Different gender-associated genotype risks of Wegener's granulomatosis and microscopic polyangiitis

Clinical Immunology

Volumn 109, Issue 3, 2003, Pages 330-337

  Bártfai, Zoltán ^a,b   Gaede, Karoline I ^a   Russell, Kimberly A ^c   Muraközy, Gabriella ^a,b   Müller Quernheim, Joachim ^a   Specks, Ulrich ^c  

^a RESEARCH CENTER BORSTEL   (Germany)

^b SEMMELWEIS UNIVERSITY   (Hungary)

^c MAYO CLINIC   (United States)

Author keywords

ANCA; Gender risk; Gene polymorphism; Interleukin 10; Microscopic polyangiitis; Systemic vasculitis; Wegener's granulomatosis

Indexed keywords

CYTOKINE; INTERLEUKIN 10; TRANSFORMING GROWTH FACTOR BETA1;

ADULT; ALLELE; ARTICLE; BLOOD SAMPLING; CLINICAL FEATURE; CODON; CONTROLLED STUDY; FEMALE; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENETIC RISK; GENETIC SUSCEPTIBILITY; GENOTYPE; HEALTH STATUS; HOMOZYGOSITY; HUMAN; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; SEX DIFFERENCE; STATISTICAL SIGNIFICANCE; VASCULITIS; WEGENER GRANULOMATOSIS;

EID: 0347755085     PISSN: 15216616     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1521-6616(03)00211-0     Document Type: Article

References (69)

