Top

Published in:

01-07-2018 | Original Article

C-reactive protein (CRP) polymorphisms and haplotypes are associated with SLE susceptibility and activity but not with serum CRP levels in Mexican population

Authors: Yemil Atisha-Fregoso, Guadalupe Lima, Eduardo Carrillo-Maravilla, Rosalinda Posadas-Sánchez, Nonanzit Pérez-Hernández, Miguel Baños-Peláez, Alejandra Iturralde-Chávez, Nora Hernández-Díaz, Juan Jakez-Ocampo, José Manuel Rodríguez-Pérez, Gilberto Vargas-Alarcón, Luis Llorente, Juanita Romero-Díaz

Published in: Clinical Rheumatology | Issue 7/2018

Abstract

To evaluate the association of C-reactive protein (CRP) polymorphisms with risk of development SLE in a group of Mexican individuals. Five CRP polymorphisms (rs3093059, rs3093062, rs1800947, rs1130864, and rs1205) were determined by PCR-restriction fragment length polymorphism and SNP rs3093061 by refractory mutation system PCR assay in 126 SLE patients and 131 controls. Four of the polymorphisms showed differences between patients and controls. rs3093061 polymorphism was associated with a lower risk of developing lupus principally in the codominant 2 (OR = 0.219, 95% CI 0.108–0.785, P = 0.015) model. rs1130864 was associated with decreased risk mainly under codominant 1 (OR = 0.288, 95% CI 0.143–0.581, P = 0.001) model. rs1205 was associated under the over-dominant model (OR = 0.504, 95% CI 0.270–0.942, P = 0.032). The rs3091244 polymorphism was associated with decreased risk of SLE mostly under additive (OR = 0.605, 95% CI 0.393–0.931. P = 0.022) model. Our study establishes that rs3093061, rs1130864, rs1205, and rs3091244 polymorphisms are associated with decreased risk of developing SLE.

Hurlimann J, Thorbecke GJ, Hochwald GM (1966) The liver as the site of C-reactive protein formation. J Exp Med 123:365–378CrossRefPubMedPubMedCentral

Manfredi AA, Rovere-Querini P, Bottazzi B, Garlanda C, Mantovani A (2008) Pentraxins, humoral innate immunity and tissue injury. Curr Opin Immunol 20:538–544CrossRefPubMed

Pepys MB, Hirschfield GM (2003) C-reactive protein: a critical update. J Clin Invest 111:1805–1812CrossRefPubMedPubMedCentral

Volanakis J, Kaplan M (1971) Specificity of C-reactive protein for choline phosphate residues of pneumococcal C-polysaccharide. Proc Soc Exp Biol Med 136:612–614CrossRefPubMed

Du Clos TW (1989) C-reactive protein reacts with the U1 small nuclear ribonucleoprotein. J Immunol 143:2553–2559PubMed

Chang M-K, Binder CJ, Torzewski M, Witztum JL (2002) C-reactive protein binds to both oxidized LDL and apoptotic cells through recognition of a common ligand: phosphorylcholine of oxidized phospholipids. Proc Natl Acad Sci U S A 99:13043–13048CrossRefPubMedPubMedCentral

Marnell L, Mold C, Du Clos TW (2005) C-reactive protein: ligands, receptors and role in inflammation. Clin Immunol 117:104–111CrossRefPubMed

Muñoz LE, Janko C, Grossmayer GE, Frey B, Voll RE, Kern P, Kalden JR, Schett G, Fietkau R, Herrmann M, Gaipl US (2009) Remnants of secondarily necrotic cells fuel inflammation in systemic lupus erythematosus. Arthritis Rheum 60:1733–1742CrossRefPubMed

Herrmann M, Voll RE, Zoller OM, Hagenhofer M, Ponner BB, Kalden JR (1998) Impaired phagocytosis of apoptotic cell material by monocyte-derived macrophages from patients with systemic lupus erythematosus. Arthritis Rheum 41:1241–1250CrossRefPubMed

10.

Gaitonde S, Samols D, Kushner I (2008) C-reactive protein and systemic lupus erythematosus. Arthritis Rheum 59:1814–1820CrossRefPubMed

11.

