Confirmation of association of FCGR3B but not FCGR3A copy number with susceptibility to autoantibody positive rheumatoid arthritis

Human Mutation

Volumn 33, Issue 4, 2012, Pages 741-749

  Robinson, James I ^a   Carr, Ian M ^a   Cooper, Dawn L ^a   Rashid, Lubna H ^a   Martin, Stephen G ^a   Emery, Paul ^a   Isaacs, John D ^b   Barton, Anne ^c   Wilson, Anthony G ^d   Barrett, Jennifer H ^a,e   Morgan, Ann W ^a,e  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d Biologics in Rheumatoid Arthritis Genetics and Genomics Study Syndicate ^*  (United Kingdom)

^e UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

CD16; CNV; FCGR3A; FCGR3B; QSV; Rheumatoid arthritis

Indexed keywords

AUTOANTIBODY; FC RECEPTOR; FCGR3A PROTEIN; FCGR3B PROTEIN; UNCLASSIFIED DRUG;

ANTIGEN EXPRESSION; ARTICLE; CHROMOSOME 18; CONTROLLED STUDY; COPY NUMBER VARIATION; GENE DELETION; GENE FREQUENCY; GENE LOCUS; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; HUMAN; IMMUNOASSAY; IMMUNOPATHOGENESIS; MAJOR CLINICAL STUDY; NEUTROPHIL; NUCLEOTIDE REPEAT; POPULATION GENETICS; PRIORITY JOURNAL; QUALITY CONTROL; RHEUMATOID ARTHRITIS;

ARTHRITIS, RHEUMATOID; AUTOANTIBODIES; CASE-CONTROL STUDIES; EUROPEAN CONTINENTAL ANCESTRY GROUP; GENE DOSAGE; GENETIC PREDISPOSITION TO DISEASE; GENETICS, POPULATION; GPI-LINKED PROTEINS; HUMANS; MODELS, GENETIC; NEUTROPHILS; RECEPTORS, IGG; REPRODUCIBILITY OF RESULTS;

EID: 84858291311     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.22031     Document Type: Article

References (50)

