CTLA-4 gene polymorphisms and susceptibility to type 1 diabetes mellitus: A HuGE review and meta-analysis

American Journal of Epidemiology

Volumn 162, Issue 1, 2005, Pages 3-16

  Kavvoura, Fotini K ^a   Ioannidis, John P A ^a,b,c  

^a UNIVERSITY OF IOANNINA   (Greece)

^b INSTITUTE OF COMPUTER SCIENCE   (Greece)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CTLA 4; Diabetes mellitus, type 1; Epidemiology; Genes; Meta analysis; Polymorphism, genetic

Indexed keywords

AUTOANTIBODY; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GLUTAMATE DECARBOXYLASE 65 ANTIBODY;

DIABETES; META-ANALYSIS;

BASE PAIRING; DNA POLYMORPHISM; EMBASE; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC EPIDEMIOLOGY; GENETIC SUSCEPTIBILITY; GENOTYPE; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; MEDLINE; MICROSATELLITE MARKER; ONSET AGE; REVIEW;

ANTIGENS, CD; ANTIGENS, DIFFERENTIATION; AUTOANTIBODIES; DEVELOPED COUNTRIES; DIABETES MELLITUS, TYPE 1; GENETIC HETEROGENEITY; GENETIC PREDISPOSITION TO DISEASE; GLUTAMATE DECARBOXYLASE; HUMANS; ISOENZYMES; MICROSATELLITE REPEATS; POLYMORPHISM, GENETIC;

EID: 21244490890     PISSN: 00029262     EISSN: None     Source Type: Journal    
DOI: 10.1093/aje/kwi165     Document Type: Review

References (91)

