MHC class II polymorphisms, autoreactive T-cells, and autoimmunity

Frontiers in Immunology

Volumn 4, Issue OCT, 2013, Pages

  Tsai, Sue ^a,c   Santamaria, Pere ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^c UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Autoimmune diseases; Autoreactive T cells; MHC class II; Resistance genes; Susceptibility genes; T regulatory cells; Type 1 diabetes

Indexed keywords

HLA DRB1 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; T LYMPHOCYTE RECEPTOR;

ALLELE; AUTOIMMUNITY; AUTOREACTIVE T LYMPHOCYTE; CELL SELECTION; DISEASE PREDISPOSITION; DNA POLYMORPHISM; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; MULTIPLE SCLEROSIS; NONHUMAN; REGULATORY T LYMPHOCYTE; RHEUMATOID ARTHRITIS; SHORT SURVEY; T LYMPHOCYTE; THYMOCYTE;

EID: 84885415450     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00321     Document Type: Short Survey

References (67)

1. Todd JA, Wicker LS. Genetic protection from the inflammatory disease type 1 diabetes in humans and animal models. Immunity (2001) 15:387-95. doi: 10.1016/S1074-7613(01)00202-3.
2. MacKay K, Eyre S, Myerscough A, Milicic A, Barton A, Laval S, et al. Whole-genome linkage analysis of rheumatoid arthritis susceptibility loci in 252 affected sibling pairs in the United Kingdom. Arthritis Rheum (2002) 46:632-9. doi:10.1002/art.10147.
3. Hafler DA, Compston A, Sawcer S, Lander ES, Daly MJ, De Jager PL, et al. Risk alleles for multiple sclerosis identified by a genome wide study. N Engl J Med (2007) 357:851-62. doi:10.1056/NEJMoa073493.
4. Palmer E. Negative selection-clearing out the bad apples from the T-cell repertoire. Nat Rev Immunol (2003) 3:383-91. doi:10.1038/nri1085.
5. Bouneaud C, Kourilsky P, Bousso P. Impact of negative selection on the T cell repertoire reactive to a self-peptide: a large fraction of T cell clones escapes clonal deletion. Immunity (2000) 13:829-40. doi:10.1016/S1074-7613(00)00080-7.
6. Zehn D, Bevan MJ. T cells with low avidity for a tissue-restricted antigen routinely evade central and peripheral tolerance and cause autoimmunity. Immunity (2006) 25:261-70. doi:10.1016/j.immuni.2006.06.009.
7. Walker LS, Abbas AK. The enemy within: keeping self-reactive T cells at bay in the periphery. Nat Rev Immunol (2002) 2:11-9. doi:10.1038/nri701.
8. Steinman RM, Hawiger D, Nussenzweig MC. Tolerogenic dendritic cells. Annu Rev Immunol (2003) 21:685-711. doi:10.1146/annurev.immunol.21.120601.141040.
9. Bettini M, Vignali DA. Regulatory T cells and inhibitory cytokines in autoimmunity. Curr Opin Immunol (2009) 21:612-8. doi:10.1016/j.coi.2009.09.011.
10. Fallarino F, Grohmann U, Hwang KW, Orabona C, Vacca C, Bianchi R, et al. Modulation of tryptophan catabolism by regulatory T cells. Nat Immunol (2003) 4:1206-12. doi:10.1038/ni1003.
11. Serra P, Amrani A, Yamanouchi J, Han B, Thiessen S, Utsugi T, et al. CD40 ligation releases immature dendritic cells from the control of regulatory CD4+CD25+ T cells. Immunity (2003) 19:877-89. doi:10.1016/S1074-7613(03)00327-3.
12. Tang Q, Adams JY, Tooley AJ, Bi M, Fife BT, Serra P, et al. Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat Immunol (2006) 7:83-92. doi:10.1038/ni1289.
13. Borsellino G, Kleinewietfeld M, Di Mitri D, Sternjak A, Diamantini A, Giometto R, et al. Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: hydrolysis of extracellular ATP and immune suppression. Blood (2007) 110:1225-32. doi:10.1182/blood-2006-12-064527.
14. Deaglio S, Dwyer KM, Gao W, Friedman D, Usheva A, Erat A, et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med (2007) 204:1257-65. doi:10.1084/jem.20062512.
15. Latek RR, Suri A, Petzold SJ, Nelson CA, Kanagawa O, Unanue ER, et al. Structural basis of peptide binding and presentation by the type I diabetes-associated MHC class II molecule of NOD mice. Immunity (2000) 12:699-710. doi:10.1016/S1074-7613(00)80220-4.