1. Aitman TJ, Dong R, Vyse TJ, Norsworthy PJ, Johnson MD, Smith J, Mangion J, Roberton-Lowe C, Marshall AJ, Petretto E, Hodges MD, Bhangal G, Patel SG, Sheehan-Rooney K, Duda M, Cook PR, Evans DJ, Domin J, Flint J, Boyle JJ, Pusey CD, Cook HT. 2006. Copy number polymorphism in Fcgr3 predisposes to glomerulonephritis in rats and humans. Nature 439:851-855.
2. Aldred PM, Hollox EJ, Armour JA. 2005. Copy number polymorphism and expression level variation of the human alpha-defensin genes DEFA1 and DEFA3. Hum Mol Genet 14:2045-2052.
3. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS, Medsger TA, Mitchell DM, Neustadt DH, Pinals RS, Schaller JG, Sharp JT, Wilder RL, Hunder G. 1988. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31:315-324.
4. Bailey JA, Gu Z, Clark RA, Reinert K, Samonte RV, Schwartz S, Adams MD, Myers EW, Li PW, Eichler EE. 2002. Recent segmental duplications in the human genome. Science 297:1003-1007.
5. Barnes C, Plagnol V, Fitzgerald T, Redon R, Marchini J, Clayton D, Hurles ME. 2008. A robust statistical method for case-control association testing with copy number variation. Nat Genet 40:1245-1252.
6. Breunis WB, van ME, Bruin M, Geissler J, de BM, Peters M, Roos D, de HM, Koene HR, Kuijpers TW. 2008. Copy number variation of the activating FCGR2C gene predisposes to idiopathic thrombocytopenic purpura. Blood 111:1029-1038.
7. Breunis WB, van ME, Geissler J, Laddach N, Wolbink G, van der Schoot E, de HM, de BM, Roos D, Kuijpers TW, Breunis WB, van Mirre E, Geissler J, Laddach N, Wolbink G, van der Schoot E, de Haas M, de Boer M, Roos D, Kuijpers TW. 2009. Copy number variation at the FCGR locus includes FCGR3A, FCGR2C and FCGR3B but not FCGR2A and FCGR2B. Hum Mutat 30:E640-E650.
8. Carr IM, Robinson JI, Dimitriou R, Markham AF, Morgan AW, Bonthron DT. 2009. Inferring relative proportions of DNA variants from sequencing electropherograms. Bioinformatics 25:3244-3250.
9. Carter NP. 2007. Methods and strategies for analysing copy number variation using DNA microarrays. Nat Genet Suppl 39:S16-S21.
10. Chuang FY, Sassaroli M, Unkeless JC. 2000. Convergence of Fc gamma receptor IIA and Fc gamma receptor IIIB signaling pathways in human neutrophils. J Immunol 164:350-360.
11. Conrad DF, Pinto D, Redon R, Feuk L, Gokcumen O, Zhang Y, Aerts J, Andrews TD, Barnes C, Campbell P, Fitzgerald T, Hu M, Ihm CH, Kristiansson K, Macarthur DG, Macdonald JR, Onyiah I, Pang AW, Robson S, Stirrups K, Valsesia A, Walter K, Wei J, Tyler-Smith C, Carter NP, Lee C, Scherer SW, Hurles ME. 2010. Origins and functional impact of copy number variation in the human genome. Nature 464:704-712.
12. Cooke TD, Hurd ER, Jasin HE, Bienenstock J, Ziff M. 1975. Identification of immunoglobulins and complement in rheumatoid articular collagenous tissues. Arthritis Rheum 18:541-551.
13. de Haas M, Kleijer M, van Zwieten R, Roos D, von dem Borne AEGK. 1995. Neutrophil FcγRIIIb deficiency, nature, and clinical consequences: a study of 21 individuals from 14 families. Blood 86:2403-2413.
14. Ernst LK, Metes D, Herberman RB, Morel PA. 2002. Allelic polymorphisms in the FcgammaRIIC gene can influence its function on normal human natural killer cells. J Mol Med 80:248-257.
15. Estivill X, Cheung J, Pujana MA, Nakabayashi K, Scherer SW, Tsui LC. 2002. Chromosomal regions containing high-density and ambiguously mapped putative single nucleotide polymorphisms (SNPs) correlate with segmental duplications in the human genome. Hum Mol Genet 11:1987-1995.
16. Fanciulli M, Norsworthy PJ, Petretto E, Dong R, Harper L, Kamesh L, Heward JM, Gough SCL, de Smith A, Blakemore AIF, Froguel P, Owen CJ, Pearce SHS, Teixeira L, Guillevin L, Graham DSC, Pusey CD, Cook HT, Vyse TJ, Aitman TJ. 2007. FCGR3B copy number variation is associated with susceptibility to systemic, but not organ-specific, autoimmunity. Nat Genet 39:721-723.