1. Brunet JF, Denizot F, Luciani MF, et al. A new member of the immunoglobulin superfamily-CTLA-4. Nature 1987;328: 267-70.
2. Vaidya B, Pearce S. The emerging role of the CTLA-4 gene in autoimmune endocrinopathies. Eur J Endocrinol 2004;150: 619-26.
3. Kristiansen OP, Larsen ZM, Pociot F. CTLA-4 in autoimmune diseases-a general susceptibility gene to autoimmunity? Genes Immun 2000;1:170-84.
4. Waterhouse P, Penninger JM, Timms E, et al. Lymphoproliferative disorders with early lethality in mice deficient in CTLA-4. Science 1995;270:985-8.
5. Tivol EA, Borriello F, Schweitzer AN, et al. Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 1995;3:541-7.
6. Harbo HF, Celius EG, Vartdal F, et al. CTLA-4 promoter and exon 1 dimorphisms in multiple sclerosis. Tissue Antigens 1999;53:106-10.
7. Seidl C, Donner H, Fischer B, et al. CTLA-4 codon 17 dimorphism in patients with rheumatoid arthritis. Tissue Antigens 1998;51:62-6.
8. Vaidya B, Pearce SH, Charlton S, et al. An association between the CTLA-4 exon 1 polymorphism and early rheumatoid arthritis with autoimmune endocrinopathies. Rheumatology (Oxf) 2002;41:180-3.
9. Djilali-Saiah I, Schmitz J, Harfouch-Hammoud E, et al. CTLA-4 gene polymorphism is associated with predisposition to coeliac disease. Gut 1998;43:187-9.
10. Agarwal K, Jones DE, Daly AK, et al. CTLA-4 gene polymorphism confers susceptibility to primary biliary cirrhosis. J Hepatol 2000;32:538-41.
11. Dariavach P, Mattei MG, Goldstein P, et al. Human Ig superfamily CTLA-4 gene: chromosomal localization and identity of protein sequence between murine and human CTLA-4 cytoplasmic domains. Eur J Immunol 1988;18:1901-5.
12. Deichmann K, Heinzmann A, Bruggenolte E, et al. An Mse I RFLP in the human CTLA4 promoter. Biochem Biophys Res Commun 1996;225:817-18.
13. Nistico L, Buzzetti R, Pritchard LE, et al. The CTLA-4 gene region of chromosome 2q33 is linked to, and associated with, type 1 diabetes. Belgian Diabetes Registry. Hum Mol Genet 1996;5:1075-80.
14. Harper K, Balzano C, Rouvier E, et al. CTLA-4 and CD28 activated lymphocyte molecules are closely related in both mouse and human as to sequence, message expression, gene structure, and chromosomal location. J Immunol 1996; 147:1037-44.
15. Donner H, Seidl C, Braun J, et al. CTLA4 gene haplotypes cannot protect from IDDM in the presence of high-risk HLA DQ8 or DQ2 alleles in German families. Diabetes 1998;47: 1158-60.
16. Larsen ZM, Kristiansen OP, Mato E, et al. IDDM12 (CTLA4) on 2q33 and IDDM13 on 2q34 in genetic susceptibility to type 1 diabetes (insulin-dependent). Autoimmunity 1998;31:35-42.
17. Kouki T, Gardine CA, Yanagawa T, et al. Relation of three polymorphisms of the CTLA-4 gene in patients with Graves' disease. J Endocrinol Invest 2002;25:208-13.
18. Shaw G, Kamen R. A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 1986;46:659-67.
19. Maurer M, Loserth S, Kolb-Maurer A, et al. A polymorphism in the human cytotoxic T-lymphocyte antigen 4 (CTLA4) gene (exon 1+49) alters T-cell activation. Immunogenetics 2002; 54:1-8.
20. Kouki T, Sawai Y, Gardine CA, et al. CTLA-4 gene polymorphism at position 49 in exon 1 reduces the inhibitory function of CTLA-4 and contributes to the pathogenesis of Graves' disease. J Immunol 2000;165:6606-11.
21. Donner H, Rau H, Walfish PG, et al. CTLA4 alanine-17 confers genetic susceptibility to Graves' disease and to type 1 diabetes mellitus. J Clin Endocrinol Metab 1997;82:143-6.
22. Van der Auwera BJ, Vandewalle CL, Schuit FC, et al. CTLA-4 gene polymorphism confers susceptibility to insulin-dependent diabetes mellitus (IDDM) independently from age and from other genetic or immune disease markers. Clin Exp Immunol 1997;110:98-103.
23. Krokowski M, Bodalski J, Bratek A, et al. CTLA-4 gene polymorphism is associated with predisposition to IDDM in a population from central Poland. Diabetes Metab 1998; 24:241-3.
