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Published in: Immunologic Research 1/2017

01-02-2017 | Environment and Autoimmunity

HLA-DRB1 the notorious gene in the mosaic of autoimmunity

Authors: María-Teresa Arango, Carlo Perricone, Shaye Kivity, Enrica Cipriano, Fulvia Ceccarelli, Guido Valesini, Yehuda Shoenfeld

Published in: Immunologic Research | Issue 1/2017

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Abstract

The major histocompatibility complex system is the most polymorphic gene cluster of the mammal genome. In humans, this is a genomic locus known as the human leukocyte antigen (HLA) system. The HLA encodes mostly immune-associated proteins whose main effect is the presentation of antigens to the immune cells. Thus, it is clear that it is essential for to the proper function of the immune response against pathogens and strongly implicated in the development of autoimmune diseases. Nonetheless, there are hundreds of polymorphisms of HLA-DRB1 which have been associated with different autoimmune disorders as well as with immune response to infection and vaccines. It is possible that the interaction of specific HLA with pathogenic antigens is one of the keys favoring (or protecting) toward the development of an autoimmune disease. In the era of personalized medicine, it would be of great help to build a map of the genomic risk of each individual to evaluate the risk of developing an autoimmune condition.
Literature
8.
go back to reference Shoenfeld Y, et al. The mosaic of autoimmunity: prediction, autoantibodies, and therapy in autoimmune diseases–2008. Isr Med Assoc J. 2008;10(1):13–9.PubMed Shoenfeld Y, et al. The mosaic of autoimmunity: prediction, autoantibodies, and therapy in autoimmune diseases–2008. Isr Med Assoc J. 2008;10(1):13–9.PubMed
15.
go back to reference Tomijenovic L, et al. Vaccination in autoimmune animal models. Isr Med Assoc J. 2014;16(10):657–8.PubMed Tomijenovic L, et al. Vaccination in autoimmune animal models. Isr Med Assoc J. 2014;16(10):657–8.PubMed
17.
go back to reference Kaufman JF, et al. The class II molecules of the human and murine major histocompatibility complex. Cell. 1984;36(1):1–13.PubMedCrossRef Kaufman JF, et al. The class II molecules of the human and murine major histocompatibility complex. Cell. 1984;36(1):1–13.PubMedCrossRef
19.
go back to reference Klein J, Figueroa F. Evolution of the major histocompatibility complex. Crit Rev Immunol. 1986;6(4):295–386.PubMed Klein J, Figueroa F. Evolution of the major histocompatibility complex. Crit Rev Immunol. 1986;6(4):295–386.PubMed
27.
go back to reference de Vries N, et al. HLA-DR1 and rheumatoid arthritis in Israeli Jews: sequencing reveals that DRB1*0102 is the predominant HLA-DR1 subtype. Tissue Antigens. 1993;41(1):26–30.PubMedCrossRef de Vries N, et al. HLA-DR1 and rheumatoid arthritis in Israeli Jews: sequencing reveals that DRB1*0102 is the predominant HLA-DR1 subtype. Tissue Antigens. 1993;41(1):26–30.PubMedCrossRef
28.
go back to reference Terao C, et al. Brief Report: main contribution of DRB1*04:05 among the shared epitope alleles and involvement of DRB1 amino acid position 57 in association with joint destruction in anti-citrullinated protein antibody-positive rheumatoid arthritis. Arthritis Rheumatol. 2015;67(7):1744–50. doi:10.1002/art.39105.PubMedCrossRef Terao C, et al. Brief Report: main contribution of DRB1*04:05 among the shared epitope alleles and involvement of DRB1 amino acid position 57 in association with joint destruction in anti-citrullinated protein antibody-positive rheumatoid arthritis. Arthritis Rheumatol. 2015;67(7):1744–50. doi:10.​1002/​art.​39105.PubMedCrossRef
34.
go back to reference Nakken B, et al. Associations of MHC class II alleles in Norwegian primary Sjogren’s syndrome patients: implications for development of autoantibodies to the Ro52 autoantigen. Scand J Immunol. 2001;54(4):428–33.PubMedCrossRef Nakken B, et al. Associations of MHC class II alleles in Norwegian primary Sjogren’s syndrome patients: implications for development of autoantibodies to the Ro52 autoantigen. Scand J Immunol. 2001;54(4):428–33.PubMedCrossRef
35.
go back to reference Roitberg-Tambur A, et al. Molecular analysis of HLA class II genes in primary Sjogren’s syndrome. A study of Israeli Jewish and Greek non-Jewish patients. Hum Immunol. 1993;36(4):235–42.PubMedCrossRef Roitberg-Tambur A, et al. Molecular analysis of HLA class II genes in primary Sjogren’s syndrome. A study of Israeli Jewish and Greek non-Jewish patients. Hum Immunol. 1993;36(4):235–42.PubMedCrossRef
48.