17. Hollox EJ, Detering JC, Dehnugara T. 2009. An integrated approach for measuring copy number variation at the FCGR3 (CD16) locus. Hum Mutat 30:477-484.
18. Koene HR, de HM, Kleijer M, Roos D, von dem Borne AE, Koene HR, de Haas M, Kleijer M, Roos D, von dem Borne AE. 1996. NA-phenotype-dependent differences in neutrophil Fc gamma RIIIb expression cause differences in plasma levels of soluble Fc gamma RIII. Br J Haematol 93:235-241.
19. Mamtani M, Anaya JM, He W, Ahuja SK. 2010. Association of copy number variation in the FCGR3B gene with risk of autoimmune diseases. Genes Immun 11:155-160.
20. McCarroll SA, Hadnott TN, Perry GH, Sabeti PC, Zody MC, Barrett JC, Dallaire S, Gabriel SB, Lee C, Daly MJ, Altshuler DM, International HapMap Consortium 2006. Common deletion polymorphisms in the human genome. Nat Genet 38:86-92.
21. McCarroll SA, Kuruvilla FG, Korn JM, Cawley S, Nemesh J, Wysoker A, Shapero MH, de Bakker PIW, Maller JB, Kirby A, Elliott AL, Parkin M, Hubbell E, Webster T, Mei R, Veitch J, Collins PJ, Handsaker R, Lincoln S, Nizzari M, Blume J, Jones KW, Rava R, Daly MJ, Gabriel SB, Altshuler D. 2008. Integrated detection and population-genetic analysis of SNPs and copy number variation. Nat Genet 40:1166-1174.
22. McKinney C, Fanciulli M, Merriman ME, Phipps-Green A, Alizadeh BZ, Koeleman BP, Dalbeth N, Gow PJ, Harrison AA, Highton J, Jones PB, Stamp LK, Steer S, Barrera P, Coenen MJ, Franke B, van Riel PL, Vyse TJ, Aitman TJ, Radstake TR, Merriman TR. 2010. Association of variation in Fc gamma receptor 3B gene copy number with rheumatoid arthritis in Caucasian samples. Ann Rheum Dis 69:1711-1716.
23. Mewar D, Coote A, Moore D, Marinou I, Keyworth J, Dickson M, Montgomery D, Binks M, Wilson A. 2006. Independent associations of anti-cyclic citrullinated peptide antibodies and rheumatoid factor with radiographic severity of rheumatoid arthritis. Arthritis Res Ther 8:R128.
24. Morgan AW, Barrett JH, Griffiths B, Subramanian D, Robinson JI, Keyte VH, Ali M, Jones EA, Old RW, Ponchel F, Boylston AW, Situnayake RD, Markham AF, Emery P, Isaacs JD. 2006. Analysis of Fcγ receptor haplotypes in rheumatoid arthritis. FCGR3A remains a major susceptibility gene at this locus with an additional contribution from FCGR3B. Arthritis Res Ther 8:R5.
25. Morgan AW, Thompson W, Martin SG, YEAR consortium, Carter AM, UKRAG Consortium, Erlich HA, Barton A, Hocking L, Reid DM, Harrison P, Wordsworth BP, Steer S, Worthington J, Emery P, Wilson AG, Barrett JH. 2009. Re-evaluation of the interaction between HLA-DRB1 SE alleles, PTPN22 and smoking in determining the susceptibility to autoantibody positive and negative rheumatoid arthritis in a large UK Caucasian population. Arthritis Rheum 60:2565-2576.
26. Morris DL, Roberts AL, Witherden AS, Tarzi R, Barros P, Whittaker JC, Cook TH, Aitman TJ, Vyse TJ. 2010. Evidence for both copy number and allelic (NA1/NA2) risk at the FCGR3B locus in systemic lupus erythematosus. Eur J Hum Genet 18:1027-1031.
27. Niederer HA, Willcocks LC, Rayner TF, Yang W, Lau YL, Williams TN, Scott JA, Urban BC, Peshu N, Dunstan SJ, Hien TT, Phu NH, Padyukov L, Gunnarsson I, Svenungsson E, Savage CO, Watts RA, Lyons PA, Clayton DG, Smith KG. 2010. Copy number, linkage disequilibrium and disease association in the FCGR locus. Hum Mol Genet 19:3282-3294.
28. Parsian AJ, Sheren JE, Tao TY, Goswami PC, Malyapa R, Van Rheeden R, Watson MS, Hunt CR. 2000. The human Hsp70B gene at the HSPA7 locus of chromosome 1 is transcribed, but non-functional. Biochim Biophys Acta 1494:201-205.