1. Jennette J.C., Falk R.J., Andrassy K., Bacon B.A., Churg J., Gross W.L., Hagen E.C., Hoffmann G.S., Hunder G.G., Kallenberg C.G.M., McCluskey R.T., Sinico R.A., Rees A.J., Van Es L.A., Waldherr R., Wiik A. Nomenclature of systemic vasculitides the proposal of an international consensus conference . Arthritis Rheum. 37:1994;187-192.
2. Falk R.J., Jennette J.C. Anti-neutrophil cytoplasmic autoantibodies with specificity for myeloperoxidase in patients with systemic vasculitis and idiopathic necrotizing and crescentic glomerulonephritis. N. Engl. J. Med. 25:1988;1651-1657.
3. Nölle B., Specks U., Lüdemann J., Rohrbach M.S., DeRemee R.A., Gross W.L. Anticytoplasmic autoantibodies their immunodiagnostic value . Ann. Intern. Med. 111:1989;28-40.
4. Hoffman G.S., Kerr G.S., Leavitt R.Y., Hallahan C.W., Lebovics R.S., Travis W.D., Rottem M., Fauci A.S. Wegener granulomatosis an analysis of 158 patients . Ann. Intern. Med. 116:1992;488-498.
5. Guillevin L., Durand-Gasselin B., Cevallos R., Gayraud M., Lhote F., Callard P., Amouroux J., Casassus P., Jarrousse B. Microscopic polyangiitis clinical and laboratory findings in eighty-five patients . Arthritis Rheum. 42:1999;421-430.
6. Reinhold-Keller E., Beuge N., Latza U., de Groot K., Rudert H., Nolle B., Heller M., Gross W.L. An interdisciplinary approach to the care of patients with Wegener's granulomatosis long-term outcome in 155 patients . Arthritis Rheum. 43:2000;1021-1032.
7. Carrington C.B., Liebow A.A. Limited forms of angiitis and granulomatosis of Wegener's type. Am. J. Med. 41:1966;497-527.
8. Walton E.W. Giant-cell granuloma of the respiratory tract (Wegener's granulomatosis). Br. Med. J. 2:1958;265-270.
9. DeRemee R.A., McDonald T.J., Harrison E.G., Coles D.T. Wegener's granulomatosis anatomic correlates, a proposed classification . Mayo Clin. Proc. 51:1975;777-781.
10. Fienberg R. The protracted superficial phenomenon in pathergic (Wegener's) granulomatosis. Hum. Pathol. 12:1980;458-467.
11. Spencer S.J., Burns A., Gaskin G., Pusey C.D., Rees A.J. HLA class II specificities in vasculitis with antibodies to neutrophil cytoplasmic antigens. Kidney Int. 41:1992;1059-1063.
12. Hagen E.C., Stegeman C.A., D'Amaro J., Schreuder F.M.T., Lems S.P.M., Tervaert J.W.C., de Jong G.M.T., Hené R.J., Kallenberg C.G.M., Daha M.R., van der Woude F.J. Decreased frequency of HLA-DR13DR6 in Wegner's granulomatosis. Kidney Int. 48:1995;801-805.
13. Zhang L., Jayne D.R., Zhao M.H., Lockwood C.M., Oliveira D.B. Distribution of MHC class II alleles in primary systemic vasculitis. Kidney Int. 47:1995;294-298.
14. Griffith M.E., Pusey C.D. HLA genes in ANCA-associated vasculitides. Exp. Clin. Immunogenet. 14:1997;196-205.
15. Gencik M., Borgmann S., Zahn R., Albert E., Sitter T., Epplen J.T., Fricke H. Immunogenetic risk factors for anti-neutrophil cytoplasmic antibody (ANCA)-associated systemic vasculitis. Clin. Exp. Immunol. 117:1999;412-417.
16. Kallenberg C.G., Rarok A., Stegeman C.A. Genetics of ANCA-associated vasculitides. Cleve. Clin. J. Med. 69:2002;SII61-SII63.
17. Russell K.A., Specks U. Are antineutrophil cytoplasmic antibodies pathogenic? Experimental approaches to understand the antineutrophil cytoplasmic antibody phenomenon. Rheum. Dis. Clin. North. Am. 27:2001;815-832.
18. Witko-Sarsat V., Lesavre P., Lopez S., Bessou G., Hieblot C., Prum B., Noel L.H., Guillevin L., Ravaud P., Sermet-Gaudelus I., Timsit J., Grunfeld J.P., Halbwachs-Mecarelli L. A large subset of neutrophils expressing membrane proteinase 3 is a risk factor for vasculitis and rheumatoid arthritis. J. Am. Soc. Nephrol. 10:1999;1224-1233.
19. Muller Kobold A.C., Kallenberg C.G., Tervaert J.W. Leucocyte membrane expression of proteinase 3 correlates with disease activity in patients with Wegener's granulomatosis. Br. J. Rheumatol. 37:1998;901-907.