24. Djilali-Saiah I, Larger E, Harfouch-Hammound E, et al. No major role for the CTLA-4 gene in the association of autoimmune thyroid disease with IDDM. Diabetes 1998;47:125-7.
25. Awata T, Kurihara S, Iitaka M, et al. Association of CTLA-4 gene A-G polymorphism (IDDM12 locus) with acute-onset and insulin-depleted IDDM as well as autoimmune thyroid disease (Graves' disease and Hashimoto's thyroiditis) in the Japanese population. Diabetes 1998;47:128-9.
26. Yanagawa T, Maruyama T, Gomi K, et al. Lack of association between CTLA-4 gene polymorphism and IDDM in Japanese subjects. Autoimmunity 1999;29:53-5.
27. Hayashi H, Kusaka I, Nagasaka S, et al. Association of CTLA-4 polymorphism with positive anti-GAD antibody in Japanese subjects with type 1 diabetes mellitus. Clin Endocrinol (Oxf) 1999;51:793-9.
28. Abe T, Takino H, Yamazaki H, et al. CTLA4 gene polymorphism correlates with the mode of onset of ICA512 Ab in Japanese type 1 diabetes. Diabetes Res Clin Pract 1999;46:169-75.
29. Takara M, Komiya I, Kinjo Y, et al. Association of CTLA-4 gene A/G polymorphism in Japanese type 1 diabetic patients with younger age of onset and autoimmune thyroid disease. Diabetes Care 2000;23:975-8.
30. Lee YJ, Huang FY, Lo FS, et al. Association of CTLA4 gene A-G polymorphism with type 1 diabetes in Chinese children. Clin Endocrinol (Oxf) 2000;52:153-7.
31. Ihara K, Ahmed S, Nakao F, et al. Association studies of CTLA-4, CD28, and ICOS gene polymorphisms with type diabetes in the Japanese population. Immunogenetics 2001; 53:447-54.
32. Kamoun Abid H, Hmida S, Smaoui N, et al. Association between type 1 diabetes and polymorphism of the CTLA-4 gene in a Tunisian population. (In French). Pathol Biol (Paris) 2001;49:794-8.
33. Osei-Hyiaman D, Hou L, Zhiyin R, et al. Association of a novel point mutation (C159G) of the CTLA4 gene with type 1 diabetes in West Africans but not in Chinese. Diabetes 2001;50:2169-71.
34. McCormack RM, Maxwell AP, Carson D, et al. Possible association between CTLA4 DNA polymorphisms and early onset type 1 diabetes in a UK population. Genes Immun 2001;2:233-5.
35. Kikuoka N, Sugihara S, Yanagawa T, et al. Cytotoxic T lymphocyte antigen 4 gene polymorphism confers susceptibility to type 1 diabetes in Japanese children: analysis of association with HLA genotypes and autoantibodies. Clin Endocrinol (Oxf) 2001;55:597-603.
36. Cosentino A, Gambelunghe G, Tortoioli C, et al. CTLA-4 gene polymorphism contributes to the genetic risk for latent autoimmune diabetes in adults. Ann N Y Acad Sci 2002; 958:337-40.
37. Fajardy I, Vambergue A, Stuckens C, et al. CTLA-4 49 A/G dimorphism and type 1 diabetes susceptibility: a French case-control study and segregation analysis. Evidence of a maternal effect. Eur J Immunogenet 2002;29:251-7.
38. Cinek O, Drevinek P, Sumnik Z, et al. The CTLA4 +49 A/G dimorphism is not associated with type 1 diabetes in Czech children. Eur J Immunogenet 2002;29:219-22.
39. Ma Y, Tang X, Chang W, et al. CTLA-4 gene A/G polymorphism associated with diabetes mellitus in Han Chinese. Chin Med J (Engl) 2002;115:1248-50.
40. Klitz W, Bugawan TL, Panelo A, et al. Association of CTLA-4 variation with type I diabetes in Filipinos. Immunogenetics 2002;54:310-13.
41. Wood JP, Pani MA, Bieda K, et al. A recently described polymorphism in the CD28 gene on chromosome 2q33 is not associated with susceptibility to type 1 diabetes. Eur J Immunogenet 2002;29:347-9.
42. Ongagna JC, Sapin R, Pinget M, et al. Markers for risk of type 1 diabetes in relatives of Alsacian patients with type 1 diabetes. Int J Exp Diabetes Res 2002;3:1-9.
43. Mochizuki M, Amemiya S, Kobayashi K, et al. Association of the CTLA-4 gene 49 A/G polymorphism with type 1 diabetes and autoimmune thyroid disease in Japanese children. Diabetes Care 2003;26:843-7.
