Association of the T-cell regulatory gene CTLA4 with susceptibility to autoimmune disease

Nature

Volumn 423, Issue 6939, 2003, Pages 506-511

  Ueda, Hironori ^a   Howson, Joanna M M ^a   Esposito, Laura ^a   Heward, Joanne ^b   Snook, Hywel ^a   Chamberlain, Giselle ^a   Rainbow, Daniel B ^a   Hunter, Kara M D ^a   Smith, Annabel N ^a   Di Genova, Gianfranco ^a,m   Herr, Mathias H ^a,n   Dahlman, Ingrid ^a,o   Payne, Felicity ^a   Smyth, Deborah ^a   Lowe, Christopher ^a   Twells, Rebecca C J ^a   Howlett, Sarah ^a   Healy, Barry ^a   Nutland, Sarah ^a   Rance, Helen E ^a   Everett, Vin ^a   Smink, Luc J ^a   Lam, Alex C ^a   Cordell, Heather J ^a   Walker, Neil M ^a   Bordin, Cristina ^a,p   Hulme, John ^a   Motzo, Costantino ^c   Cucca, Francesco ^c   Hess, J Fred ^d   Metzker, Michael L ^d,q   Rogers, Jane ^e   Gregory, Simon ^e   Allahabadia, Amit ^b,r   Nithiyananthan, Ratnasingam ^b   Tuomilehto Wolf, Eva ^f   Tuomilehto, Jaakko ^f   Bingley, Polly ^g   Gillespie, Kathleen M ^g   Undlien, Dag E ^h,s   Rønningen, Kjersti S ⁱ   Guja, Cristian ^j   Ionescu Tirgovişte, Constantin ^j   Savage, David A ^k   Maxwell, A Peter ^l   Carson, Dennis J ^k   Patterson, Chris C ^k   Franklyn, Jayne A ^b   Clayton, David G ^a   Peterson, Laurence B ^d   Wicker, Linda S ^a   Todd, John A ^a   Gough, Stephen C L ^b   more..

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c UNIVERSITY OF CAGLIARI   (Italy)

^d MERCK RESEARCH LABORATORIES   (United States)

^e WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^f UNIVERSITY OF HELSINKI   (Finland)

^g UNIVERSITY OF BRISTOL   (United Kingdom)

^h ULLEVÅL UNIVERSITY HOSPITAL   (Norway)

ⁱ NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

^j Institute of Diabetes   (Romania)

^k QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^l BELFAST CITY HOSPITAL   (United Kingdom)

^m SOUTHAMPTON GENERAL HOSPITAL   (United Kingdom)

ⁿ HUMBOLDT UNIVERSITY   (Germany)

^o KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^p HUTCHISON MRC RESEARCH CENTRE   (United Kingdom)

^q BAYLOR COLLEGE OF MEDICINE   (United States)

^r UNIVERSITY OF SHEFFIELD   (United Kingdom)

^s UNIVERSITY OF OSLO   (Norway)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DISEASES; GENETIC ENGINEERING; IMMUNOLOGY; RNA; TISSUE;

AUTOIMMUNE DISORDERS;

GENES;

CYTOTOXIC T LYMPHOCYTE ANTIGEN 4;

DISEASE;

ADULT; ALTERNATIVE RNA SPLICING; ARTICLE; AUTOIMMUNE DISEASE; CYTOTOXIC T LYMPHOCYTE; FEMALE; GENE MAPPING; GENETIC ASSOCIATION; GENETIC RISK; GENETIC SUSCEPTIBILITY; GENOTYPE; GRAVES DISEASE; HUMAN; HUMAN CELL; IMMUNE SYSTEM; INSULIN DEPENDENT DIABETES MELLITUS; LIGAND BINDING; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; T LYMPHOCYTE ACTIVATION;

ALTERNATIVE SPLICING; ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION; AUTOIMMUNE DISEASES; BASE SEQUENCE; DIABETES MELLITUS, TYPE 1; DISEASE MODELS, ANIMAL; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; GRAVES DISEASE; HUMANS; HYPOTHYROIDISM; IMMUNOCONJUGATES; MICE; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN ISOFORMS; T-LYMPHOCYTES;

EID: 0037648405     PISSN: 00280836     EISSN: None     Source Type: Journal    
DOI: 10.1038/nature01621     Document Type: Article

