Association analysis of functional variants of the FcgRIIa and FcgRIIIa genes with type 1 diabetes, celiac disease and rheumatoid arthritis

Human Molecular Genetics

Volumn 16, Issue 21, 2007, Pages 2552-2559

  Alizadeh, Behrooz Z ^a,b   Valdigem, Gustavo ^a   Coenen, Marieke J H ^c   Zhernakova, Alexandra ^a   Franke, Barbara ^c   Monsuur, Alienke ^a   Van riel, Piet L C M ^c   Barrera, Pilar ^c   Radstake, Timothy R D J ^c   Roep, Bart O ^b   Wijmenga, Cisca ^a,d   Koeleman, Bobby P C ^a,b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; FC RECEPTOR; FC RECEPTOR IIA; FC RECEPTOR IIIA; GUANINE; UNCLASSIFIED DRUG;

ADOLESCENT; ARTICLE; AUTOIMMUNE DISEASE; CELIAC DISEASE; COHORT ANALYSIS; CONTROLLED STUDY; GENE FREQUENCY; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENETIC RISK; GENETIC VARIABILITY; GENOTYPE; HUMAN; INFANT; INSULIN DEPENDENT DIABETES MELLITUS; MAJOR CLINICAL STUDY; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN FUNCTION; RHEUMATOID ARTHRITIS; RISK ASSESSMENT; RISK FACTOR; SCHOOL CHILD;

ADOLESCENT; ARTHRITIS, RHEUMATOID; CELIAC DISEASE; CHILD; CHILD, PRESCHOOL; COHORT STUDIES; DIABETES MELLITUS, TYPE 1; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HUMANS; INFANT; LINKAGE DISEQUILIBRIUM; MALE; RECEPTORS, IGG;

EID: 35448941585     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddm194     Document Type: Article

References (66)

1. Karassa, F.B., Trikalinos, T.A. and Ioannidis, J.P. (2004) The role of FcgammaRIIA and IIIA polymprphisms in autoimmune diseases. Biomed. Pharmacother., 58, 286-291.
2. Dijstelbloem, H.M., van de Winkel, J.G. and Kallenberg, C.G. (2001) Inflammation in autoimmunity: Receptors for IgG revisited. Trends Immunol., 22, 510-516.
3. Takai, T. (2005) Fc receptors and their role in immune regulation and autoimmunity. J. Clin. Immunol., 25, 1-18.
4. Karassa, F.B., Bijl, M., Davies, K.A., Kallenberg, C.G., Khamashta, M.A., Manger, K., Michel, M., Piette, J.C., Salmon, J.E., Song, Y.W. et al. (2003) Role of the Fcgamma receptor IIA polymorphism in the antiphospholipid syndrome: An international meta-analysis. Arthritis Rheum., 48, 1930-1938.
5. Nakamura, A., Akiyama, K. and Takai, T. (2005) Fc receptor targeting in the treatment of allergy, autoimmune diseases and cancer. Expert Opin. Ther. Targets, 9, 169-190.
6. Bredius, R.G., Fijen, C.A., De Haas, M., Kuijper, E.J., Weening, R.S., Van de Winkel, J.G. and Out, T.A. (1994) Role of neutrophil Fc gamma RIIa (CD32) and Fc gamma RIIIb (CD16) polymorphic forms in phagocytosis of human IgG1- and IgG3-opsonized bacteria and erythrocytes. Immunology, 83, 624-630.
7. Corper, A.L., Sohi, M.K., Bonagura, V.R., Steinitz, M., Jefferis, R., Feinstein, A., Beale, D., Taussig, M.J. and Sutton, B.J. (1997) Structure of human IgM rheumatoid factor Fab bound to its autoantigen IgG Fc reveals a novel topology of antibody-antigen interaction. Nat. Struct. Biol., 4, 374-381.
8. Salmon, J.E., Edberg, J.C., Brogle, N.L. and Kimberly, R.P. (1992) Allelic polymorphisms of human Fc gamma receptor IIA and Fc gamma receptor IIIB. Independent mechanisms for differences in human phagocyte function. J. Clin. Invest., 89, 1274-1281.
9. Bredius, R.G., Derkx, B.H., Fijen, C.A., de Wit, T.P., de Haas, M., Weening, R.S., van de Winkel, J.G. and Out, T.A. (1994) Fc gamma receptor IIa (CD32) polymorphism in fulminant meningococcal septic shock in children. J. Infect. Dis., 170, 848-853.