16. Jones EY, Fugger L, Strominger JL, Siebold C. MHC class II proteins and disease: a structural perspective. Nat Rev Immunol (2006) 6:271-82. doi:10.1038/nri1805.
17. Gregersen PK, Silver J, Winchester RJ. The shared epitope hypothesis. An approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum (1987) 30:1205-13. doi:10.1002/art.1780301102.
18. Raychaudhuri S, Sandor C, Stahl EA, Freudenberg J, Lee HS, Jia X, et al. Five amino acids in three HLA proteins explain most of the association between MHC and seropositive rheumatoid arthritis. Nat Genet (2012) 44:291-6. doi:10.1038/ng.1076.
19. Hammer J, Gallazzi F, Bono E, Karr RW, Guenot J, Valsasnini P, et al. Peptide binding specificity of HLA-DR4 molecules: correlation with rheumatoid arthritis association. J Exp Med (1995) 181:1847-55. doi:10.1084/jem.181.5.1847.
20. Menconi F, Monti MC, Greenberg DA, Oashi T, Osman R, Davies TF, et al. Molecular amino acid signatures in the MHC class II peptide-binding pocket predispose to autoimmune thyroiditis in humans and in mice. Proc Natl Acad Sci U S A (2008) 105:14034-9. doi:10.1073/pnas.0806584105.
21. Smith KJ, Pyrdol J, Gauthier L, Wiley DC, Wucherpfennig KW. Crystal structure of HLA-DR2 (DRA*0101, DRB1*1501) complexed with a peptide from human myelin basic protein. J Exp Med (1998) 188:1511-20. doi:10.1084/jem.188.8.1511.
22. Acha-Orbea H, McDevitt HO. The first external domain of the nonobese diabetic mouse class II I-A beta chain is unique. Proc Natl Acad Sci U S A (1987) 84:2435-9.
23. Todd JA, Bell JI, Mcdevitt HO. HLA-DQ beta gene contributes to susceptibility and resistance to insulin-dependent diabetes mellitus. Nature (1987) 329:599-604. doi:10.1038/329599a0.
24. Suri A, Vidavsky I, Van Der Drift K, Kanagawa O, Gross ML, Unanue ER. In APCs, the autologous peptides selected by the diabetogenic I-Ag7 molecule are unique and determined by the amino acid changes in the P9 pocket. J Immunol (2002) 168:1235-43.
25. Suri A, Walters JJ, Rohrs HW, Gross ML, Unanue ER. First signature of islet beta-cell-derived naturally processed peptides selected by diabetogenic class II MHC molecules. J Immunol (2008) 180:3849-56.
26. Carrasco-Marin E, Shimizu J, Kanagawa O, Unanue ER. The class II MHC I-Ag7 molecules from non-obese diabetic mice are poor peptide binders. J Immunol (1996) 156:450-8.
27. Corper AL, Stratmann T, Apostolopoulos V, Scott CA, Garcia KC, Kang AS, et al. A structural framework for deciphering the link between I-Ag7 and autoimmune diabetes. Science (2000) 288:505-11. doi:10.1126/science.288.5465.505.
28. Stratmann T, Apostolopoulos V, Mallet-Designe V, Corper AL, Scott CA, Wilson IA, et al. The I-Ag7 MHC class II molecule linked to murine diabetes is a promiscuous peptide binder. J Immunol (2000) 165:3214-25.
29. Stadinski BD, Zhang L, Crawford F, Marrack P, Eisenbarth GS, Kappler JW. Diabetogenic T cells recognize insulin bound to IAg7 in an unexpected, weakly binding register. Proc Natl Acad Sci U S A (2010) 107:10978-83. doi:10.1073/pnas.1006545107.
30. Mohan JF, Unanue ER. Unconventional recognition of peptides by T cells and the implications for autoimmunity. Nat Rev Immunol (2012) 12:721-8. doi:10.1038/nri3294.
31. Godkin A, Friede T, Davenport M, Stevanovic S, Willis A, Jewell D, et al. Use of eluted peptide sequence data to identify the binding characteristics of peptides to the insulin-dependent diabetes susceptibility allele HLA-DQ8 (DQ 3.2). Int Immunol (1997) 9:905-11. doi:10.1093/intimm/9.6.905.
32. van Lummel M, Van Veelen PA, Zaldumbide A, De Ru A, Janssen GM, Moustakas AK, et al. Type 1 diabetes-associated HLA-DQ8 transdimer accommodates a unique peptide repertoire. J Biol Chem (2012) 287:9514-24. doi:10.1074/jbc.M111.313940.
