Association of extended interleukin-10 promoter haplotypes with disease susceptibility and manifestations in German patients with systemic lupus erythematosus

Lupus

Volumn 23, Issue 4, 2014, Pages 378-385

  Schotte, H ^a   Willeke, P ^b   Becker, H ^b   Poggemeyer, J ^a   Gaubitz, M ^c   Schmidt, H ^d   Schluter B ^d  

^a Franziskus Hospital Harderberg   (Germany)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^c Akademie fur Manuelle Medizin   (Germany)

^d Institut für Klinische Chemie und Laboratoriumsmedizin Universitätsklinkum Münster   (Germany)

Author keywords

cytokines; disease susceptibility; genetic polymorphism; immunogenetics; interleukin 10; SLE

Indexed keywords

DOUBLE STRANDED DNA ANTIBODY; INTERLEUKIN 10; DNA;

ADOLESCENT; ADULT; AGED; ALLELE; ARTICLE; CHILD; CLINICAL FEATURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; FUNCTIONAL STATUS; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENOTYPING TECHNIQUE; GERMANY; GLOMERULONEPHRITIS; HAPLOTYPE; HUMAN; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; PRESCHOOL CHILD; PRIORITY JOURNAL; PROMOTER REGION; SCHOOL CHILD; SINGLE NUCLEOTIDE POLYMORPHISM; SYSTEMIC LUPUS ERYTHEMATOSUS; YOUNG ADULT; CASE CONTROL STUDY; CAUCASIAN; GENETICS; GENOTYPE; IMMUNOLOGY; THEORETICAL MODEL;

ALLELES; CASE-CONTROL STUDIES; DNA; EUROPEAN CONTINENTAL ANCESTRY GROUP; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; GERMANY; HAPLOTYPES; HUMANS; INTERLEUKIN-10; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MODELS, THEORETICAL; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC;

EID: 84896114393     PISSN: 09612033     EISSN: 14770962     Source Type: Journal    
DOI: 10.1177/0961203314522334     Document Type: Article

References (58)