49.
go back to reference Deighton CM, et al. The contribution of HLA to rheumatoid arthritis. Clin Genet. 1989;36(3):178–82.PubMedCrossRef Deighton CM, et al. The contribution of HLA to rheumatoid arthritis. Clin Genet. 1989;36(3):178–82.PubMedCrossRef
50.
go back to reference Stastny P, Fink CW. HLA-Dw4 in adult and juvenile rheumatoid arthritis. Transplant Proc. 1977;9(4):1863–6.PubMed Stastny P, Fink CW. HLA-Dw4 in adult and juvenile rheumatoid arthritis. Transplant Proc. 1977;9(4):1863–6.PubMed
51.
52.
go back to reference Gregersen PK, et al. The shared epitope hypothesis. An approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum. 1987;30(11):1205–13.PubMedCrossRef Gregersen PK, et al. The shared epitope hypothesis. An approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum. 1987;30(11):1205–13.PubMedCrossRef
54.
go back to reference Gonzalez-Gay MA, et al. Influence of human leukocyte antigen-DRB1 on the susceptibility and severity of rheumatoid arthritis. Semin Arthritis Rheum. 2002;31(6):355–60.PubMedCrossRef Gonzalez-Gay MA, et al. Influence of human leukocyte antigen-DRB1 on the susceptibility and severity of rheumatoid arthritis. Semin Arthritis Rheum. 2002;31(6):355–60.PubMedCrossRef
56.
go back to reference Plant MJ, et al. Patterns of radiological progression in early rheumatoid arthritis: results of an 8 year prospective study. J Rheumatol. 1998;25(3):417–26.PubMed Plant MJ, et al. Patterns of radiological progression in early rheumatoid arthritis: results of an 8 year prospective study. J Rheumatol. 1998;25(3):417–26.PubMed
57.
go back to reference Weyand CM, Goronzy JJ. Disease mechanisms in rheumatoid arthritis: gene dosage effect of HLA-DR haplotypes. J Lab Clin Med. 1994;124(3):335–8.PubMed Weyand CM, Goronzy JJ. Disease mechanisms in rheumatoid arthritis: gene dosage effect of HLA-DR haplotypes. J Lab Clin Med. 1994;124(3):335–8.PubMed
60.
61.
go back to reference Ling S, et al. The rheumatoid arthritis shared epitope triggers innate immune signaling via cell surface calreticulin. J Immunol. 2007;179(9):6359–67.PubMedCrossRef Ling S, et al. The rheumatoid arthritis shared epitope triggers innate immune signaling via cell surface calreticulin. J Immunol. 2007;179(9):6359–67.PubMedCrossRef
64.
go back to reference Terao C, et al. An association between amino acid position 74 of HLA-DRB1 and anti-citrullinated protein antibody levels in Japanese patients with anti-citrullinated protein antibody-positive rheumatoid arthritis. Arthritis Rheumatol. 2015;67(8):2038–45. doi:10.1002/art.39133.PubMedCrossRef Terao C, et al. An association between amino acid position 74 of HLA-DRB1 and anti-citrullinated protein antibody levels in Japanese patients with anti-citrullinated protein antibody-positive rheumatoid arthritis. Arthritis Rheumatol. 2015;67(8):2038–45. doi:10.​1002/​art.​39133.PubMedCrossRef
66.
go back to reference Jiang X, et al. An Immunochip-based interaction study of contrasting interaction effects with smoking in ACPA-positive versus ACPA-negative rheumatoid arthritis. Rheumatology (Oxford). 2016;55(1):149–55. doi:10.1093/rheumatology/kev285.CrossRef Jiang X, et al. An Immunochip-based interaction study of contrasting interaction effects with smoking in ACPA-positive versus ACPA-negative rheumatoid arthritis. Rheumatology (Oxford). 2016;55(1):149–55. doi:10.​1093/​rheumatology/​kev285.CrossRef
67.
go back to reference Moll JM, et al. Associations between ankylosing spondylitis, psoriatic arthritis, Reiter’s disease, the intestinal arthropathies, and Behcet’s syndrome. Medicine (Baltimore). 1974;53(5):343–64.CrossRef Moll JM, et al. Associations between ankylosing spondylitis, psoriatic arthritis, Reiter’s disease, the intestinal arthropathies, and Behcet’s syndrome. Medicine (Baltimore). 1974;53(5):343–64.CrossRef
70.
go back to reference Martinez-Borra J, et al. HLA-B27 alone rather than B27-related class I haplotypes contributes to ankylosing spondylitis susceptibility. Hum Immunol. 2000;61(2):131–9.PubMedCrossRef Martinez-Borra J, et al. HLA-B27 alone rather than B27-related class I haplotypes contributes to ankylosing spondylitis susceptibility. Hum Immunol. 2000;61(2):131–9.PubMedCrossRef
71.
go back to reference Rubin LA, et al. Investigating the genetic basis for ankylosing spondylitis. Linkage studies with the major histocompatibility complex region. Arthritis Rheum. 1994;37(8):1212–20.PubMedCrossRef Rubin LA, et al. Investigating the genetic basis for ankylosing spondylitis. Linkage studies with the major histocompatibility complex region. Arthritis Rheum. 1994;37(8):1212–20.PubMedCrossRef
72.
