of HLA-DO in mouse dendritic cells diminishes MHC class II antigen presentation. J. Immunol. 173: 1549-1560. (Pubitemid 38971584)
33. Honey, K., K. Forbush, P. E. Jensen, and A. Y. Rudensky. 2004. Effect of decreasing the affinity of the class II-associated invariant chain peptide on the MHC class II peptide repertoire in the presence or absence of H-2M. J. Immunol. 172: 4142-4150. (Pubitemid 38375226)
34. Lich, J. D., J. A. Jayne, D. Zhou, J. F. Elliott, and J. S. Blum. 2003. Editing of an immunodominant epitope of glutamate decarboxylase by HLA-DM. J. Immunol. 171: 853-859. (Pubitemid 36871397)
35. Price, P., C. Witt, R. Allcock, D. Sayer, M. Garlepp, C. C. Kok, M. French, S. Mallal, and F. Christiansen. 1999. The genetic basis for the association of the 8.1 ancestral haplotype (A1, B8, DR3) with multiple immunopathological diseases. Immunol. Rev. 167: 257-274. (Pubitemid 29178987)
36. Anderson, R. P., P. Degano, A. J. Godkin, D. P. Jewell, and A. V. Hill. 2000. In vivo antigen challenge in celiac disease identifies a single transglutaminase-modified peptide as the dominant A-gliadin T-cell epitope. Nat. Med. 6: 337-342. (Pubitemid 30148628)
37. Qiao, S. W., E. Bergseng, O. Molberg, J. Xia, B. Fleckenstein, C. Khosla, and L. M. Sollid. 2004. Antigen presentation to celiac lesion-derived T cells of a 33-mer gliadin peptide naturally formed by gastrointestinal digestion. J. Immunol. 173: 1757-1762. (Pubitemid 38971607)
38. Sollid, L. M., and E. Thorsby. 1993. HLA susceptibility genes in celiac disease: genetic mapping and role in pathogenesis. Gastroenterology 105: 910-922. (Pubitemid 23249504)
39. Sollid, L. M., G. Markussen, J. Ek, H. Gjerde, F. Vartdal, and E. Thorsby. 1989. Evidence for a primary association of celiac disease to a particular HLA-DQ alpha/beta heterodimer. J. Exp. Med. 169: 345-350. (Pubitemid 19035567)
40. Bergseng, E., J. Xia, C. Y. Kim, C. Khosla, and L. M. Sollid. 2005. Main chain hydrogen bond interactions in the binding of proline-rich gluten peptides to the celiac disease-associated HLA-DQ2 molecule. J. Biol. Chem. 280: 21791-21796. (Pubitemid 40827828)
41. Sant, A. J., C. Beeson, B. McFarland, J. Cao, S. Ceman, P. W. Bryant, and S. Wu. 1999. Individual hydrogen bonds play a critical role in MHC class II: peptide interactions: implications for the dynamic aspects of class II trafficking and DM-mediated peptide exchange. Immunol. Rev. 172: 239-253. (Pubitemid 30000482)
42. Stratikos, E., D. C. Wiley, and L. J. Stern. 2004. Enhanced catalytic action of HLA-DM on the exchange of peptides lacking backbone hydrogen bonds between their N-terminal region and the MHC class II alpha-chain. J. Immunol. 172: 1109-1117. (Pubitemid 38113771)
43. Guo, X., P. Ni, and L. Li. 2001. [Association between asthma and the polymorphism of HLA-DQ genes]. Zhonghua Jie He He Hu Xi Za Zhi 24: 139-141.
44. Donn, R. P., W. Thomson, L. Pepper, D. Carthy, A. Farhan, C. Ryder, T. Southwood, L. Holt, and W. Ollier. 1995. Antinuclear antibodies in early onset pauciarticular juvenile chronic arthritis (JCA) are associated with HLADQB1*0603: a possible JCA-associated human leucocyte antigen haplotype. Br. J. Rheumatol. 34: 461-465.
45. Kwon, O. J., A. Karni, S. Israel, C. Brautbar, A. Amar, Z. Meiner, O. Abramsky, and D. Karussis. 1999. HLA class II susceptibility to multiple sclerosis among Ashkenazi and non-Ashkenazi Jews. Arch. Neurol. 56: 555-560. (Pubitemid 29218150)
46. Lazarski, C. A., F. A. Chaves, and A. J. Sant. 2006. The impact of DM on MHC class II-restricted antigen presentation can be altered by manipulation of MHC-peptide kinetic stability. J. Exp. Med. 203: 1319-1328. (Pubitemid 43736600)
47. Rinderknecht, C. H., M. P. Belmares, T. L. Catanzarite, A. J. Bankovich, T. H. Holmes, K. C. Garcia, N. K. Nanda, R. Busch, S. Kovats, and E. D. Mellins. 2007. Posttranslational regulation of I-Ed by affinity for CLIP. J. Immunol. 179: 5907-5915.