33. Luhder F, Katz J, Benoist C, Mathis D. Major histocompatibility complex class II molecules can protect from diabetes by positively selecting T cells with additional specificities. J Exp Med (1998) 187:379-87. doi:10.1084/jem.187.3.379.
34. Schmidt D, Verdaguer J, Averill N, Santamaria P. A mechanism for the major histocompatibility complex-linked resistance to autoimmunity. J Exp Med (1997) 186:1059-75. doi:10.1084/jem.186.7.1059.
35. Schmidt D, Amrani A, Verdaguer J, Bou S, Santamaria P. Autoantigen-independent deletion of diabetogenic CD4+ thymocytes by protective MHC class II molecules. J Immunol (1999) 162:4627-36.
36. Thiessen S, Serra P, Amrani A, Verdaguer J, Santamaria P. T-cell tolerance by dendritic cells and macrophages as a mechanism for the major histocompatibility complex-linked resistance to autoimmune diabetes. Diabetes (2002) 51:325-38. doi:10.2337/diabetes.51.2.325.
37. Taneja V, Behrens M, Basal E, Sparks J, Griffiths MM, Luthra H, et al. Delineating the role of the HLA-DR4 "shared epitope" in susceptibility versus resistance to develop arthritis. J Immunol (2008) 181:2869-77.
38. Tsai S, Serra P, Clemente-Casares X, Yamanouchi J, Thiessen S, Slattery RM, et al. Antidiabetogenic MHC class II promotes the differentiation of MHC-promiscuous autoreactive T cells into FOXP3+ regulatory T cells. Proc Natl Acad Sci U S A (2013) 110:3471-6. doi:10.1073/pnas.1211391110.
39. Tsai S, Serra P, Clemente-Casares X, Slattery RM, Santamaria P. Dendritic cell-dependent in vivo generation of autoregulatory T cells by antidiabetogenic MHC class II. J Immunol (2013) 191:70-82. doi:10.4049/jimmunol.1300168.
40. Gascoigne NR, Palmer E. Signaling in thymic selection. Curr Opin Immunol (2011) 23:207-12. doi:10.1016/j.coi.2010.12.017.
41. Mohan JF, Levisetti MG, Calderon B, Herzog JW, Petzold SJ, Unanue ER. Unique autoreactive T cells recognize insulin peptides generated within the islets of Langerhans in autoimmune diabetes. Nat Immunol (2010) 11:350-4. doi:10.1038/ni.1850.
42. Bohme J, Schuhbaur B, Kanagawa O, Benoist C, Mathis D. MHC-linked protection from diabetes dissociated from clonal deletion of T cells. Science (1990) 249:293-5. doi:10.1126/science.2115690.
43. Han B, Serra P, Amrani A, Yamanouchi J, Maree AF, Edelstein-Keshet L, et al. Prevention of diabetes by manipulation of anti-IGRP autoimmunity: high efficiency of a low-affinity peptide. Nat Med (2005) 11:645-52. doi:10.1038/nm1250.
44. Jordan MS, Boesteanu A, Reed AJ, Petrone AL, Holenbeck AE, Lerman MA, et al. Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat Immunol (2001) 2:301-6. doi:10.1038/86302.
45. Hsieh CS, Lee HM, Lio CW. Selection of regulatory T cells in the thymus. Nat Rev Immunol (2012) 12:157-67.
46. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol (1995) 155:1151-64.
47. Singer SM, Tisch R, Yang XD, Mcdevitt HO. An Abd transgene prevents diabetes in nonobese diabetic mice by inducing regulatory T cells. Proc Natl Acad Sci U S A (1993) 90:9566-70. doi:10.1073/pnas.90.20.9566.
48. Singer SM, Tisch R, Yang XD, Sytwu HK, Liblau R, Mcdevitt HO. Prevention of diabetes in NOD mice by a mutated I-Ab transgene. Diabetes (1998) 47:1570-7. doi:10.2337/diabetes.47.10.1570.
49. Moran AE, Holzapfel KL, Xing Y, Cunningham NR, Maltzman JS, Punt J, et al. T cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J Exp Med (2011) 208:1279-89. doi:10.1084/jem.20110308.
50. Mangalam AK, Taneja V, David CS. HLA class II molecules influence susceptibility versus protection in inflammatory diseases by determining the cytokine profile. J Immunol (2013) 190:513-8. doi:10.4049/jimmunol.1201891.
51. Deng H, Apple R, Clare-Salzler M, Trembleau S, Mathis D, Adorini L, et al. Determinant capture as a possible mechanism of protection afforded by major histocompatibility complex class II molecules in autoimmune disease. J Exp Med (1993) 178:1675-80. doi:10.1084/jem.178.5.1675.