73.
go back to reference Perez-Guijo V, et al. Distribution of HLA-DRB1 genes in patients with sporadic ankylosing spondylitis in the south of Spain. Joint Bone Spine. 2002;69(5):458–62.PubMedCrossRef Perez-Guijo V, et al. Distribution of HLA-DRB1 genes in patients with sporadic ankylosing spondylitis in the south of Spain. Joint Bone Spine. 2002;69(5):458–62.PubMedCrossRef
74.
go back to reference Said-Nahal R, et al. The role of HLA genes in familial spondyloarthropathy: a comprehensive study of 70 multiplex families. Ann Rheum Dis. 2002;61(3):201–6.PubMedPubMedCentralCrossRef Said-Nahal R, et al. The role of HLA genes in familial spondyloarthropathy: a comprehensive study of 70 multiplex families. Ann Rheum Dis. 2002;61(3):201–6.PubMedPubMedCentralCrossRef
75.
76.
go back to reference Monowarul Islam SM, et al. HLA-DR8 and acute anterior uveitis in ankylosing spondylitis. Arthritis Rheum. 1995;38(4):547–50.PubMedCrossRef Monowarul Islam SM, et al. HLA-DR8 and acute anterior uveitis in ankylosing spondylitis. Arthritis Rheum. 1995;38(4):547–50.PubMedCrossRef
77.
go back to reference Breban M, et al. Animal models of the spondyloarthropathies. Curr Rheumatol Rep. 2000;2(4):282–7.PubMedCrossRef Breban M, et al. Animal models of the spondyloarthropathies. Curr Rheumatol Rep. 2000;2(4):282–7.PubMedCrossRef
78.
go back to reference Reveille JD. The genetic contribution to the pathogenesis of rheumatoid arthritis. Curr Opin Rheumatol. 1998;10(3):187–200.PubMedCrossRef Reveille JD. The genetic contribution to the pathogenesis of rheumatoid arthritis. Curr Opin Rheumatol. 1998;10(3):187–200.PubMedCrossRef
79.
go back to reference Rantapaa Dahlqvist S, et al. HLA antigens in rheumatoid arthritis patients with and without a family history of polyarthritis. Scand J Rheumatol. 1985;14(4):375–80.PubMedCrossRef Rantapaa Dahlqvist S, et al. HLA antigens in rheumatoid arthritis patients with and without a family history of polyarthritis. Scand J Rheumatol. 1985;14(4):375–80.PubMedCrossRef
85.
go back to reference Tsao BP. Update on human systemic lupus erythematosus genetics. Curr Opin Rheumatol. 2004;16(5):513–21.PubMedCrossRef Tsao BP. Update on human systemic lupus erythematosus genetics. Curr Opin Rheumatol. 2004;16(5):513–21.PubMedCrossRef
87.
go back to reference Podrebarac TA, et al. Clinical correlates, serum autoantibodies and the role of the major histocompatibility complex in French Canadian and non-French Canadian Caucasians with SLE. Lupus. 1998;7(3):183–91.PubMedCrossRef Podrebarac TA, et al. Clinical correlates, serum autoantibodies and the role of the major histocompatibility complex in French Canadian and non-French Canadian Caucasians with SLE. Lupus. 1998;7(3):183–91.PubMedCrossRef
92.
go back to reference Reveille JD, Arnett FC. The immunogenetics of Sjogren’s syndrome. Rheum Dis Clin North Am. 1992;18(3):539–50.PubMed Reveille JD, Arnett FC. The immunogenetics of Sjogren’s syndrome. Rheum Dis Clin North Am. 1992;18(3):539–50.PubMed
95.
go back to reference Lessard CJ, et al. Variants at multiple loci implicated in both innate and adaptive immune responses are associated with Sjogren’s syndrome. Nat Genet. 2013;45(11):1284–92. doi:10.1038/ng.2792.PubMedCrossRef Lessard CJ, et al. Variants at multiple loci implicated in both innate and adaptive immune responses are associated with Sjogren’s syndrome. Nat Genet. 2013;45(11):1284–92. doi:10.​1038/​ng.​2792.PubMedCrossRef
97.
go back to reference Reveille JD, et al. Specific amino acid residues in the second hypervariable region of HLA-DQA1 and DQB1 chain genes promote the Ro (SS-A)/La (SS-B) autoantibody responses. J Immunol. 1991;146(11):3871–6.PubMed Reveille JD, et al. Specific amino acid residues in the second hypervariable region of HLA-DQA1 and DQB1 chain genes promote the Ro (SS-A)/La (SS-B) autoantibody responses. J Immunol. 1991;146(11):3871–6.PubMed
99.