20. Rarok A.A., Stegeman C.A., Limburg P.C., Kallenberg C.G. Neutrophil membrane expression of proteinase 3 (PR3) is related to relapse in PR3-ANCA-associated vasculitis. J. Am. Soc. Nephrol. 13:2002;2232-2238.
21. Csernok E., Szymkowiak C.H., Mistry N., Daha M.R., Gross W.L., Kekow J. Transforming growth factor-beta (TGF-β) expression and interaction with proteinase 3 (PR3) in anti-neutrophil cytoplasmic antibody (ANCA)-associated vasculitis. Clin. Exp. Immunol. 105:1996;104-111.
22. Wahl S.M., McCartney-Francis N., Mergenhagen S.E. Inflammatory and immunomodulatory roles of TGF-β Immunol. Today. 10:1989;258-261.
23. Wahl S.M. Transforming growth factor beta the good, the bad, and the ugly . J. Exp. Med. 180:1994;1587-1590.
24. Zissel G., Homolka J., Schlaak J., Schlaak M., Muller-Quernheim J. Anti-inflammatory cytokine release by alveolar macrophages in pulmonary sarcoidosis. Am. J. Respir. Crit. Care Med. 154:1996;713-719.
25. Goodnow C.C. Pathways for self-tolerance and the treatment of autoimmune diseases. Lancet. 357:2001;2115-2121.
26. Ballieux B.E.P.B., Van der Burg S.H., Hagen E.C., van der Woude F.J., Melief C.J.M., Daha M.R. Cell-mediated autoimmunity in patients with Wegener's granulomatosis (WG). Clin. Exp. Immunol. 100:1995;186-193.
27. Griffith M.E., Coulthart A., Pusey C.D. T cell responses to myeloperoxidase (MPO) and proteinase 3 (PR) in patients with systemic vasculitis. Clin. Exp. Immunol. 103:1996;253-258.
28. King W.J., Brooks C.J., Holder R., Hughes P., Adu D., Savage C.O.S. T lymphocyte responses to anti-neutrophil cytoplasmic autoantibody (ANCA) antigens are present in patients with ANCA-associated systemic vasculitis and persist during idsease remission. Clin. Exp. Immunol. 112:1998;539-546.
29. Popa E.R., Stegeman C.A., Bos N.A., Kallenberg C.G., Tervaert J.W. Differential B- and T-cell activation in Wegener's granulomatosis. J. Allergy Clin. Immunol. 103:1999;885-894.
30. van der Geld Y.M., Huitema M.G., Franssen C.F., van der Zee R., Limburg P.C., Kallenberg C.G. In vitro T lymphocyte responses to proteinase 3 (PR3) and linear peptides of PR3 in patients with Wegener's granulomatosis (WG). Clin. Exp. Immunol. 122:2000;504-513.
31. Popa E.R., Franssen C.F., Limburg P.C., Huitema M.G., Kallenberg C.G., Cohen Tervaert J.W. In vitro cytokine production and proliferation of T cells from patients with anti-proteinase 3- and antimyeloperoxidase-associated vasculitis, in response to proteinase 3 and myeloperoxidase. Arthritis Rheum. 46:2002;1894-1904.
32. Csernok E., Trabandt A., Muller A., Wang G.C., Moosig F., Paulsen J., Schnabel A., Gross W.L. Cytokine profiles in Wegener's granulomatosis predominance of type 1 (Th1) in the granulomatous inflammation . Arthritis Rheum. 42:1999;742-750.
33. Lúdvíksson B.R., Sneller M.C., Chua K.S., Talar-Williams C., Langford A.A., Ehrhardt R.O., Fauci A.S., Strober W. Active Wegener's granulomatosis is associated with HLA-DR = CD4+ T cells exhibiting an unbalanced Th1-type T cell cytokine pattern reversal with IL-10 . J. Immunol. 160:1998;3602-3609.
34. Muller A., Trabandt A., Gloeckner-Hofmann K., Seitzer U., Csernok E., Schonermarck U., Feller A.C., Gross W.L. Localized Wegener's granulomatosis predominance of CD26 and IFN-gamma expression . J. Pathol. 192:2000;113-120.
35. Balding C.E., Howie A.J., Drake-Lee A.B., Savage C.O. Th2 dominance in nasal mucosa in patients with Wegener's granulomatosis. Clin. Exp. Immunol. 125:2001;332-339.
36. Sher A., Fiorentino D., Caspar P., Pearce E., Mosmann T. Production of IL-10 by CD4+ T lymphocytes correlates with down-regulation of Th1 cytokine synthesis in helminth infection. J. Immunol. 147:1991;2713-2716.
37. Taga K., Tosato G. IL-10 inhibits human T cell proliferation and IL-2 production. J. Immunol. 148:1992;1143-1148.