52. Trembleau S, Gregori S, Penna G, Gorny I, Adorini L. IL-12 administration reveals diabetogenic T cells in genetically resistant I-Ealpha-transgenic nonobese diabetic mice: resistance to autoimmune diabetes is associated with binding of Ealpha-derived peptides to the I-A(g7) molecule. J Immunol (2001) 167:4104-14.
53. Ge X, James EA, Reijonen H, Kwok WW. Differences in self-peptide binding between T1D-related susceptible and protective DR4 subtypes. J Autoimmun (2011) 36:155-60. doi:10.1016/j.jaut.2010.12.004.
54. Katz JD, Wang B, Haskins K, Benoist C, Mathis D. Following a diabetogenic T cell from genesis through pathogenesis. Cell (1993) 74:1089-100. doi:10.1016/0092-8674(93)90730-E.
55. Hanson MS, Cetkovic-Cvrlje M, Ramiya VK, Atkinson MA, Maclaren NK, Singh B, et al. Quantitative thresholds of MHC class II I-E expressed on hematopoietically derived antigen-presenting cells in transgenic NOD/Lt mice determine level of diabetes resistance and indicate mechanism of protection. J Immunol (1996) 157:1279-87.
56. Mellanby RJ, Phillips JM, Parish NM, Cooke A. Both central and peripheral tolerance mechanisms play roles in diabetes prevention in NOD-E transgenic mice. Autoimmunity (2008) 41:383-94. doi:10.1080/08916930801991021.
57. Hsieh CS, Liang Y, Tyznik AJ, Self SG, Liggitt D, Rudensky AY. Recognition of the peripheral self by naturally arising CD25+ CD4+ T cell receptors. Immunity (2004) 21:267-77. doi:10.1016/j.immuni.2004.07.009.
58. Andersson J, Stefanova I, Stephens GL, Shevach EM. CD4+CD25+ regulatory T cells are activated in vivo by recognition of self. Int Immunol (2007) 19:557-66. doi:10.1093/intimm/dxm021.
59. Wooldridge L, Ekeruche-Makinde J, Van Den Berg HA, Skowera A, Miles JJ, Tan MP, et al. A single autoimmune T cell receptor recognizes more than a million different peptides. J Biol Chem (2011) 287:1168-77. doi:10.1074/jbc.M111.289488.
60. Brock R, Wiesmuller KH, Jung G, Walden P. Molecular basis for the recognition of two structurally different major histocompatibility complex/peptide complexes by a single T-cell receptor. Proc Natl Acad Sci U S A (1996) 93:13108-13. doi:10.1073/pnas.93.23.13108.
61. Doherty DG, Penzotti JE, Koelle DM, Kwok WW, Lybrand TP, Masewicz S, et al. Structural basis of specificity and degeneracy of T cell recognition: pluriallelic restriction of T cell responses to a peptide antigen involves both specific and promiscuous interactions between the T cell receptor, peptide, and HLA-DR. J Immunol (1998) 161:3527-35.
62. Ranheim EA, Tarbell KV, Krogsgaard M, Mallet-Designe V, Teyton L, Mcdevitt HO, et al. Selection of aberrant class II restricted CD8+ T cells in NOD mice expressing a glutamic acid decarboxylase (GAD)65-specific T cell receptor transgene. Autoimmunity (2004) 37:555-67. doi:10.1080/08916930400020545.
63. Serreze DV, Holl TM, Marron MP, Graser RT, Johnson EA, Choisy-Rossi C, et al. MHC class II molecules play a role in the selection of autoreactive class I-restricted CD8 T cells that are essential contributors to type 1 diabetes development in nonobese diabetic mice. J Immunol (2004) 172:871-9.
64. Logunova NN, Viret C, Pobezinsky LA, Miller SA, Kazansky DB, Sundberg JP, et al. Restricted MHC-peptide repertoire predisposes to autoimmunity. J Exp Med (2005) 202:73-84. doi:10.1084/jem.20050198.
65. Wucherpfennig KW, Call MJ, Deng L, Mariuzza R. Structural alterations in peptide-MHC recognition by self-reactive T cell receptors. Curr Opin Immunol (2009) 21:590-5. doi:10.1016/j.coi.2009.07.008.
66. Wucherpfennig KW, Sethi D. T cell receptor recognition of self and foreign antigens in the induction of autoimmunity. Semin Immunol (2011) 23:84-91. doi:10.1016/j.smim.2011.01.007.
67. Yin Y, Li Y, Mariuzza RA. Structural basis for self-recognition by autoimmune T-cell receptors. Immunol Rev (2012) 250:32-48. doi:10.1111/imr.12002.