1. Mok CC, Lau CS. Pathogenesis of systemic lupus erythematosus. J Clin Pathol. 2003 ; 56: 481-490
2. Prokunina L, Alarcon-Riquelme M. The genetic basis of systemic lupus erythematosus-knowledge of today and thoughts for tomorrow. Hum Mol Genet. 2004 ; 13: R143 - R148
3. Tsokos GC. Systemic lupus erythematosus. N Engl J Med. 2011 ; 365: 2110-2121
4. Manolio TA, Collins FS, Cox NJ, et al. Finding the missing heritability of complex diseases. Nature. 2009 ; 461: 747-753
5. Sabat R, Grutz G, Warszawska K, et al. Biology of interleukin-10. Cytokine Growth Factor Rev. 2010 ; 21: 331-344
6. Fiorentino DF, Zlotnik A, Vieira P, et al. IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1 cells. J Immunol. 1991 ; 146: 3444-3451
7. de Waal MR, Haanen J, Spits H, et al. Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J Exp Med. 1991 ; 174: 915-924
8. Fiorentino DF, Bond MW, Mosmann TR. Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J Exp Med. 1989 ; 170: 2081-2095
9. Wanidworanun C, Strober W. Predominant role of tumor necrosis factor-alpha in human monocyte IL-10 synthesis. J Immunol. 1993 ; 151: 6853-6861
10. Rousset F, Garcia E, Defrance T, et al. Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc Natl Acad Sci U S A. 1992 ; 89: 1890-1893
11. Ding L, Linsley PS, Huang LY, Germain RN, Shevach EM. IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression. J Immunol. 1993 ; 151: 1224-1234
12. De Waal Malefyt R, Yssel H, De Vries JE. Direct effects of IL-10 on subsets of human CD4 + T cell clones and resting T cells. Specific inhibition of IL-2 production and proliferation. J Immunol. 1993 ; 150: 4754-4765
13. Llorente L, Richaud-Patin Y, Wijdenes J, et al. Spontaneous production of interleukin-10 by B lymphocytes and monocytes in systemic lupus erythematosus. Eur Cytokine Netw. 1993 ; 4: 421-427
14. Llorente L, Richaud-Patin Y, Fior R, et al. In vivo production of interleukin-10 by non-T cells in rheumatoid arthritis, Sjogren's syndrome, and systemic lupus erythematosus. A potential mechanism of B lymphocyte hyperactivity and autoimmunity. Arthritis Rheum. 1994 ; 37: 1647-1655
15. Llorente L, Zou W, Levy Y, et al. Role of interleukin 10 in the B lymphocyte hyperactivity and autoantibody production of human systemic lupus erythematosus. J Exp Med. 1995 ; 181: 839-844
16. Horwitz DA, Gray JD, Behrendsen SC, et al. Decreased production of interleukin-12 and other Th1-type cytokines in patients with recent-onset systemic lupus erythematosus. Arthritis Rheum. 1998 ; 41: 838-844
17. Houssiau FA, Lefebvre C, Vanden Berghe M, Lambert M, Devogelaer JP, Renauld JC. Serum interleukin 10 titers in systemic lupus erythematosus reflect disease activity. Lupus. 1995 ; 4: 393-395
18. Hagiwara E, Gourley MF, Lee S, Klinman DK. Disease severity in patients with systemic lupus erythematosus correlates with an increased ratio of interleukin-10:interferon-gamma-secreting cells in the peripheral blood. Arthritis Rheum. 1996 ; 39: 379-385
19. Park YB, Lee SK, Kim DS, Lee J, Lee CH, Song CH. Elevated interleukin-10 levels correlated with disease activity in systemic lupus erythematosus. Clin Exp Rheumatol. 1998 ; 16: 283-88
20. Capper ER, Maskill JK, Gordon C, Blakemore AI. Interleukin (IL)-10, IL-1ra and IL-12 profiles in active and quiescent systemic lupus erythematosus: could longitudinal studies reveal patient subgroups of differing pathology?. Clin Exp Immunol. 2004 ; 138: 348-356
21. Chun HY, Chung JW, Kim HA, et al. Cytokine IL-6 and IL-10 as biomarkers in systemic lupus erythematosus. J Clin Immunol. 2007 ; 27: 461-466
22. Llorente L, Richaud-Patin Y, Garcia-Padilla C, et al. Clinical and biologic effects of anti-interleukin-10 monoclonal antibody administration in systemic lupus erythematosus. Arthritis Rheum. 2000 ; 43: 1790-1800
23. Miles S, Isenberg D. A review of serological abnormalities in relatives of SLE patients. Lupus. 1993 ; 2: 145-150
24. Llorente L, Richaud-Patin Y, Couderc J, et al. Dysregulation of interleukin-10 production in relatives of patients with systemic lupus erythematosus. Arthritis Rheum. 1997 ; 40: 1429-1435
25. Llorente L, Richaud-Patin Y. The role of interleukin-10 in systemic lupus erythematosus. J Autoimmun. 2003 ; 20: 287-289
26. Westendorp RG, Langermans JA, Huizinga TW, et al. Genetic influence on cytokine production and fatal meningococcal disease. Lancet. 1997 ; 349: 170-173
27. Gateva V, Sandling JK, Hom G, et al. A large-scale replication study identifies TNIP1, PRDM1, JAZF1, UHRF1BP1 and IL10 as risk loci for systemic lupus erythematosus. Nat Genet. 2009 ; 41: 1228-1233
28. Eskdale J, Kube D, Tesch H, Gallagher G. Mapping of the human IL10 gene and further characterization of the 5' flanking sequence. Immunogenetics. 1997 ; 46: 120-128
29. Schotte H, Gaubitz M, Willeke P, et al. Interleukin-10 promoter microsatellite polymorphisms in systemic lupus erythematosus: association with the anti-Sm immune response. Rheumatology (Oxford). 2004 ; 43: 1357-1363