38. Turner D.M., Williams D.M., Sankaran D., Lazarus M., Sinnott P.J., Hutchinson I.V. An investigation of polymorphism in the interleukin-10 gene promoter. Eur. J. Immunogenet. 24:1997;1-8.
39. Awad M.R., El-Gamel A., Hasleton P., Turner D.M., Sinnott P.J., Hutchinson I.V. Genotypic variation in the transforming growth factor-beta1 gene association with transforming growth factor-β1 production, fibrotic lung disease, and graft fibrosis after lung transplantation . Transplantation. 66:1998;1014-1020.
40. Muraközy G., Gaede K.I., Ruprecht B., Gutzeit O., Schurmann M., Schnabel A., Schlaak M., Gross W.L., Muller-Quernheim J. Gene polymorphisms of immunoregulatory cytokines and angiotensin-converting enzyme in Wegener's granulomatosis. J. Mol. Med. 79:2001;665-670.
41. Leavitt R.Y., Fauci A.S., Bloch D.A., Michel B.A., Hunder G.G., Arend W.P., Calabrese L.H., Fries J.F., Lie J.T., Lightfoot R.W.J., Masi A.T., McShane D.J., Mills J.A., Stevens M.B., Wallace S.L., Zvaifler N.J. The American College of Rheumatology 1990 criteria for the classification of Wegener's granulomatosis. Arthritis Rheum. 33:1990;1101-1107.
42. Lario S., Inigo P., Campistol J.M., Poch E., Rivera F., Oppenheimer F. Restriction enzyme-based method for transforming growth factor-β(1) genotyping nonisotopic detection of polymorphisms in codons 10 and 25 and the 5′-flanking region . Clin. Chem. 45:1999;1290-1292.
43. Perrey C., Turner S.J., Pravica V., Howell W.M., Hutchinson I.V. ARMS-PCR methodologies to determine IL-10, TNF-α, TNF-β and TGF-β 1 gene polymorphisms. Transpl. Immunol. 7:1999;127-128.
44. Cambien F., Ricard S., Troesch A., Mallet C., Generenaz L., Evans A., Arveiler D., Luc G., Ruidavets J.B., Poirier O. Polymorphisms of the transforming growth factor-beta 1 gene in relation to myocardial infarction and blood pressure the Etude Cas-Temoin de I'Infarctus du Myocarde (ECTIM) Study . Hypertension. 28:1996;881-887.
45. Pickard C., Mann C., Sinnott P., Boggild M., Hawkins C., Strange R.C., Hutchinson I.V., Ollier W.E., Donn R.P. Interleukin-10 (IL10) promoter polymorphisms and multiple sclerosis. J. Neuroimmunol. 101:1999;207-210.
46. Tagore A., Gonsalkorale W.M., Pravica V., Hajeer A.H., McMahon R., Whorwell P.J., Sinnott P.J., Hutchinson I.V. Interleukin-10 (IL-10) genotypes in inflammatory bowel disease. Tissue Antigens. 54:1999;386-390.
47. Cantagrel A., Navaux F., Loubet-Lescoulie P., Nourhashemi F., Enault G., Abbal M., Constantin A., Laroche M., Mazieres B. Interleukin-1beta, interleukin-1 receptor antagonist, interleukin-4, and interleukin-10 gene polymorphisms relationship to occurrence and severity of rheumatoid arthritis . Arthritis Rheum. 42:1999;1093-1100.
48. Huang D.R., Zhou Y.H., Xia S.Q., Liu L., Pirskanen R., Lefvert A.K. Markers in the promoter region of interleukin-10 (IL-10) gene in myasthenia gravis implications of diverse effects of IL-10 in the pathogenesis of the disease . J. Neuroimmunol. 94:1999;82-87.
49. Hewins P., Tervaert J.W., Savage C.O., Kallenberg C.G. Is Wegener's granulomatosis an autoimmune disease? Curr. Opin. Rheumatol. 12:2000;3-10.
50. Lamprecht P., Kumanovics G., Mueller A., Csernok E., Komocsi A., Trabandt A., Gross W.L., Schnabel A. Elevated monocytic IL-12 and TNF-α production in Wegener's granulomatosis is normalized by cyclophosphamide and corticosteroid therapy. Clin. Exp. Immunol. 128:2002;181-186.
51. Markowitz S., Wang J., Myeroff L., Parsons R., Sun L., Lutterbaugh J., Fan R.S., Zborowska E., Kinzler K.W., Vogelstein B., et al. Inactivation of the type II TGF-β receptor in colon cancer cells with microsatellite instability. Science. 268:1995;1336-1338.
52. Grainger D.J., Kemp P.R., Metcalfe J.C., Liu A.C., Lawn R.M., Williams N.R., Grace A.A., Schofield P.M., Chauhan A. The serum concentration of active transforming growth factor-β is severely depressed in advanced atherosclerosis. Nat. Med. 1:1995;74-79.