References (46)

1. Lohmueller, K. E., Pearce, C. L., Pike, M., Lander, E. S. & Hirschhorn, J. N. Meta-analysis of genetic association studies supports a contribution of common variants to susceptibility to common disease. Nature Genet. 33, 177-182 (2003).
2. Dahlman, I. et al. Parameters for reliable results in genetic association studies in common disease. Nature Genet. 30, 149-150 (2002).
3. Lesage, S. & Goodnow, C. C. Organ-specific autoimmune disease: a deficiency of tolerogenic stimulation. J. Exp. Med. 194, F31-F36 (2001).
4. Finger, E. & Bluestone, J. When ligand becomes receptor-tolerance via B7 signaling on DCs. Nature Immunol. 3, 1056-1057 (2002).
5. Egen, J. G., Kuhns, M. S. & Allison, J. P. CTLA-4: new insights into its biological function and use in tumour immunotherapy. Nature Immunol. 3, 611-618 (2002).
6. Nistico, L. et al. The CTLA-4 gene region of chromosome 2q33 is linked to, and associated with, type 1 diabetes. Hum. Mol. Gen. 5, 1075-1080 (1996).
7. Marron, M. P. 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 49, 492-499 (2000).
8. Allahabadia, A. et al. The MHC class II region, CTLA-4 gene and ophthalmopathy in patients with Graves' disease. Lancet 358, 984-985 (2001).
9. Kristiansen, O. P., Larsen, Z. M. & Pociot, F. CTLA-4 in autoimmune diseases - a general susceptibility gene to autoimmunity? Genes Immun. 1, 170-184 (2000).
10. Colucci, F., Bergman, M., Penha-Goncalves, C., Cilio, C. M. & Holmberg, D. Apoptosis resistance of nonobese diabetic peripheral lymphocytes linked to the Idd5 diabetes susceptibility region. Proc. Natl Acad. Sci. USA 94, 8670-8674 (1997).
11. Hill, N. J. et al. The NOD Idd5 locus controls insulitis and diabetes and overlaps the orthologous CTLA4/IDDM12 and NRAMP1 loci in humans. Diabetes 49, 1744-1747 (2000).
12. Lamhamedi-Cherradi, S. E. et al. Further mapping of the Idd5.1 locus for autoimmune diabetes in NOD mice. Diabetes 50, 2874-2878 (2001).
13. Sharpe, A. H. & Freeman, G. J. The B7-CD28 superfamily. Nature Rev. Immunol. 2, 116-126 (2002).
14. Grohmann, U. et al. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nature Immunol. 3, 1097-1101 (2002).
15. Lin, H, et al. Cytotoxic T lymphocyte antigen 4 (CTLA4) blockade accelerates the acute rejection of cardiac allografts in CD28-deficient mice: CTLA4 can function independently of CD28. J. Exp. Med. 188, 199-204 (1998).
16. Chikuma, S., Imboden, J. & Bluestone, J. A. Negative regulation of T cell receptor-lipid raft interaction by cytotoxic T lymphocyte-associated antigen 4. J. Exp. Med. 197, 129-135 (2003).
17. Gabriel, S. B. et al. The structure of haplotype blocks in the human genome. Science 296, 2225-2229 (2002).
18. Cordell, H. J. & Clayton, D. G. A unified stepwise regression procedure for evaluating the relative effects of polymorphisms within a gene using case/control or family data: application to HLA in type 1 diabetes. Am. J. Hum. Genet. 70, 124-141 (2002).
19. Magistrelli, G. et al. A soluble form of CTLA-4 generated by alternative splicing is expressed by nonstimulated human T cells. Eur. J. Immunol. 29, 3596-3602 (1999).
20. Oaks, M. K. & Hallett, K. M. Cutting edge: a soluble form of CTLA-4 in patients with autoimmune thyroid disease. J. Immunol. 164, 5015-5018 (2000).
21. Oaks, M. K. et al. A native soluble form of CTLA-4. Cell Immunol. 201, 144-153 (2000).
22. Kaijzel, E. L. et al. Allele-specific quantification of tumour necrosis factor alpha (TNF) transcription and the role of promoter polymorphisms in rheumatoid arthritis patients and healthy individuals. Genes Immun. 2, 135-144 (2001).