44. Bouqbis L, Izaabel H, Akhayat O, et al. Association of the CTLA4 promoter region (-1661G allele) with type 1 diabetes in the South Moroccan population. Genes Immun 2003;4:132-7.
45. Zalloua P, Abchee A, Shbaklo H, et al. Patients with early onset of type 1 diabetes have significantly higher GG genotype at position 49 of the CTLA4 gene. Hum Immunol 2004; 65:719-24.
46. Haller K, Kisand K, Nemvalts V, et al. Type 1 diabetes is insulin -2221 MspI and CTLA-4 +49 A/G polymorphism dependent. Eur J Clin Invest 2004;34:543-8.
47. Ide A, Kawasaki F, Abiru N, et al. Association between IL-18 gene promoter polymorphisms and CTLA-4 gene 49 A/G polymorphism in Japanese patients with type 1 diabetes. J Autoimmun 2004;22:73-8.
48. Lee YJ, Lo FS, Shu SG, et al. The promoter region of the CTLA4 gene is associated with type 1 diabetes mellitus. J Pediatr Endocrinol Metab 2001;14:383-8.
49. Bassuny WM, Ihara K, Matsuura N, et al. Association study of the NRAMP1 gene promoter polymorphism and early-onset type 1 diabetes. Immunogenetics 2002;54:282-5.
50. Lowe RM, Graham J, Sund G, et al. The length of the CTLA-4 microsatellite (AT)N-repeat affects the risk for type 1 diabetes. Diabetes Incidence in Sweden Study Group. Autoimmunity 2000;32:173-80.
51. Ban Y, Taniyama M, Tozaki T, et al. No association of type 1 diabetes with a microsatellite marker for CTLA-4 in a Japanese population. Autoimmunity 2001;34:39-43.
52. Owerbach D, Naya FJ, Tsai MJ, et al. Analysis of candidate genes for susceptibility to type I diabetes: a case-control and family-association study of genes on chromosome 2q31-35. Diabetes 1997;46:1069-74.
53. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2004;27(suppl 1):S5-10.
54. Karvonen M, Tuomilehto J, Libman I, et al. A review of the recent epidemiological data on the worldwide incidence of type 1 (insulin-dependent) diabetes mellitus. World Health Organization DIAMOND Project Group. Diabetologia 1993; 36:883-92.
55. Dorman JS, Bunker CH. HLA-DQ locus of the human leucocyte antigen complex and type 1 diabetes mellitus: a HuGE review. Epidemiol Rev 2000;22:218-27.
56. Hawa MI, Beyan H, Buckley LR, et al. Impact of genetic and non-genetic factors in type 1 diabetes. Am J Med Genet 2002;115:8-17.
57. Karvonen M, Pitkniemi M, Pitkniemi J, et al. Sex difference in the incidence of IDDM: an analysis of the recent epidemiological data. Diabetes Metab Rev 1997;13:275-91.
58. Levy-Marchal C, Patterson C, Green A. Variation by age and seasonality at diagnosis of childhood IDDM in Europe. The EURODIAB ACE Study Group. Diabetologia 1995;38: 823-30.
59. Foulis AK. The pathology of the endocrine pancreas in type I (insulin-dependent) diabetes mellitus. APMIS 1996;104:161-7.
60. von Herrath MG, Holz A, Homann D, et al. Role of viruses in type I diabetes. Semin Immunol 1998;10:87-100.
61. Graves M, Norris JM, Pallansch MA, et al. The role of enteroviral infections in the development of IDDM: limitations of current approaches. Diabetes 1997;46:161-8.
62. Andrcoletti L, Hober D, Hober-Vandenberghc C, et al. Coxsackie B virus infection and beta cell autoantibodies in newly diagnosed IDDM adult patients. Clin Diagn Virol 1998;9:125-33.
63. Hyoty H, Hiltunen M, Reuranen A, et al. Decline of mumps antibodies in type 1 (insulin-dependent) diabetic children with a plateau in the rising incidence of type 1 diabetes after introduction of the mumps-measles-rubella vaccine in Finland. Diabetologia 1993;36:1303-8.
64. McIntosh EDG, Menser M. A fifty-year follow-up of congenital rubella. Lancet 1992;340:414-15.
65. Todd JA, Bell JI, McDevitt HO. HLA-DQ gene contributes to susceptibility and resistance to IDDM. Nature 1987;329: 599-604.
66. Todd JA, Acha-Orbea H, Bell JI, et al. A molecular basis for MHC class II-associated autoimmunity. Science 1988;240: 1003-9.