29. Poo H, Krauss JC, Mayo-Bond L, Todd RF 3rd, Petty HR. 1995. Interaction of Fc gamma receptor type IIIB with complement receptor type 3 in fibroblast transfectants: evidence from lateral diffusion and resonance energy transfer studies. J Mol Biol 247:597-603.
30. Ravetch JV, Perussia B. 1989. Alternative membrane forms of FcγRIII(CD16) on human natural killer cells and neutrophils. Cell type-specific expression of two genes that differ in single nucleotide substitutions. J Exp Med 170:481-497.
31. Raychaudhuri S, Thomson BP, Remmers EF, Eyre S, Hinks A, Guiducci C, Catanese JJ, Xie G, Stahl EA, Chen R, Alfredsson L, Amos CI, Ardlie KG, BIRAC Consortium, Barton A, Bowes J, Burtt NP, Chang M, Coblyn J, Costenbader KH, Criswell LA, Crusius JB, Cui J, De Jager PL, Ding B, Emery P, Flynn E, Harrison P, Hocking LJ, Huizinga TW, Kastner DL, Ke X, Kurreeman FA, Lee AT, Liu X, Li Y, Martin P, Morgan AW, Padyukov L, Reid DM, Seielstad M, Seldin MF, Shadick NA, Steer S, Tak PP, Thomson W, van der Helm-van Mil AH, van der Horst-Bruinsma IE, Weinblatt ME, Wilson AG, Wolbink GJ, Wordsworth P, YEAR consortium, Altshuler D, Karlson EW, Toes RE, de VN, Begovich AB, Siminovitch KA, Worthington J, Klareskog L, Gregersen PK, Daly MJ, Plenge RM, Raychaudhuri S, Thomson BP, Remmers EF, Eyre S, Hinks A, Guiducci C, Catanese JJ, Xie G, Stahl EA, Chen R, Alfredsson L, Amos CI, Ardlie KG, BIRAC Consortium, Barton A, Bowes J, Burtt NP, Chang M, Coblyn J, Costenbader KH, Criswell LA, Crusius JB, Cui J, De Jager PL, Ding B, Emery P, Flynn E, Harrison P, Hocking LJ, Huizinga TWJ, Kastner DL, Ke X, Kurreeman FAS, Lee AT, Liu X, Li Y, Martin P, Morgan AW, Padyukov L, Reid DM, Seielstad M, Seldin MF, Shadick NA, Steer S, Tak PP, Thomson W, van der Helm-van Mil A, van der Horst-Bruinsma I, Weinblatt ME, Wilson AG, Wolbink GJ, Wordsworth P, YEAR consortium, Altshuler D, Karlson EW, Toes REM, de Vries N, Begovich AB, Siminovitch KA, Worthington J, Klareskog L, Gregersen PK, Daly MJ, Plenge RM. 2009. Genetic variants at CD28, PRDM1 and CD2/CD58 are associated with rheumatoid arthritis risk. Nat Genet 41:1313-1318.
32. Raza K, Scheel-Toellner D, Lee CY, Pilling D, Curnow SJ, Falciani F, Trevino V, Kumar K, Assi LK, Lord JM, Gordon C, Buckley CD, Salmon M. 2006. Synovial fluid leukocyte apoptosis is inhibited in patients with very early rheumatoid arthritis. Arthritis Res Ther 8:R120.
33. Redon R, Ishikawa S, Fitch KR, Feuk L, Perry GH, Andrews TD, Fiegler H, Shapero MH, Carson AR, Chen W, Cho EK, Dallaire S, Freeman JL, González JR, Gratacòs M, Huang J, Kalaitzopoulos D, Komura D, MacDonald JR, Marshall CR, Mei R, Montgomery L, Nishimura K, Okamura K, Shen F, Somerville MJ, Tchinda J, Valsesia A, Woodwark C, Yang F, Zhang J, Zerjal T, Zhang J, Armengol L, Conrad DF, Estivill X, Tyler-Smith C, Carter NP, Aburatani H, Lee C, Jones KW, Scherer SW, Hurles ME. 2006. Global variation in copy number in the human genome. Nature 444:444-454.
34. Robinson JI, Barrett JH, Taylor JC, Naven M, Corscadden D, Barton A, Wilson AG, Emery P, Isaacs JD, Morgan AW. 2009. Dissection of the FCGR3A association with RA: increased association in men and with autoantibody positive disease. Ann Rheum Dis 69:1054-1057.
35. Salmon JE, Edberg JC, Kimberly RP. 1990. Fc gamma receptor III on human neutrophils. Allelic variants have functionally distinct capacities. J Clin Invest 85:1287-1295.
36. Selvaraj P, Fifadara N, Nagarajan S, Cimino A, Wang G. 2004. Functional regulation of human neutrophil Fc gamma receptors. Immunol Res 29:219-230.