23. Lynch, K. W. & Weiss, A. A CD45 polymorphism associated with multiple sclerosis disrupts an exonic splicing silencer. J. Biol. Chem. 276, 24341-24347 (2001).
24. Zheng, Z.-M., He, P.-J. & Baker, C. Function of a bovine papillomavirus type 1 exonic splicing suppressor requires a suboptimal upstream 3′ splice site. J. Virol. 73, 29-36 (1999).
25. Asano, M., Toda, M., Sakguchi, N. & Sakaguchi, S. Autoimmune disease as a consequence of developmental abnormality of a T cell population. J. Exp. Med. 184, 387-396 (1996).
26. + regulatory cells. Eur. J. Immunol. 32, 2888-2896 (2002).
27. Maloy K. J. et al. CD4 + CD25 + T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms. J. Exp. Med. 197, 111-119 (2003).
28. Sakaguchi, S. Control of immune responses by naturally arising CD4(+) regulatory T cells that express Toll-like receptors. J. Exp. Med. 197, 397-401 (2003).
29. + T cell-mediated suppression by dendritic cells. Science 299, 1033-1036 (2003).
30. Kaufman, K. A. et al. The CTLA-4 gene is expressed in placental fibroblasts. Mol. Hum. Reprod. 5, 84-87 (1999).
31. Huang, D., Giscombe, R., Zhou, Y., Pirskanen, R. & Lefvert, A. Dinucleotide repeat expansion in the CTLA-4 gene leads to T cell hyper-reactivity via the CD28 pathway in myasthenia gravis. J. Neuroimmunol. 105, 69-77 (2000).
32. Kouki, T. 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. 165, 6606-6611 (2000).
33. Maurer, M. et al. A polymorphism in the human cytotoxic T-lymphocyte antigen 4 (CTLA4) gene (exon 1 +49) alters T-cell activation. Immunogenetics 54, 1-8 (2002).
34. Magistrelli, G. et al. Identification of three alternatively spliced variants of human CD28 mRNA. Biochem. Biophys. Res. Commun. 259, 34-37 (1999).
35. Hanawa, H. et al. A novel costimulatory signalling in human T lymphocytes by a splice variant of CD28. Blood 99, 2138-2145 (2002).
36. Howard, T. et al. Fine mapping of an IgE-controlling gene on chromosome 2q: analysis of CTLA4 and CD28. J. Allegy Clin. Immunol. 110, 743-751 (2002).
37. Todd, J. A. A protective role of the environment in the development of type 1 diabetes? Diabetic Med. 8, 906-910 (1991).
38. Strachan, D. P. Hay fever, hygiene, and household size. Br. Med. J. 299, 1259-1260 (1989).
39. Bain, S. C., Todd, J. A. & Barnett, A. H. The British Diabetic Association - Warren Repository. Autoimmunity 7, 83-85 (1990).
40. Lernmark, A. et al. Family cell lines available for research. Am. J. Hum. Genet. 47, 1028-1030 (1990).
41. Patterson, C. C., Carson, D. J. & Hadden, D. R. Epidemiology of childhood IDDM in Northern Ireland 1989-1994: low incidence in areas with highest population density and most household crowding. Northern Ireland Diabetes Study Group. Diabetologia 39, 1063-1069 (1996).
42. Tuomilehto, J. et al. Epidemiology of childhood diabetes mellitus in Finland - background of a nationwide study of type 1 (insulin-dependent) diabetes mellitus. The Childhood Diabetes in Finland (DiMe) Study Group. Diabetologia 35, 70-76 (1992).
43. Mein, C. A. et al. Evaluation of single nucleotide polymorphism typing with invader on PCR amplicons and its automation. Genome Res. 10, 330-343 (2000).
44. Olivier, M. et al. High-throughput genotyping of single nucleotide polymorphisms using new biplex invader technology. Nucleic Acids Res. 30, e53 (2002).
45. Clayton, D. in Handbook of Statistical Genetics (eds Balding, D., Bishop, M. & Cannings, C.) 519-540 (Wiley, Chichester, 2001).
46. Spielman, R., McGinnis, R. & Ewens, W. Transmission test for linkage disequilibrium: the insulin gene region and insulin-dependent diabetes mellitus (IDDM). Am. J. Hum. Genet. 52, 506-516 (1993).