48. Sant, A. J., F. A. Chaves, S. A. Jenks, K. A. Richards, P. Menges, J. M. Weaver, and C. A. Lazarski. 2005. The relationship between immunodominance, DM editing, and the kinetic stability of MHC class II:peptide complexes. Immunol. Rev. 207: 261-278. (Pubitemid 41415023)
49. Kagnoff, M. F., R. K. Austin, H. C. Johnson, J. E. Bernardin, M. D. Dietler, and D. D. Kasarda. 1982. Celiac sprue: correlation with murine T cell responses to wheat gliadin components. J. Immunol. 129: 2693-2697. (Pubitemid 13245546)
50. Franco, A., E. Appella, M. F. Kagnoff, Y. Chowers, K. Sakaguchi, H. M. Grey, and A. Sette. 1994. Peripheral T cell response to A-gliadin in celiac disease: differential processing and presentation capacities of Epstein-Barr-transformed B cells and fibroblasts. Clin. Immunol. Immunopathol. 71: 75-81.
51. Marti, T., O. Molberg, Q. Li, G. M. Gray, C. Khosla, and L. M. Sollid. 2005. Prolyl endopeptidase-mediated destruction of T cell epitopes in whole gluten: chemical and immunological characterization. J. Pharmacol. Exp. Ther. 312: 19-26. (Pubitemid 40096448)
52. Thomson, G., W. P. Robinson, M. K. Kuhner, S. Joe, M. J. MacDonald, J. L. Gottschall, J. Barbosa, S. S. Rich, J. Bertrams, M. P. Baur, et al. 1988. Genetic heterogeneity, modes of inheritance, and risk estimates for a joint study of Caucasians with insulin-dependent diabetes mellitus. Am. J. Hum. Genet. 43: 799-816. (Pubitemid 19018982)
53. Mellins, E. D. 1992. The role of the MHC in autoimmunity: an overview. J. Rheumatol. Suppl. 33: 63-69.
54. Rinderknecht, C. H., N. Lu, O. Crespo, P. Truong, T. Hou, N. Wang, N. Rajasekaran, and E. D. Mellins. 2010. I-Ag7 is subject to post-translational chaperoning by CLIP. Int. Immunol. 22: 705-716.
55. Rinderknecht, C. H., S. Roh, A. Pashine, M. P. Belmares, N. S. Patil, N. Lu, P. Truong, T. Hou, C. Macaubas, T. Yoon, et al. 2010. DM influences the abundance of major histocompatibility complex class II alleles with low affinity for class II-associated invariant chain peptides via multiple mechanisms. Immunology 131: 18-32.
56. Fung-Leung, W. P., C. D. Surh, M. Liljedahl, J. Pang, D. Leturcq, P. A. Peterson, S. R. Webb, and L. Karlsson. 1996. Antigen presentation and T cell development in H2-M-deficient mice. Science 271: 1278-1281. (Pubitemid 26082648)
57. Martin, W. D., G. G. Hicks, S. K. Mendiratta, H. I. Leva, H. E. Ruley, and L. Van Kaer. 1996. H2-M mutant mice are defective in the peptide loading of class II molecules, antigen presentation, and T cell repertoire selection. Cell 84: 543-550. (Pubitemid 26071735)
58. Miyazaki, T., P. Wolf, S. Tourne, C. Waltzinger, A. Dierich, N. Barois, H. Ploegh, C. Benoist, and D. Mathis. 1996. Mice lacking H2-M complexes, enigmatic elements of the MHC class II peptide-loading pathway. Cell 84: 531-541. (Pubitemid 26071734)
59. Surh, C. D., D. S. Lee, W. P. Fung-Leung, L. Karlsson, and J. Sprent. 1997. Thymic selection by a single MHC/peptide ligand produces a semidiverse repertoire of CD4+ T cells. Immunity 7: 209-219. (Pubitemid 27392013)
60. Bevan, M. J. 1997. In thymic selection, peptide diversity gives and takes away. Immunity 7: 175-178. (Pubitemid 27392009)
61. Ng, A. W., A. Bidani, and T. A. Heming. 2004. Innate host defense of the lung: effects of lung-lining fluid pH. Lung 182: 297-317. (Pubitemid 40365049)
62. Radu, C. G., A. Nijagal, J. McLaughlin, L. Wang, and O. N. Witte. 2005. Differential proton sensitivity of related G protein-coupled receptors T cell death-associated gene 8 and G2A expressed in immune cells. Proc. Natl. Acad. Sci. USA 102: 1632-1637. (Pubitemid 40209219)