37. Stahl EA, Raychaudhuri S, Remmers EF, Xie G, Eyre S, Thomson BP, Li Y, Kurreeman FA, Zhernakova A, Hinks A, Guiducci C, Chen R, Alfredsson L, Amos CI, Ardlie KG, Barton A, Bowes J, Brouwer E, Burtt NP, Catanese JJ, Coblyn J, Coenen MJ, Costenbader KH, Criswell LA, Crusius JB, Cui J, de Bakker PI, De Jager PL, Ding B, Emery P, Flynn E, Harrison P, Hocking LJ, Huizinga TW, Kastner DL, Ke X, Lee AT, Liu X, Martin P, Morgan AW, Padyukov L, Posthumus MD, Radstake TR, Reid DM, Seielstad M, Seldin MF, Shadick NA, Steer S, Tak PP, Thomson W, van der Helm-van Mil AH, van der Horst-Bruinsma IE, van der Schoot CE, van Riel PL, Weinblatt ME, Wilson AG, Wolbink GJ, Wordsworth BP, Wijmenga C, Karlson EW, Toes RE, de VN, Begovich AB, Worthington J, Siminovitch KA, Gregersen PK, Klareskog L, Plenge RM. 2010. Genome-wide association study meta-analysis identifies seven new rheumatoid arthritis risk loci. Nat Genet 42:508-514.
38. Stranger BE, Forrest MS, Dunning M, Ingle CE, Beazley C, Thorne N, Redon R, Bird CP, de GA, Lee C, Tyler-Smith C, Carter N, Scherer SW, Tavare S, Deloukas P, Hurles ME, Dermitzakis ET. 2007. Relative impact of nucleotide and copy number variation on gene expression phenotypes. Science 315:848-853.
39. Symmons D, Turner G, Webb R, Asten P, Barrett E, Lunt M, Scott D, Silman A. 2002. The prevalence of rheumatoid arthritis in the United Kingdom: new estimates for a new century. Rheumatology 41:793-800.
40. Thabet MM, Huizinga TW, Marques RB, Stoeken-Rijsbergen G, Bakker AM, Kurreeman FA, White SJ, Toes RE, van der Helm-van Mil AH. 2009. Contribution of Fcgamma receptor IIIA gene 158V/F polymorphism and copy number variation to the risk of ACPA-positive rheumatoid arthritis. Ann Rheum Dis 68:1775-1780.
41. The Wellcome Trust Case Control Consortium. 2007. Genome-wide association study of 14, 000 cases of seven common diseases and 3, 000 shared controls. Nature 447:661-678.
42. The Wellcome Trust Case Control Consortium. 2010. Genome-wide association study of CNVs in 16, 000 cases of eight common diseases and 3, 000 shared controls. Nature 464:713-720.
43. Tsuboi N, Asano K, Lauterbach M, Mayadas TN. 2008. Human neutrophil Fc[gamma] receptors initiate and play specialized nonredundant roles in antibody-mediated inflammatory diseases. Immunity 28:833-846.
44. Tuzun E, Sharp AJ, Bailey JA, Kaul R, Morrison VA, Pertz LM, Haugen E, Hayden H, Albertson D, Pinkel D, Olson MV, Eichler EE. 2005. Fine-scale structural variation of the human genome. Nat Genet 37:727-732.
45. Vetto AA, Mannik M, Zatarain-Rios E, Wener MH. 1990. Immune deposits in articular cartilage of patients with rheumatoid arthritis have a granular pattern not seen in osteoarthritis. Rheumatol Int 10:13-19.
46. Wagner C, Hansch GM. 2004. Genetic deficiency of CD16, the low-affinity receptor for immunoglobulin G, has no impact on the functional capacity of polymorphonuclear neutrophils. Eur J Clin Invest 34:149-155.
47. Willcocks LC, Lyons PA, Clatworthy MR, Robinson JI, Yang W, Newland SA, Plagnol V, McGovern N, Condliffe A, Chilvers ER, Adu D, Jolly EC, Watts R, Lau YL, Morgan AW, Nash G, Smith KGC. 2008. Copy number of FCGR3B, which is associated with systemic lupus erythematosus, correlates with protein expression and immune complex uptake. J Exp Med 205:1573-1582.
48. Wright HL, Moots RJ, Bucknall RC, Edwards SW. 2010. Neutrophil function in inflammation and inflammatory diseases. Rheumatology (Oxford) 49:1618-1631
49. Yang H, Zhou Q, Chen Dj, Jiang H, Mao Y, Chen J. 2010. The single nucleotide polymorphisms gene but not the copy number variation of Fcgr3B is associated with lupus nephritis in Chinese people. Lupus 19:662-664.
50. Zhou XJ, Lv JC, Bu DF, Yu L, Yang YR, Zhao J, Cui Z, Yang R, Zhao MH, Zhang H. 2009. Copy number variation of FCGR3A rather than FCGR3B and FCGR2B is associated with susceptibility to anti-GBM disease. Int Immunol 22:4.