go back to reference Jean S, et al. DRB1*15 and DRB1*03 extended haplotype interaction in primary Sjogren’s syndrome genetic susceptibility. Clin Exp Rheumatol. 1998;16(6):725–8.PubMed Jean S, et al. DRB1*15 and DRB1*03 extended haplotype interaction in primary Sjogren’s syndrome genetic susceptibility. Clin Exp Rheumatol. 1998;16(6):725–8.PubMed
100.
go back to reference Anaya JM, et al. TAP, HLA-DQB1, and HLA-DRB1 polymorphism in Colombian patients with primary Sjogren’s syndrome. Semin Arthritis Rheum. 2002;31(6):396–405.PubMedCrossRef Anaya JM, et al. TAP, HLA-DQB1, and HLA-DRB1 polymorphism in Colombian patients with primary Sjogren’s syndrome. Semin Arthritis Rheum. 2002;31(6):396–405.PubMedCrossRef
101.
go back to reference Morling N, et al. Immunogenetics of rheumatoid arthritis and primary Sjogren’s syndrome: DNA polymorphism of HLA class II genes. Dis Markers. 1991;9(5):289–96.PubMed Morling N, et al. Immunogenetics of rheumatoid arthritis and primary Sjogren’s syndrome: DNA polymorphism of HLA class II genes. Dis Markers. 1991;9(5):289–96.PubMed
102.
go back to reference Kang HI, et al. Comparison of HLA class II genes in Caucasoid, Chinese, and Japanese patients with primary Sjogren’s syndrome. J Immunol. 1993;150(8 Pt 1):3615–23.PubMed Kang HI, et al. Comparison of HLA class II genes in Caucasoid, Chinese, and Japanese patients with primary Sjogren’s syndrome. J Immunol. 1993;150(8 Pt 1):3615–23.PubMed
103.
go back to reference Garcia Portales R, et al. Immunogenetics of the Sjogren’s syndrome in southern Spain. Ann Med Int. 1994;11(2):56–61. Garcia Portales R, et al. Immunogenetics of the Sjogren’s syndrome in southern Spain. Ann Med Int. 1994;11(2):56–61.
104.
go back to reference Price P, et al. The genetic basis for the association of the 8.1 ancestral haplotype (A1, B8, DR3) with multiple immunopathological diseases. Immunol Rev. 1999;167:257–74.PubMedCrossRef Price P, et al. The genetic basis for the association of the 8.1 ancestral haplotype (A1, B8, DR3) with multiple immunopathological diseases. Immunol Rev. 1999;167:257–74.PubMedCrossRef
106.
go back to reference Mavragani CP, et al. Sjogren’s syndrome: autoantibodies to cellular antigens. Clinical and molecular aspects. Int Arch Allergy Immunol. 2000;123(1):46–57.PubMedCrossRef Mavragani CP, et al. Sjogren’s syndrome: autoantibodies to cellular antigens. Clinical and molecular aspects. Int Arch Allergy Immunol. 2000;123(1):46–57.PubMedCrossRef
107.
go back to reference Cooper GS, et al. The role of genetic factors in autoimmune disease: implications for environmental research. Environ Health Perspect. 1999;107(Suppl 5):693–700.PubMedPubMedCentralCrossRef Cooper GS, et al. The role of genetic factors in autoimmune disease: implications for environmental research. Environ Health Perspect. 1999;107(Suppl 5):693–700.PubMedPubMedCentralCrossRef
108.
go back to reference Chinoy H, et al. In adult onset myositis, the presence of interstitial lung disease and myositis specific/associated antibodies are governed by HLA class II haplotype, rather than by myositis subtype. Arthritis Res Ther. 2006;8(1):R13. doi:10.1186/ar1862.PubMedCrossRef Chinoy H, et al. In adult onset myositis, the presence of interstitial lung disease and myositis specific/associated antibodies are governed by HLA class II haplotype, rather than by myositis subtype. Arthritis Res Ther. 2006;8(1):R13. doi:10.​1186/​ar1862.PubMedCrossRef
109.
go back to reference Love LA, et al. A new approach to the classification of idiopathic inflammatory myopathy: myositis-specific autoantibodies define useful homogeneous patient groups. Medicine (Baltimore). 1991;70(6):360–74.CrossRef Love LA, et al. A new approach to the classification of idiopathic inflammatory myopathy: myositis-specific autoantibodies define useful homogeneous patient groups. Medicine (Baltimore). 1991;70(6):360–74.CrossRef
110.
go back to reference Reed AM, et al. Immunogenetic studies in families of children with juvenile dermatomyositis. J Rheumatol. 1998;25(5):1000–2.PubMed Reed AM, et al. Immunogenetic studies in families of children with juvenile dermatomyositis. J Rheumatol. 1998;25(5):1000–2.PubMed
111.