Rhodes B, Morris DL, Subrahmanyan L, Aubin C, de Leon CFM, Kelly JF, Evans DA, Whittaker JC, Oksenberg JR, de Jager PL, Vyse TJ (2008) Fine-mapping the genetic basis of CRP regulation in African Americans: a Bayesian approach. Hum Genet 123:633–642CrossRefPubMedPubMedCentral

12.

Edberg JC, Wu J, Langefeld CD, Brown EE, Marion MC, McGwin G Jr, Petri M, Ramsey-Goldman R, Reveille JD, Frank SG, Kaufman KM, Harley JB, Alarcón GS, Kimberly RP (2008) Genetic variation in the CRP promoter: association with systemic lupus erythematosus. Hum Mol Genet 17:1147–1155CrossRefPubMed

13.

Jönsen A, Gunnarsson I, Gullstrand B et al (2007) Association between SLE nephritis and polymorphic variants of the CRP and FcγRIIIa genes. Rheumatology 46:1417–1421CrossRefPubMed

14.

Kim H-A, Chun H-Y, Kim S-H et al (2009) C-reactive protein gene polymorphisms in disease susceptibility and clinical manifestations of Korean systemic lupus erythematosus. J Rheumatol 36:2238–2243CrossRefPubMed

15.

Rhodes B, Wong A, Navarra SV, Villamin C, Vyse TJ (2008) Genetic determinants of basal C-reactive protein expression in Filipino systemic lupus erythematosus families. Genes Immun 9:153–160CrossRefPubMedPubMedCentral

16.

Russell AI, Cunninghame Graham DS, Shepherd C, Roberton CA, Whittaker J, Meeks J, Powell RJ, Isenberg DA, Walport MJ, Vyse TJ (2004) Polymorphism at the C-reactive protein locus influences gene expression and predisposes to systemic lupus erythematosus. Hum Mol Genet 13:137–147CrossRefPubMed

17.

Shih PB, Manzi S, Shaw P, Kenney M, Kao AH, Bontempo F, Barmada MM, Kammerer C, Kamboh MI (2008) Genetic variation in C-reactive protein (CRP) gene may be associated with risk of systemic lupus erythematosus and CRP concentrations. J Rheumatol 35:2171–2178CrossRefPubMedPubMedCentral

18.

Szalai AJ, McCrory MA, Cooper GS et al (2002) Association between baseline levels of C-reactive protein (CRP) and a dinucleotide repeat polymorphism in the intron of the CRP gene. Genes Immun 3:14–19CrossRefPubMed

19.

Tan EM, Cohen AS, Fries JF, Masi AT, Mcshane DJ, Rothfield NF, Schaller JG, Talal N, Winchester RJ (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25:1271–1277CrossRefPubMed

20.

Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40:1725CrossRefPubMed

21.

Romero-Díaz J, Vargas-Vóracková F, Kimura-Hayama E et al (2012) Systemic lupus erythematosus risk factors for coronary artery calcifications. Rheumatology (Oxford) 51:110–119CrossRef

22.

Gladman DD, Ibañez D, Urowitz MB (2002) Systemic lupus erythematosus disease activity index 2000. J Rheumatol 29:288–291PubMed

23.

Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215CrossRefPubMedPubMedCentral

24.

Teng MS, Hsu LA, Wu S, et al (2009) Association between C-reactive protein gene haplotypes and C-reactive protein levels in Taiwanese: interaction with obesity. Atherosclerosis

25.

Gaudet M, Fara A-G, Beritognolo I, Sabatti M (2009) Allele-specific PCR in SNP genotyping. In: Methods Mol Biol, pp 415–424

26.

Ibañez D, Gladman D, Urowitz M (2007) Summarizing disease features over time: II. Variability measures of SLEDAI-2K. J Rheumatol 34:336–340PubMed

27.

Flores-Alfaro E, Fernández-Tilapa G, Salazar-Martínez E, Cruz M, Illades-Aguiar B, Parra-Rojas I (2012) Common variants in the CRP gene are associated with serum C-reactive protein levels and body mass index in healthy individuals in Mexico. Genet Mol Res 11:2258–2267CrossRefPubMed

28.

Graham RR, Cotsapas C, Davies L, Hackett R, Lessard CJ, Leon JM, Burtt NP, Guiducci C, Parkin M, Gates C, Plenge RM, Behrens TW, Wither JE, Rioux JD, Fortin PR, Cunninghame Graham D, Wong AK, Vyse TJ, Daly MJ, Altshuler D, Moser KL, Gaffney PM (2008) Genetic variants near TNFAIP3 on 6q23 are associated with systemic lupus erythematosus. Nat Genet 40:1059–1061CrossRefPubMedPubMedCentral

29.