10. Salmon, J.E., Edberg, J.C. and Kimberly, R.P. (1990) Fc gamma receptor III on human neutrophils. Allelic variants have functionally distinct capacities. J Clin. Invest., 85, 1287-1295.
11. Wu, J., Edberg, J.C., Redecha, P.B., Bansal, V., Guyre, P.M., Coleman, K., Salmon, J.E. and Kimberly, R.P. (1997) A novel polymorphism of FcgammaRIIIa (CD16) alters receptor function and predisposes to autoimmune disease. J. Clin. Invest., 100, 1059-1070.
12. Lee, Y.H. and Nath, S.K. (2005) Systemic lupus erythematosus susceptibility loci defined by genome scan meta-analysis. Hum. Genet. 118, 434-443.
13. Forabosco, P., Gorman, J.D., Cleveland, C., Kelly, J.A., Fisher, S.A., Ortmann, W.A., Johansson, C., Johanneson, B., Moser, K.L., Gaffney, P.M. et al. (2006) Meta-analysis of genome-wide linkage studies of systemic lupus erythematosus. Genes Immun., 7, 609-614.
14. Choi, S.J., Rho, Y.H., Ji, J.D., Song, G.G. and Lee, Y.H. (2006) Genome scan meta-analysis of rheumatoid arthritis. Rheumatology, 45 166-170.
15. Karassa, F.B., Trikalinos, T.A. and Ioannidis, J.P. (2002) Role of the Fcgamma receptor IIa polymorphism in susceptibility to systemic lupus erythematosus and lupus nephritis: A meta-analysis. Arthritis Rheum. 46, 1563-1571.
16. Karassa, F.B., Trikalinos, T.A. and Ioannidis, J.P. (2003) The Fc gamma RIIIA-F158 allele is a risk factor for the development of lupus nephritis: A meta-analysis. Kidney Int., 63, 1475-1482.
17. Zuniga, R., Ng, S., Peterson, M.G., Reveille, J.D., Baethge, B.A., Alarcon, G.S. and Salmon, J.E. (2001) Low-binding alleles of Fcgamma receptor types IIA and IIIA are inherited independently and are associated with systemic lupus erythematosus in Hispanic patients. Arthritis Rheum., 44, 361-367.
18. Dijstelbloem, H.M., Scheepers, R.H., Oost, W.W., Stegeman, C.A., van der Pol, W.L., Sluiter, W.J., Kallenberg, C.G., van de Winkel, J.G. and Tervaert, J.W. (1999) Fcgamma receptor polymorphisms in Wegener's granulomatosis: Risk factors for disease relapse. Arthritis Rheum. 42, 1823-1827.
19. Salmon, J.E., Ng, S., Yoo, D.H., Kim, T.H., Kim, S.Y. and Song, G.G. (1999) Altered distribution of Fcgamma receptor IIIA alleles in a cohort of Korean patients with lupus nephritis. Arthritis Rheum., 42 818-819.
20. Trikalinos, T.A., Karassa, F.B. and Ioannidis, J.P. (2001) Meta-analysis of the association between low-affinity Fcgamma receptor gene polymorphisms and hematologic and autoimmune disease. Blood, 98 1634-1635.
21. Lehrnbecher, T., Foster, C.B., Zhu, S., Leitman, S.F., Goldin, L.R., Huppi, K. and Chanock, S.J. (1999) Variant genotypes of the low-affinity Fcgamma receptors in two control populations and a review of low-affinity Fcgamma receptor polymorphisms in control and disease populations. Blood, 94, 4220-4232.
22. Kyogoku, C., Tsuchiya, N., Matsuta, K. and Tokunaga, K. (2002) Studies on the association of Fc gamma receptor IIA, IIB, IIIA and IIIB polymorphisms with rheumatoid arthritis in the Japanese: Evidence for a genetic interaction between HLA-DRB1 and FCGR3A. Genes Immun., 3, 488-493.
23. Kyogoku, C., Dijstelbloem, H.M., Tsuchiya, N., Hatta, Y., Kato, H., Yamaguchi, A., Fukazawa, T., Jansen, M.D., Hashimoto, H., van de Winkel, J.G. et al. (2002) Fcgamma receptor gene polymorphisms in Japanese patients with systemic lupus erythematosus: Contribution of FCGR2B to genetic susceptibility. Arthritis Rheum., 46, 1242-1254.