go back to reference Wedderburn LR, et al. HLA class II haplotype and autoantibody associations in children with juvenile dermatomyositis and juvenile dermatomyositis-scleroderma overlap. Rheumatology (Oxford). 2007;46(12):1786–91. doi:10.1093/rheumatology/kem265.CrossRef Wedderburn LR, et al. HLA class II haplotype and autoantibody associations in children with juvenile dermatomyositis and juvenile dermatomyositis-scleroderma overlap. Rheumatology (Oxford). 2007;46(12):1786–91. doi:10.​1093/​rheumatology/​kem265.CrossRef
112.
go back to reference Arnett FC, et al. Interrelationship of major histocompatibility complex class II alleles and autoantibodies in four ethnic groups with various forms of myositis. Arthritis Rheum. 1996;39(9):1507–18.PubMedCrossRef Arnett FC, et al. Interrelationship of major histocompatibility complex class II alleles and autoantibodies in four ethnic groups with various forms of myositis. Arthritis Rheum. 1996;39(9):1507–18.PubMedCrossRef
113.
go back to reference Arnett FC, et al. The Jo-1 antibody system in myositis: relationships to clinical features and HLA. J Rheumatol. 1981;8(6):925–30.PubMed Arnett FC, et al. The Jo-1 antibody system in myositis: relationships to clinical features and HLA. J Rheumatol. 1981;8(6):925–30.PubMed
114.
go back to reference O’Hanlon TP, et al. Immunogenetic risk and protective factors for the idiopathic inflammatory myopathies: distinct HLA-A, -B, -Cw, -DRB1, and -DQA1 allelic profiles distinguish European American patients with different myositis autoantibodies. Medicine (Baltimore). 2006;85(2):111–27. doi:10.1097/01.md.0000217525.82287.eb.CrossRef O’Hanlon TP, et al. Immunogenetic risk and protective factors for the idiopathic inflammatory myopathies: distinct HLA-A, -B, -Cw, -DRB1, and -DQA1 allelic profiles distinguish European American patients with different myositis autoantibodies. Medicine (Baltimore). 2006;85(2):111–27. doi:10.​1097/​01.​md.​0000217525.​82287.​eb.CrossRef
115.
117.
go back to reference Rothwell S, et al. Dense genotyping of immune-related loci in idiopathic inflammatory myopathies confirms HLA alleles as the strongest genetic risk factor and suggests different genetic background for major clinical subgroups. Ann Rheum Dis. 2015;. doi:10.1136/annrheumdis-2015-208119.PubMed Rothwell S, et al. Dense genotyping of immune-related loci in idiopathic inflammatory myopathies confirms HLA alleles as the strongest genetic risk factor and suggests different genetic background for major clinical subgroups. Ann Rheum Dis. 2015;. doi:10.​1136/​annrheumdis-2015-208119.PubMed
119.
go back to reference Hansen T, et al. Concordance for multiple sclerosis in Danish twins: an update of a nationwide study. Mult Scler. 2005;11(5):504–10.PubMedCrossRef Hansen T, et al. Concordance for multiple sclerosis in Danish twins: an update of a nationwide study. Mult Scler. 2005;11(5):504–10.PubMedCrossRef
131.
go back to reference Marrosu MG, et al. Dissection of the HLA association with multiple sclerosis in the founder isolated population of Sardinia. Hum Mol Genet. 2001;10(25):2907–16.PubMedCrossRef Marrosu MG, et al. Dissection of the HLA association with multiple sclerosis in the founder isolated population of Sardinia. Hum Mol Genet. 2001;10(25):2907–16.PubMedCrossRef
133.
go back to reference Saruhan-Direskeneli G, et al. HLA-DR and -DQ associations with multiple sclerosis in Turkey. Hum Immunol. 1997;55(1):59–65.PubMedCrossRef Saruhan-Direskeneli G, et al. HLA-DR and -DQ associations with multiple sclerosis in Turkey. Hum Immunol. 1997;55(1):59–65.PubMedCrossRef
139.
go back to reference Hasan ZN, et al. Association between human leukocyte antigen-DR and demylinating Guillain–Barre syndrome. Neurosciences (Riyadh). 2014;19(4):301–5. Hasan ZN, et al. Association between human leukocyte antigen-DR and demylinating Guillain–Barre syndrome. Neurosciences (Riyadh). 2014;19(4):301–5.