Han JW, Zheng HF, Cui Y, Sun LD, Ye DQ, Hu Z, Xu JH, Cai ZM, Huang W, Zhao GP, Xie HF, Fang H, Lu QJ, Xu JH, Li XP, Pan YF, Deng DQ, Zeng FQ, Ye ZZ, Zhang XY, Wang QW, Hao F, Ma L, Zuo XB, Zhou FS, du WH, Cheng YL, Yang JQ, Shen SK, Li J, Sheng YJ, Zuo XX, Zhu WF, Gao F, Zhang PL, Guo Q, Li B, Gao M, Xiao FL, Quan C, Zhang C, Zhang Z, Zhu KJ, Li Y, Hu DY, Lu WS, Huang JL, Liu SX, Li H, Ren YQ, Wang ZX, Yang CJ, Wang PG, Zhou WM, Lv YM, Zhang AP, Zhang SQ, Lin D, Li Y, Low HQ, Shen M, Zhai ZF, Wang Y, Zhang FY, Yang S, Liu JJ, Zhang XJ (2009) Genome-wide association study in a Chinese Han population identifies nine new susceptibility loci for systemic lupus erythematosus. Nat Genet 41:1234–1237CrossRefPubMed

30.

Harley J, Alarcón-Riquelme M (2013) Genome-wide association scan in women with systemic lupus erythematosus identifies susceptibility variants in ITGAM, PXK, KIAA1542 and other loci. Nat Genet 40:204–210CrossRef

31.

Hom G, Graham RR, Modrek B, Taylor KE, Ortmann W, Garnier S, Lee AT, Chung SA, Ferreira RC, Pant PVK, Ballinger DG, Kosoy R, Demirci FY, Kamboh MI, Kao AH, Tian C, Gunnarsson I, Bengtsson AA, Rantapää-Dahlqvist S, Petri M, Manzi S, Seldin MF, Rönnblom L, Syvänen AC, Criswell LA, Gregersen PK, Behrens TW (2008) Association of systemic lupus erythematosus with C8orf13-BLK and ITGAM-ITGAX. N Engl J Med 358:900–909CrossRefPubMed

32.

Yang W, Shen N, Ye DQ et al (2010) Genome-wide association study in Asian populations identifies variants in ETS1 and WDFY4 associated with systemic lupus erythematosus. PLoS Genet 6(2):e1000841CrossRefPubMedPubMedCentral

33.

Rhodes B, Furnrohr BG, Vyse TJ et al (2011) C-reactive protein in rheumatology: biology and genetics. Nat Rev Rheumatol 7:282–289CrossRefPubMed

34.

Shen J, Ordovas JM (2009) Impact of genetic and environmental factors on hsCRP concentrations and response to therapeutic agents. Clin Chem 55:256–264CrossRefPubMed

35.

Zee RYL, Ridker PM (2002) Polymorphism in the human C-reactive protein (CRP) gene, plasma concentrations of CRP, and the risk of future arterial thrombosis. Atherosclerosis 162:217–219CrossRefPubMed

36.

Verzilli C, Shah T, Casas JP, Chapman J, Sandhu M, Debenham SL, Boekholdt MS, Khaw KT, Wareham NJ, Judson R, Benjamin EJ, Kathiresan S, Larson MG, Rong J, Sofat R, Humphries SE, Smeeth L, Cavalleri G, Whittaker JC, Hingorani AD (2008) Bayesian meta-analysis of genetic association studies with different sets of markers. Am J Hum Genet 82:859–872CrossRefPubMedPubMedCentral

37.

Rhodes B, Merriman ME, Harrison A, Nissen MJ, Smith M, Stamp L, Steer S, Merriman TR, Vyse TJ (2010) A genetic association study of serum acute-phase C-reactive protein levels in rheumatoid arthritis: implications for clinical interpretation. PLoS Med 7:e1000341CrossRefPubMedPubMedCentral

38.

Gabay C, Roux-Lombard P, De Moerloose P et al (1993) Absence of correlation between interleukin 6 and C-reactive protein blood levels in systemic lupus erythematosus compared with rheumatoid arthritis. J Rheumatol 20:815–821PubMed

39.