24. van der Pol, W.L., van den Berg, L.H., Scheepers, R.H., van der Bom, J.G., van Doorn, P.A., van Koningsveld, R., van den Broek, M.C., Wokke, J.H. and van de Winkel, J.G. (2000) IgG receptor IIa alleles determine susceptibility and severity of Guillain-Barre syndrome. Neurology, 54, 1661-1665.
25. Kastbom, A., Ahmadi, A., Soderkvist, P. and Skogh, T. (2005) The 158V polymorphism of Fc gamma receptor type IIIA in early rheumatoid arthritis: Increased susceptibility and severity in male patients (the Swedish TIRA project). Rheumatology (Oxford), 44, 1294-1298.
26. Morgan, A.W., Griffiths, B., Ponchel, F., Montague, B.M., Ali, M., Gardner, P.P., Gooi, H.C., Situnayake, R.D., Markham, A.F., Emery, P. et al. (2000) Fcgamma receptor type IIIA is associated with rheumatoid arthritis in two distinct ethnic groups. Arthritis Rheum. 43, 2328-2334.
27. Milicic, A., Misra, R., Agrawal, S., Aggarwal, A., Brown, M.A. and Wordsworth, B.P. (2002) The F158V polymorphism in FcgammaRIIIA shows disparate associations with rheumatoid arthritis in two genetically distinct populations. Ann. Rheum. Dis., 61, 1021-1023.
28. Chu, Z.T., Tsuchiya, N., Kyogoku, C., Ohashi, J., Qian, Y.P., Xu, S.B., Mao, C.Z., Chu, J.Y. and Tokunaga, K. (2004) Association of Fcgamma receptor IIb polymorphism with susceptibility to systemic lupus erythematosus in Chinese: A common susceptibility gene in the Asian populations. Tissue Antigens, 63, 21-27.
29. Siriboonrit, U., Tsuchiya, N., Sirikong, M., Kyogoku, C., Bejrachandra, S., Suthipinittharm, P., Luangtrakool, K., Srinak, D., Thongpradit, R., Fujiwara, K. et al. (2003) Association of Fcgamma receptor IIb and IIIb polymorphisms with susceptibility to systemic lupus erythematosus in Thais. Tissue Antigens, 61, 374-383.
30. Matsumoto, I., Zhang, H., Muraki, Y., Hayashi, T., Yasukochi, T., Kori, Y., Goto, D., Ito, S., Tsutsumi, A. and Sumida, T. (2005) A functional variant of Fcgamma receptor IIIA is associated with rheumatoid arthritis in individuals who are positive for anti-glucose-6-phosphate isomerase antibodies. Arthritis Res. Ther., 7, 1183-1188.
31. Morgan, A.W., Barrett, J.H., Griffiths, B., Subramanian, D., Robinson, J.I., Keyte, V.H., Ali, M., Jones, E.A., Old, R.W., Ponchel, F. et al. (2006) Analysis of Fcgamma receptor haplotypes in rheumatoid arthritis: FCGR3A remains a major susceptibility gene at this locus, with an additional contribution from FCGR3B. Arthritis Res. Ther., 8, 5.
32. Breij, E.C., van der Pol, W.L., van Winsen, L., Jansen, M.D., Dijkstra, C.D., van de Winkel, J.G. and Uitdehaag, B.M. (2003) No association of Fc gamma RIIa, Fc gamma RIIIa and Fc gamma RIIIb polymorphisms with MS. J. Neuroimmunol., 140, 210-215.
33. Eisenbarth, G.S. (1986) Tyne I diabetes mellitus. A chronic autoimmune disease. N. Engl. J. Med., 314, 1360-1368.
34. Atkinson, M.A. and Eisenbarth, G.S. (2001) Type 1 diabetes: New perspectives on disease pathogenesis and treatment. Lancet, 358 221-229.
35. Narendran, P., Williams, A.J., Elsegood, K., Leech, N.J. and Dayan, C.M. (2003) Humoral and cellular immune responses to proinsulin in adults with newly diagnosed type 1 diabetes. Diabetes Metab. Res. Rev., 19, 52-59.
36. Colman, P.G., McNair, P.D., Gellert, S., Kewming, K., Schmidli, R.S., Steele, C.E. and Harrison, L.C. (2002) Development of autoantibodies to islet antigens during childhood: Implications for preclinical type 1 diabetes screening. Pediatr. Diabetes, 3, 144-148.