141.
go back to reference Ma JJ, et al. HLA and T-cell receptor gene polymorphisms in Guillain–Barre syndrome. Neurology. 1998;51(2):379–84.PubMedCrossRef Ma JJ, et al. HLA and T-cell receptor gene polymorphisms in Guillain–Barre syndrome. Neurology. 1998;51(2):379–84.PubMedCrossRef
144.
go back to reference Hyttinen V, et al. Genetic liability of type 1 diabetes and the onset age among 22,650 young Finnish twin pairs: a nationwide follow-up study. Diabetes. 2003;52(4):1052–5.PubMedCrossRef Hyttinen V, et al. Genetic liability of type 1 diabetes and the onset age among 22,650 young Finnish twin pairs: a nationwide follow-up study. Diabetes. 2003;52(4):1052–5.PubMedCrossRef
145.
go back to reference Concannon P, et al. Type 1 diabetes: evidence for susceptibility loci from four genome-wide linkage scans in 1,435 multiplex families. Diabetes. 2005;54(10):2995–3001.PubMedCrossRef Concannon P, et al. Type 1 diabetes: evidence for susceptibility loci from four genome-wide linkage scans in 1,435 multiplex families. Diabetes. 2005;54(10):2995–3001.PubMedCrossRef
146.
go back to reference Rich SS. Mapping genes in diabetes. Genetic epidemiological perspective. Diabetes. 1990;39(11):1315–9.PubMedCrossRef Rich SS. Mapping genes in diabetes. Genetic epidemiological perspective. Diabetes. 1990;39(11):1315–9.PubMedCrossRef
147.
go back to reference Valdes AM, et al. HLA class II DR-DQ amino acids and insulin-dependent diabetes mellitus: application of the haplotype method. Am J Hum Genet. 1997;60(3):717–28.PubMedPubMedCentral Valdes AM, et al. HLA class II DR-DQ amino acids and insulin-dependent diabetes mellitus: application of the haplotype method. Am J Hum Genet. 1997;60(3):717–28.PubMedPubMedCentral
148.
go back to reference Thomson G, et al. Genetic heterogeneity, modes of inheritance, and risk estimates for a joint study of Caucasians with insulin-dependent diabetes mellitus. Am J Hum Genet. 1988;43(6):799–816.PubMedPubMedCentral Thomson G, et al. Genetic heterogeneity, modes of inheritance, and risk estimates for a joint study of Caucasians with insulin-dependent diabetes mellitus. Am J Hum Genet. 1988;43(6):799–816.PubMedPubMedCentral
150.
go back to reference Kawabata Y, et al. Asian-specific HLA haplotypes reveal heterogeneity of the contribution of HLA-DR and -DQ haplotypes to susceptibility to type 1 diabetes. Diabetes. 2002;51(2):545–51.PubMedCrossRef Kawabata Y, et al. Asian-specific HLA haplotypes reveal heterogeneity of the contribution of HLA-DR and -DQ haplotypes to susceptibility to type 1 diabetes. Diabetes. 2002;51(2):545–51.PubMedCrossRef
151.
go back to reference She JX. Susceptibility to type I diabetes: HLA-DQ and DR revisited. Immunol Today. 1996;17(7):323–9.PubMedCrossRef She JX. Susceptibility to type I diabetes: HLA-DQ and DR revisited. Immunol Today. 1996;17(7):323–9.PubMedCrossRef
152.
go back to reference Todd JA, et al. The A3 allele of the HLA-DQA1 locus is associated with susceptibility to type 1 diabetes in Japanese. Proc Natl Acad Sci USA. 1990;87(3):1094–8.PubMedPubMedCentralCrossRef Todd JA, et al. The A3 allele of the HLA-DQA1 locus is associated with susceptibility to type 1 diabetes in Japanese. Proc Natl Acad Sci USA. 1990;87(3):1094–8.PubMedPubMedCentralCrossRef
156.
go back to reference Brix TH, et al. A population-based study of Graves’ disease in Danish twins. Clin Endocrinol (Oxf). 1998;48(4):397–400.CrossRef Brix TH, et al. A population-based study of Graves’ disease in Danish twins. Clin Endocrinol (Oxf). 1998;48(4):397–400.CrossRef
157.
160.
go back to reference Vaidya B, et al. CTLA4 gene and Graves’ disease: association of Graves’ disease with the CTLA4 exon 1 and intron 1 polymorphisms, but not with the promoter polymorphism. Clin Endocrinol (Oxf). 2003;58(6):732–5.CrossRef Vaidya B, et al. CTLA4 gene and Graves’ disease: association of Graves’ disease with the CTLA4 exon 1 and intron 1 polymorphisms, but not with the promoter polymorphism. Clin Endocrinol (Oxf). 2003;58(6):732–5.CrossRef
163.
go back to reference Heward JM, et al. Linkage disequilibrium between the human leukocyte antigen class II region of the major histocompatibility complex and Graves’ disease: replication using a population case control and family-based study. J Clin Endocrinol Metab. 1998;83(10):3394–7. doi:10.1210/jcem.83.10.5137.PubMed Heward JM, et al. Linkage disequilibrium between the human leukocyte antigen class II region of the major histocompatibility complex and Graves’ disease: replication using a population case control and family-based study. J Clin Endocrinol Metab. 1998;83(10):3394–7. doi:10.​1210/​jcem.​83.​10.​5137.PubMed
164.