30. Turner DM, Williams DM, Sankaran D, Lazarus M, Sinnott PJ, Hutchinson IV. An investigation of polymorphism in the interleukin-10 gene promoter. Eur J Immunogenet. 1997 ; 24: 1-8
31. Edwards-Smith CJ, Jonsson JR, Purdie DM, Bansal A, Shorthouse C, Powell EE. Interleukin-10 promoter polymorphism predicts initial response of chronic hepatitis C to interferon alfa. Hepatology. 1999 ; 30: 526-530
32. Lazarus M, Hajeer AH, Turner D, et al. Genetic variation in the interleukin 10 gene promoter and systemic lupus erythematosus. J Rheumatol. 1997 ; 24: 2314-2317
33. Rood MJ, Keijsers V, Van der Linden MW, et al. Neuropsychiatric systemic lupus erythematosus is associated with imbalance in interleukin 10 promoter haplotypes. Ann Rheum Dis. 1999 ; 58: 85-89
34. Lopez P, Gutierrez C, Suarez A. IL-10 and TNFalpha genotypes in SLE. J Biomed Biotechnol. 2010 ; 2010: 838390. DOI: 10.1155/2010/838390-838390. DOI: 10.1155/2010/838390
35. Rosado S, Rua-Figueroa I, Vargas JA, et al. Interleukin-10 promoter polymorphisms in patients with systemic lupus erythematosus from the Canary Islands. Int J Immunogenet. 2008 ; 35: 235-242
36. Mok CC, Lanchbury JS, Chan DW, Lau CS. Interleukin-10 promoter polymorphisms in Southern Chinese patients with systemic lupus erythematosus. Arthritis Rheum. 1998 ; 41: 1090-1095
37. Eskdale J, Gallagher G, Verweij CL, Keijsers V, Westendorp RG, Huizinga TW. Interleukin 10 secretion in relation to human IL-10 locus haplotypes. Proc Natl Acad Sci U S A. 1998 ; 95: 9465-9470
38. Mormann M, Rieth H, Hua TD, et al. Mosaics of gene variations in the Interleukin-10 gene promoter affect interleukin-10 production depending on the stimulation used. Genes Immun. 2004 ; 5: 246-255
39. Westendorp RG, van Dunne FM, Kirkwood TB, Helmerhorst FM, Huizinga TW. Optimizing human fertility and survival. Nat Med. 2001 ; 7: 873-873
40. De Jong BA, Westendorp RG, Eskdale J, Uitdehaag BM, Huizinga TW. Frequency of functional interleukin-10 promoter polymorphism is different between relapse-onset and primary progressive multiple sclerosis. Hum Immunol. 2002 ; 63: 281-285
41. Lard LR, Van Gaalen FA, Schonkeren JJ, et al. Association of the -2849 interleukin-10 promoter polymorphism with autoantibody production and joint destruction in rheumatoid arthritis. Arthritis Rheum. 2003 ; 48: 1841-1848
42. Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997 ; 40: 1725-1725
43. Assmann G, Schulte H. Relation of high-density lipoprotein cholesterol and triglycerides to incidence of atherosclerotic coronary artery disease (the PROCAM experience). Prospective Cardiovascular Munster study. Am J Cardiol. 1992 ; 70: 733-737
44. International HapMap Project. http://hapmap.ncbi.nlm.nih.gov (2011, accessed December 2011).
45. Gibson AW, Edberg JC, Wu J, Westendorp RG, Huizinga TW, Kimberly RP. Novel single nucleotide polymorphisms in the distal IL-10 promoter affect IL-10 production and enhance the risk of systemic lupus erythematosus. J Immunol. 2001 ; 166: 3915-3922
46. Higuchi R PCR-technology, principles and applications for DNA amplification. Ehrlich HA, ed. New York: Stockton Press ; 1989: 31-38.
47. Stephens M, Smith NJ, Donnelly P. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet. 2001 ; 68: 978-989
48. Stephens M, Donnelly P. A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet. 2003 ; 73: 1162-1169
49. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics. 2005 ; 21: 263-265
50. Sham PC, Curtis D. Monte Carlo tests for associations between disease and alleles at highly polymorphic loci. Ann Hum Genet. 1995 ; 59: 97-105
51. Beebe AM, Cua DJ, De Waal MR. The role of interleukin-10 in autoimmune disease: systemic lupus erythematosus (SLE) and multiple sclerosis (MS). Cytokine Growth Factor Rev. 2002 ; 13: 403-412
52. Lacki JK, Samborski W, Mackiewicz SH. Interleukin-10 and interleukin-6 in lupus erythematosus and rheumatoid arthritis, correlations with acute phase proteins. Clin Rheumatol. 1997 ; 16: 275-278
53. Tan EM, Cohen AS, Fries JF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1982 ; 25: 1271-1277
54. O'Neill S, Cervera R. Systemic lupus erythematosus. Best Pract Res Clin Rheumatol. 2010 ; 24: 841-855
55. Yap DY, Lai KN. Cytokines and their roles in the pathogenesis of systemic lupus erythematosus: from basics to recent advances. J Biomed Biotechnol. 2010 ; 2010: 365083-365083
56. Eskdale J, Gallagher G, Verweij CL, Keijsers V, Westendorp RG, Huizinga TW. Interleukin 10 secretion in relation to human IL-10 locus haplotypes. Proc Natl Acad Sci U S A. 1998 ; 95: 9465-9470
57. Nossent H, Berden J, Swaak T. Renal immunofluorescence and the prediction of renal outcome in patients with proliferative lupus nephritis. Lupus. 2000 ; 9: 504-510
58. 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. 1999 ; 1: 151-155