37. Monsuur, A.J. and Wijmenga, C. (2006) Understanding the molecular basis of celiac disease: What genetic studies reveal? Ann. Med., 38 578-591.
38. Magnusson, V., Johanneson, B., Lima, G., Odeberg, J., Alarcon-Segovia, D. and Alarcon-Riquelme, M.E. (2004) Both risk alleles for FcgammaRIIA and FcgammaRIIIA are susceptibility factors for SLE: A unifying hypothesis. Genes Immun., 5, 130-137.
39. Chatenoud, L. (2003) CD3 antibody treatment stimulates the functional capability of regulatory T cells. Novartis Found. Symp., 252 279-290.
40. Keymeulen, B., Vandemeulebroucke, E., Ziegler, A.G., Mathieu, C., Kaufman, L., Hale, G., Gorus, F., Goldman, M., Walter, M., Candon, S. et al. (2005) Insulin needs after CD3-antibody therapy in new-onset type 1 diabetes. N. Engl. J. Med., 352, 2598-2608.
41. Brand, O., Gough, S. and Heward, J. (2005) HLA, CTLA-4 and PTPN22: The shared genetic master-key to autoimmunity? Expert Rev. Mol. Med., 7, 1-15.
42. Morgan, A.W., Keyte, V.H., Babbage, S.J., Robinson, J.I., Ponchel, F., Barrett, J.H., Bhakta, B.B., Bingham, S.J., Buch, M.H., Conaghan, P.G. et al. (2003) FcgammaRIIIA-158V and rheumatoid arthritis: A confirmation study. Rheumatology (Oxford), 42, 528-533.
43. Chen, J.Y., Wang, C.M., Wu, J.M., Ho, H.H. and Luo, S.F. (2006) Association of rheumatoid factor production with FcgammaRIIIa polymorphism in Taiwanese rheumatoid arthritis. Clin. Exp. Immunol. 144, 10-16.
44. Radstake, T.R., Petit, E., Pierlot, C., van de Putte, L.B., Cornelis, F. and Barrera, P. (2003) Role of Fcgamma receptors IIA, IIIA, and IIIB in susceptibility to rheumatoid arthritis. J. Rheumatol., 30, 926-933.
45. Nieto, A., Caliz, R., Pascual, M., Mataran, L., Garcia, S. and Martin, J. (2000) Involvement of Fcgamma receptor IIIA genotypes in susceptibility to rheumatoid arthritis. Arthritis Rheum., 43 735-739.
46. Suzuki, T., Muraki, Y., Yasukochi, T., Zhang, H., Kori, Y., Wakamatsu, E., Hayashi, T., Goto, D., Ito, S., Tsutsumi, A. et al. (2005) Immunoglobulin G from anti-glucose-6-phosphate isomerase antibodies positive patient with rheumatoid arthritis induces synovitis in cynomolgus monkeys. Autoimmun. Rev., 4, 475-478.
47. Edberg, J.C., Langefeld, C.D., Wu, J., Moser, K.L., Kaufman, K.M., Kelly, J., Bansal, V., Brown, W.M., Salmon, J.E., Rich, S.S. et al. (2002) Genetic linkage and association of Fcgamma receptor IIIA (CD16A) on chromosome 1q23 with human systemic lupus erythematosus. Arthritis Rheum., 46, 2132-2140.
48. Aitman, T.J., Dong, R., Vyse, T.J., Norsworthy, P.J., Johnson, M.D., Smith, J., Mangion, J., Roberton-Lowe, C., Marshall, A.J., Petretto, E. et al. (2006) Copy number polymorphism in Fcgr3 predisposes to glomerulonephritis in rats and humans. Nature, 439, 851-855.
49. Fanciulli, M., Norsworthy, P.J., Petretto, E., Dong, R., Harper, L., Kamesh, L., Reward, J.M., Gough, S.C., de Smith, A., Blakemore, A.I. et al. (2007) FCGR3B copy number variation is associated with susceptibility to systemic, but not organ-specific, autoimmunity. Nat. Genet., 39, 721-723.
50. Herold, K.C., Hagopian, W., Auger, J.A., Poumian-Ruiz, E., Taylor, L., Donaldson, D., Gitelman, S.E., Harlan, D.M., Xu, D., Zivin, R.A. et al. (2002) Anti-CD3 monoclonal antibody in new-onset type 1 diabetes mellitus. N. Engl. J. Med., 346, 1692-1698.