go back to reference Chen QY, et al. HLA-DRB1*08, DRB1*03/DRB3*0101, and DRB3*0202 are susceptibility genes for Graves’ disease in North American Caucasians, whereas DRB1*07 is protective. J Clin Endocrinol Metab. 1999;84(9):3182–6. doi:10.1210/jcem.84.9.5991.PubMed Chen QY, et al. HLA-DRB1*08, DRB1*03/DRB3*0101, and DRB3*0202 are susceptibility genes for Graves’ disease in North American Caucasians, whereas DRB1*07 is protective. J Clin Endocrinol Metab. 1999;84(9):3182–6. doi:10.​1210/​jcem.​84.​9.​5991.PubMed
166.
167.
go back to reference Sawai Y, DeGroot LJ. Binding of human thyrotropin receptor peptides to a Graves’ disease-predisposing human leukocyte antigen class II molecule. J Clin Endocrinol Metab. 2000;85(3):1176–9. doi:10.1210/jcem.85.3.6376.PubMed Sawai Y, DeGroot LJ. Binding of human thyrotropin receptor peptides to a Graves’ disease-predisposing human leukocyte antigen class II molecule. J Clin Endocrinol Metab. 2000;85(3):1176–9. doi:10.​1210/​jcem.​85.​3.​6376.PubMed
168.
go back to reference Ban Y, et al. The influence of human leucocyte antigen (HLA) genes on autoimmune thyroid disease (AITD): results of studies in HLA-DR3 positive AITD families. Clin Endocrinol (Oxf). 2002;57(1):81–8.CrossRef Ban Y, et al. The influence of human leucocyte antigen (HLA) genes on autoimmune thyroid disease (AITD): results of studies in HLA-DR3 positive AITD families. Clin Endocrinol (Oxf). 2002;57(1):81–8.CrossRef
169.
go back to reference Katsuren E, et al. HLA class II alleles in Japanese patients with Graves’ disease: weak associations of HLA-DR and -DQ. Endocr J. 1994;41(6):599–603.PubMedCrossRef Katsuren E, et al. HLA class II alleles in Japanese patients with Graves’ disease: weak associations of HLA-DR and -DQ. Endocr J. 1994;41(6):599–603.PubMedCrossRef
170.
go back to reference Onuma H, et al. Association of HLA-DPB1*0501 with early-onset Graves’ disease in Japanese. Hum Immunol. 1994;39(3):195–201.PubMedCrossRef Onuma H, et al. Association of HLA-DPB1*0501 with early-onset Graves’ disease in Japanese. Hum Immunol. 1994;39(3):195–201.PubMedCrossRef
175.
go back to reference Fox RI, et al. Synovial fluid lymphocytes differ from peripheral blood lymphocytes in patients with rheumatoid arthritis. J Immunol. 1982;128(1):351–4.PubMed Fox RI, et al. Synovial fluid lymphocytes differ from peripheral blood lymphocytes in patients with rheumatoid arthritis. J Immunol. 1982;128(1):351–4.PubMed
176.
go back to reference Veys EM, et al. Determination of T lymphocyte subpopulations by monoclonal antibodies in rheumatoid arthritis. Influence of immunomodulating agents. Int J Immunopharmacol. 1981;3(3):313–9.PubMedCrossRef Veys EM, et al. Determination of T lymphocyte subpopulations by monoclonal antibodies in rheumatoid arthritis. Influence of immunomodulating agents. Int J Immunopharmacol. 1981;3(3):313–9.PubMedCrossRef
179.
go back to reference Moreno-Otero R, et al. Reduced numbers of CD8+ T cells and B cell-expression of Leu-8 antigen in peripheral blood of patients with primary biliary cirrhosis. Hepatogastroenterology. 1994;41(3):239–43.PubMed Moreno-Otero R, et al. Reduced numbers of CD8+ T cells and B cell-expression of Leu-8 antigen in peripheral blood of patients with primary biliary cirrhosis. Hepatogastroenterology. 1994;41(3):239–43.PubMed
181.
go back to reference LaFleur C, et al. HLA-DR antigen frequencies in Mexican patients with dengue virus infection: HLA-DR4 as a possible genetic resistance factor for dengue hemorrhagic fever. Hum Immunol. 2002;63(11):1039–44.PubMedCrossRef LaFleur C, et al. HLA-DR antigen frequencies in Mexican patients with dengue virus infection: HLA-DR4 as a possible genetic resistance factor for dengue hemorrhagic fever. Hum Immunol. 2002;63(11):1039–44.PubMedCrossRef
182.
go back to reference Han YN, et al. Relationship of human leukocyte antigen class II genes with the susceptibility to hepatitis B virus infection and the response to interferon in HBV-infected patients. World J Gastroenterol. 2005;11(36):5721–4.PubMedPubMedCentralCrossRef Han YN, et al. Relationship of human leukocyte antigen class II genes with the susceptibility to hepatitis B virus infection and the response to interferon in HBV-infected patients. World J Gastroenterol. 2005;11(36):5721–4.PubMedPubMedCentralCrossRef
184.