67. Thomson G, Robinson W, Kuhner M, et al. HLA and insulin gene associations with IDDM. Genet Epidemiol 1989;6: 155-60.
68. Bell Jl, Horita S, Karam JH. A polymorphic locus near the human insulin gene is associated with IDDM. Diabetes 1984;33:176-83.
69. Bennett ST, Lucassen AM, Gough SCL, et al. Susceptibility to human type 1 diabetes at IDDM2 is determined by tandem repeat variation at the insulin gene minisatellite locus. Nat Genet 1995;9:284-92.
70. Bell GI, Horita S, Karam JH. A polymorphic locus near the human insulin gene is associated with insulin-dependent diabetes mellitus. Diabetes 1984;33:176-83.
71. Todd JA, Farrall M. Panning for gold: genome-wide scanning for linkage in type 1 diabetes. Hum Mol Genet 1995;5: 1443-8.
72. Concannon P, Gogolin Ewens KJ, Hinds DA, et al. A second-generation screen of the human genome for susceptibility to insulin-dependent diabetes mellitus. Nat Genet 1998; 19:292-6.
73. Davies JL, Kawaguchi Y, Bennett ST, et al. A genome-wide search for human type 1 diabetes susceptibility genes. Nature 1994;371:130-6.
74. Marron MP, Zeidler A, Raffel LJ, et al. Genetic and physical mapping of a type 1 diabetes susceptibility gene (IDDM12) to a 100-kb phagemid artificial chromosome clone containing D2S72-CTLA4-D2S105 on chromosome 2q33. Diabetes 2000;49:492-9.
75. Lau J, Ioannidis JP, Schmid CH. Quantitative synthesis in systematic reviews. Ann Intern Med 1997;127:820-6.
76. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002;21:1539-58.
77. Ioannidis JP, Contopoulos-Ioannidis DG, Lau J. Recursive cumulative meta-analysis: a diagnostic for the evolution of total randomized evidence from group and individual patient data. J Clin Epidemiol 1999;52:281-91.
78. Ioannidis JPA, Ntzani EE, Trikalinos TA, et al. Replication validity of genetic association studies. Nat Genet 2001;29: 306-9.
79. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics 1994;50:1088-101.
80. Turpeinen H, Laine AP, Hermann R, et al. A linkage analysis of the CTLA4 gene region in Finnish patients with type 1 diabetes. Eur J Immunogenet 2003;30:289-93.
81. Ioannidis JP, Trikalinos TA, Ntzani EE, et al. Genetic associations in large versus small studies: an empirical assessment. Lancet 2003;361:567-71.
82. Easterbrook PJ, Berlin JA, Gopalan R, et al. Publication bias in clinical research. Lancet 1991;337:867-72.
83. Ioannidis JP. Effect of the statistical significance of results on the time to completion and publication of randomized efficacy trials. JAMA 1998;279:281-6.
84. Ioannidis JP, Ntzani EE, Trikalinos TA. 'Racial' differences in genetic effects for complex diseases. Nat Genet 2004;36: 1312-18.
85. Laine A-P, Nejentsev S, Veijola R, et al. A linkage study of 12 IDDM susceptibility loci in the Finnish population. Diabetes Metab Res Rev 2004;20:144-9.
86. Ioannidis JP. Genetic associations: false or true? Trends Mol Med 2003;9:135-8.
87. Little J, Khoury MJ, Bradley L, et al. The Human Genome Project is complete. How do we develop a handle for the pump? (Editorial). Am J Epidemiol 2003;157:667-73.
88. Gale EA, Bingley PJ, Emmett CL, et al. European Nicotinamide Diabetes Intervention Trial (ENDIT): a randomised controlled trial of intervention before the onset of type 1 diabetes. Lancet 2004;363:925-31.
89. Diabetes Prevention Trial-Type 1 Diabetes Study Group. Effects of insulin in relatives of patients with type 1 diabetes mellitus. N Engl J Med 2002;346:1685-9l.
90. Paronen J, Knip M, Savilahti E, et al. Effect of cow's milk exposure and maternal type 1 diabetes on cellular and humoral immunization to dietary insulin in infants at genetic risk for type 1 diabetes. Finnish Trial to Reduce IDDM in the Genetically At Risk Study Group. Diabetes 2000;49:1657-65.
91. Ilonen J, Simell O, Knip M, et al. Screening for genetic IDDM risk and prevention trials in infancy. Diabetes Metab Rev 1998;14:188.