53. Anscher M.S., Peters W.P., Reisenbichler H., Petros W.P., Jirtle R.L. Transforming growth factor β as a predictor of liver and lung fibrosis after autologous bone marrow transplantation for advanced breast cancer. N. Engl. J. Med. 328:1993;1592-1598.
54. Kulkarni A.B., Ward J.M., Yaswen L., Mackall C.L., Bauer S.R., Huh C.G., Gress R.E., Karlsson S. Transforming growth factor-β 1 null mice an animal model for inflammatory disorders . Am. J. Pathol. 146:1995;264-275.
55. Muraközy G., Gaede K.I., Zissel G., Schlaak M., Muller-Quernheim J. Analysis of gene polymorphisms in interleukin-10 and transforming growth factor-β 1 in sarcoidosis. Sarcoidosis Vasc. Diffuse Lung Dis. 18:2001;165-169.
56. Li B., Khanna A., Sharma V., Singh T., Suthanthiran M., August P. TGF-β 1 DNA polymorphisms, protein levels, and blood pressure. Hypertension. 33:1999;271-275.
57. Xiao H., Heeringa P., Hu P., Liu Z., Zhao M., Aratani Y., Maeda N., Falk R.J., Jennette J.C. Antineutrophil cytoplasmic autoantibodies specific for myeloperoxidase cause glomerulonephritis and vasculitis in mice. J. Clin. Invest. 110:2002;955-963.
58. Halbwachs-Mecarelli L., Bessou G., Lesavre P., Lopez S., Witko-Sarsat V. Bimodal distribution of proteinase 3 (PR3) surface expression reflects a constitutive heterogeneity in the polymorphonuclear neutrophil pool. FEBS Lett. 374:1995;29-33.
59. Schreiber A., Busjahn A., Luft F.C., Kettritz R. Membrane expression of proteinase 3 is genetically determined. J. Am. Soc. Nephrol. 14:2003;68-75.
60. Lalani I., Bhol K., Ahmed A.R. Interleukin-10 biology, role in inflammation and autoimmunity . Ann. Allergy Asthma Immunol. 79:1997;469-483.
61. Llorente L., Zou W., Levy Y., Richaud-Patin Y., Wijdenes J., Alcocer-Varela J., Morel-Fourrier B., Brouet J.C., Alarcon-Segovia D., Galanaud P., et al. Role of interleukin 10 in the B lymphocyte hyperactivity and autoantibody production of human systemic lupus erythematosus. J. Exp. Med. 181:1995;839-844.
62. Banchereau J., Briere F., Liu Y.J., Rousset F. Molecular control of B lymphocyte growth and differentiation. Stem Cells. 12:1994;278-288.
63. Eskdale J., Keijsers V., Huizinga T., Gallagher G. Microsatellite alleles and single nucleotide polymorphisms (SNP) combine to form four major haplotype families at the human interleukin-10 (IL-10) locus. Genes Immun. 1:1999;151-155.
64. Zhou Y., Giscombe R., Huang D., Lefvert A.K. Novel genetic association of Wegener's granulomatosis with the interleukin 10 gene. J. Rheumatol. 29:2002;317-320.
65. Zheng C., Huang D., Liu L., Wu R., Bergenbrant Glas S., Osterborg A., Bjorkholm M., Holm G., Yi Q., Sundblad A. Interleukin-10 gene promoter polymorphisms in multiple myeloma. Int. J. Cancer. 95:2001;184-188.
66. Gibson A.W., Edberg J.C., Wu J., Westendorp R.G., Huizinga T.W., Kimberly R.P. Novel single nucleotide polymorphisms in the distal IL-10 promoter affect IL-10 production and enhance the risk of systemic lupus erythematosus. J. Immunol. 166:2001;3915-3922.
67. Ellsworth D.L., Bielak L.F., Turner S.T., Sheedy II P.F., Boerwinkle E., Peyser P.A. Gender- and age-dependent relationships between the E-selectin S128R polymorphism and coronary artery calcification. J. Mol. Med. 79:2001;390-398.
68. Freire M.B., Ji L., Onuma T., Orban T., Warram J.H., Krolewski A.S. Gender-specific association of M235T polymorphism in angiotensinogen gene and diabetic nephropathy in NIDDM. Hypertension. 31:1998;896-899.
69. Reynolds W.F., Stegeman C.A., Cohen Tervaert J.W. -463 G/A myeloperoxidase promoter polymorphism is associated with clinical manifestations and the course of disease in MPO-ANCA-associated vasculitis. Clin. Immunol. 103:2002;154-160.