51. Herold, K.C., Gitelman, S.E., Masharani, U., Hagopian, W., Bisikirska, B., Donaldson, D., Rother, K., Diamond, B., Harlan, D.M. and Bluestone, J.A. (2005) A single course of anti-CD3 monoclonal antibody hOKT3gamma1(Ala-Ala) results in improvement in C-peptide responses and clinical parameters for at least 2 years after onset of type 1 diabetes. Diabetes, 54, 1763-1769.
52. Routledge, E.G., Falconer, M.E., Pope, H., Lloyd, I.S. and Waldmann, H. (1995) The effect of aglycosylation on the immunogenicity of a humanized therapeutic CD3 monoclonal antibody. Transplantation, 60, 847-853.
53. Alegre, M.L., Tso, J.Y., Sattar, H.A., Smith, J., Desalle, F., Cole, M. and Bluestone, J.A. (1995) An anti-murine CD3 monoclonal antibody with a low affinity for Fc gamma receptors suppresses transplantation responses while minimizing acute toxicity and immunogenicity. J. Immunol., 155, 1544-1555.
54. Tax, W.J., Frenken, L.A., Glaudemans, C.A., Tamboer, W.P. and Koene, R.A. (1995) Polymorphism of Fc receptor (Fc gamma RII) is reflected in cytokine release and adverse effects of mIgG1 anti-CD3/TCR antibody during rejection treatment after renal transplantation. Transplant. Proc., 27, 867-868.
55. Lin, T.S., Flinn, I.W., Modali, R., Lehman, T.A., Webb, J., Waymer, S., Moran, M.E., Lucas, M.S., Farag, S.S. and Byrd, J.C. (2005) FCGR3A and FCGR2A polymorphisms may not correlate with response to alemtuzumab in chronic lymphocytic leukemia. Blood, 105, 289-291.
56. Farag, S.S., Flinn, I.W., Modali, R., Lehman, T.A., Young, D. and Byrd, J.C. (2004) Fc gamma RIIIa and Fc gamma RIIa polymorphisms do not predict response to rituximab in B-cell chronic lymphocytic leukemia. Blood, 103, 1472-1474.
57. Anolik, J.H., Campbell, D., Felgar, R.E., Young, F., Sanz, I., Rosenblatt, J. and Looney, R.J. (2003) The relationship of FcgammaRIIIa genotype to degree of B cell depletion by rituximab in the treatment of systemic lupus erythematosus. Arthritis Rheum., 48, 455-459.
58. The United European Gastroenterology (2001) When is a coeliac a coeliac? Report of a working group of the United European Gastroenterology Week in Amsterdam, 2001. Eur. J. Gastroenterol. Hepatol., 13, 1123-1128.
59. Welsing, P.M. and van Riel, P.L. (2004) The Nijmegen inception cohort of early rheumatoid arthritis. J. Rheumatol., 69, 14-21.
60. Arnett, F.C., Edworthy, S.M., Bloch, D.A., McShane, D.J., Fries, J.F., Cooper, N.S., Healey, L.A., Kaplan, S.R., Liang, M.H., Luthra, H.S. et al. (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum., 31, 315-324.
61. Hughes, L.B., Criswell, L.A., Beasley, T.M., Edberg, J.C., Kimberly, R.P., Moreland, L.W., Seldin, M.F. and Bridges, S.L. (2004) Genetic risk factors for infection in patients with early rheumatoid arthritis. Genes Immun., 5, 641-647.
62. Brun, J.G., Madland, T.M. and Vedeler, C.A. (2002) Immunoglobulin G fc-receptor (FcgammaR) IIA, IIIA, and IIIB polymorphisms related to disease severity in rheumatoid arthritis. J. Rheumatol., 29, 1135-1140.
63. Stewart-Akers, A.M., Cunningham, A., Wasko, M.C. and Morel, P.A. (2004) Fc gamma R expression on NK cells influences disease severity in rheumatoid arthritis. Genes Immun., 5, 521-529.
64. Chiano, M.N. and Clayton, D.G. (1998) Fine genetic mapping using haplotype analysis and the missing data problem. Ann. Hum. Genet., 62, 55-60.
65. Dudbridge, F. (2003) Pedigree disequilibrium tests for multilocus haplotypes. Genet. Epidemiol., 25, 115-121.
66. Cordell, H.J. and Clayton, D.G. (2002) 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.