Mok CC, Birmingham DJ, Ho LY, Hebert LA, Rovin BH (2013) High-sensitivity C-reactive protein, disease activity, and cardiovascular risk factors in systemic lupus erythematosus. Arthritis Care Res (Hoboken) 65:441–447CrossRef

40.

Enocsson H, Sjöwall C, Kastbom A, Skogh T, Eloranta ML, Rönnblom L, Wetterö J (2014) Association of serum C-reactive protein levels with lupus disease activity in the absence of measurable interferon-α and a C-reactive protein gene variant. Arthritis Rheumatol (Hoboken, NJ) 66:1568–1573CrossRef

41.

Ridker PM, Pare G, Parker A, Zee RYL, Danik JS, Buring JE, Kwiatkowski D, Cook NR, Miletich JP, Chasman DI (2008) Loci related to metabolic-syndrome pathways including LEPR, HNF1A, IL6R, and GCKR associate with plasma C-reactive protein: the Women’s Genome Health Study. Am J Hum Genet 82:1185–1192CrossRefPubMedPubMedCentral

42.

Szalai AJ, Alarcón GS, Calvo-Alén J et al (2005) Systemic lupus erythematosus in a multiethnic US cohort (LUMINA). XXX: association between C-reactive protein (CRP) gene polymorphisms and vascular events. Rheumatology 44:864–868CrossRefPubMed

43.

Karassa FB, Trikalinos T, Ioannidis JP (2004) The role of FcgammaRIIA and IIIA polymorphisms in autoimmune diseases. Biomed Pharmacother 58:286–291CrossRefPubMed

44.

Urowitz MB, Gladman D, Ibañez D, Bae SC, Sanchez-Guerrero J, Gordon C, Clarke A, Bernatsky S, Fortin PR, Hanly JG, Wallace DJ, Isenberg D, Rahman A, Alarcón GS, Merrill JT, Ginzler E, Khamashta M, Nived O, Sturfelt G, Bruce IN, Steinsson K, Manzi S, Ramsey-Goldman R, Dooley MA, Zoma A, Kalunian K, Ramos M, van Vollenhoven RF, Aranow C, Stoll T, Petri M, Maddison P, Systemic Lupus International Collaborating Clinics (2010) Atherosclerotic vascular events in a multinational inception cohort of systemic lupus erythematosus. Arthritis Care Res (Hoboken) 62:881–887CrossRef

45.

Toloza SMA, Uribe AG, McGwin G et al (2004) Systemic lupus erythematosus in a multiethnic US cohort (LUMINA): XXIII. Baseline predictors of vascular events. Arthritis Rheum 50:3947–3957CrossRefPubMed

Title: C-reactive protein (CRP) polymorphisms and haplotypes are associated with SLE susceptibility and activity but not with serum CRP levels in Mexican population
Authors: Yemil Atisha-Fregoso
Guadalupe Lima
Eduardo Carrillo-Maravilla
Rosalinda Posadas-Sánchez
Nonanzit Pérez-Hernández
Miguel Baños-Peláez
Alejandra Iturralde-Chávez
Nora Hernández-Díaz
Juan Jakez-Ocampo
José Manuel Rodríguez-Pérez
Gilberto Vargas-Alarcón
Luis Llorente
Juanita Romero-Díaz
Publication date: 01-07-2018
Publisher: Springer London
Published in: Clinical Rheumatology / Issue 7/2018
Print ISSN: 0770-3198
Electronic ISSN: 1434-9949
DOI: https://doi.org/10.1007/s10067-018-4059-5

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

C-reactive protein (CRP) polymorphisms and haplotypes are associated with SLE susceptibility and activity but not with serum CRP levels in Mexican population

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 7/2018

Sharp decline in hydroxychloroquine dosing—analysis of 17,797 initiators from 2007 to 2016

Clinical relevance of ANCA in small-vessel vasculitis: positioning of antigen-specific immunoassays

Assessing information needs and use of online resources for disease self-management in patients with rheumatoid arthritis: a qualitative study

Monoclonal gammopathy in rheumatic diseases

Letter to the Editor: Time for cost-effectiveness studies for preventive strategies applied according to risk of cytomegalovirus-related morbidity and mortality in ANCA-associated vasculitis

Pain threshold and temporomandibular function in systemic sclerosis: comparison with psoriatic arthritis

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page