187.
go back to reference Gokhale P, et al. Variations in immunogenetics, human papillomavirus (HPV) infection & predisposition to cervical cancer in Indian women. Indian J Med Res. 2014;140(Suppl):S36–43.PubMedPubMedCentral Gokhale P, et al. Variations in immunogenetics, human papillomavirus (HPV) infection & predisposition to cervical cancer in Indian women. Indian J Med Res. 2014;140(Suppl):S36–43.PubMedPubMedCentral
188.
go back to reference Thanapati S, et al. Association of human leukocyte antigen class II allele and haplotypes in chikungunya viral infection in a western Indian population. Trans R Soc Trop Med Hyg. 2014;108(5):277–82. doi:10.1093/trstmh/tru030.PubMedCrossRef Thanapati S, et al. Association of human leukocyte antigen class II allele and haplotypes in chikungunya viral infection in a western Indian population. Trans R Soc Trop Med Hyg. 2014;108(5):277–82. doi:10.​1093/​trstmh/​tru030.PubMedCrossRef
190.
200.
201.
go back to reference Li Q, et al. Epstein-Barr virus uses HLA class II as a cofactor for infection of B lymphocytes. J Virol. 1997;71(6):4657–62.PubMedPubMedCentral Li Q, et al. Epstein-Barr virus uses HLA class II as a cofactor for infection of B lymphocytes. J Virol. 1997;71(6):4657–62.PubMedPubMedCentral
202.
go back to reference Truedsson L, et al. Sharing of MHC haplotypes among patients with systemic lupus erythematosus from unrelated Caucasian multicase families: disease association with the extended haplotype [HLA-B8, SC01, DR17]. J Rheumatol. 1995;22(10):1852–61.PubMed Truedsson L, et al. Sharing of MHC haplotypes among patients with systemic lupus erythematosus from unrelated Caucasian multicase families: disease association with the extended haplotype [HLA-B8, SC01, DR17]. J Rheumatol. 1995;22(10):1852–61.PubMed
203.
go back to reference Marchini M, et al. HLA class II antigens associated with lupus nephritis in Italian SLE patients. Hum Immunol. 2003;64(4):462–8.PubMedCrossRef Marchini M, et al. HLA class II antigens associated with lupus nephritis in Italian SLE patients. Hum Immunol. 2003;64(4):462–8.PubMedCrossRef
208.
go back to reference Zandman-Goddard G, et al. A comparison of autoantibody production in asymptomatic and symptomatic women with silicone breast implants. J Rheumatol. 1999;26(1):73–7.PubMed Zandman-Goddard G, et al. A comparison of autoantibody production in asymptomatic and symptomatic women with silicone breast implants. J Rheumatol. 1999;26(1):73–7.PubMed
209.
go back to reference Bar-Meir E, et al. Silicone gel breast implants and connective tissue disease—a comprehensive review. Autoimmunity. 2003;36(4):193–7.PubMedCrossRef Bar-Meir E, et al. Silicone gel breast implants and connective tissue disease—a comprehensive review. Autoimmunity. 2003;36(4):193–7.PubMedCrossRef
215.
222.
go back to reference Mineta M, et al. Contribution of HLA class I and class II alleles to the regulation of antibody production to hepatitis B surface antigen in humans. Int Immunol. 1996;8(4):525–31.PubMedCrossRef Mineta M, et al. Contribution of HLA class I and class II alleles to the regulation of antibody production to hepatitis B surface antigen in humans. Int Immunol. 1996;8(4):525–31.PubMedCrossRef
230.
go back to reference Pan L, et al. A genome-wide association study identifies polymorphisms in the HLA-DR region associated with non-response to hepatitis B vaccination in Chinese Han populations. Hum Mol Genet. 2014;23(8):2210–9. doi:10.1093/hmg/ddt586.PubMedCrossRef Pan L, et al. A genome-wide association study identifies polymorphisms in the HLA-DR region associated with non-response to hepatitis B vaccination in Chinese Han populations. Hum Mol Genet. 2014;23(8):2210–9. doi:10.​1093/​hmg/​ddt586.PubMedCrossRef
Metadata
Title
HLA-DRB1 the notorious gene in the mosaic of autoimmunity
Authors
María-Teresa Arango
Carlo Perricone
Shaye Kivity
Enrica Cipriano
Fulvia Ceccarelli
Guido Valesini
Yehuda Shoenfeld
Publication date
01-02-2017
Publisher
Springer US
Published in
Immunologic Research / Issue 1/2017
Print ISSN: 0257-277X
Electronic ISSN: 1559-0755
DOI
https://doi.org/10.1007/s12026-016-8817-7

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