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TNFSF4 is a risk factor to systemic lupus erythematosus in a Latin American population

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Abstract

Objective

The aim of this study was to examine the association of three TNFSF4 single nucleotide variants (SNVs) with systemic lupus erythematosus (SLE) susceptibility in Mexican patients.

Methods

Genotypes of the TNFSF4 rs1234315T/C, rs2205960G/T, and rs704840T/G SNVs were determined using a TaqMan assay. In our study, we included 395 patients with SLE and 500 controls.

Results

Our information shows a significant difference in the allelic and genotypic frequency of the three TNFSF4 SNVs between cases and controls. Thus, our data showed an association between TNFSF4 rs1234315T/C (T vs. C, OR 1.40, p = 0.00087), rs2205960G/T (G vs. T, OR 1.32, p = 0.0037), and rs704840T/G (T vs. G, OR 1.41, p = 0.0003) and SLE susceptibility in Mexican subjects. Besides, we conducted a meta-analysis to determine the role of TNFSF4 rs2205960G/T and SLE susceptibility; our results showed that this variant is a risk factor for SLE in Latin Americans and Asians.

Conclusion

Our results show that TNFSF4 rs1234315T/C, rs2205960G/T, and rs704840T/G are risk factors to SLE in Mexicans. This is the first study to document an association between TNFSF4 rs704840T/G and SLE in a Latin American population. In addition, our meta-analysis showed that TNFSF4 rs2205960G/T is a risk factor for Asians and Latin Americans.

Key Point

• The TNFSF4 rs1234315T/C, rs2205960G/T, and rs704849T/G SNVs are risk factors to SLE in patients from Mexico.

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References

  1. Tsokos GC, Lo MS, Costa Reis P, Sullivan KE (2016) New insights into the immunopathogenesis of systemic lupus erythematosus. Nat Rev Rheumatol 12(12):716–730. https://doi.org/10.1038/nrrheum.2016.186

    Article  CAS  PubMed  Google Scholar 

  2. Tsokos GC (2011) Systemic lupus erythematosus. N Engl J Med 365(22):2110–2121. https://doi.org/10.1056/NEJMra1100359

    Article  CAS  PubMed  Google Scholar 

  3. Arnett FC, Shulman LE (1976) Studies in familial systemic lupus erythematosus. Medicine (Baltimore) 55(4):313–322. https://doi.org/10.1097/00005792-197607000-00003

    Article  CAS  Google Scholar 

  4. Johanneson B, Lima G, von Salome J, Alarcon-Segovia D, Alarcon-Riquelme ME, Collaborative Group on the Genetics of Sle TBIICotGoSLE, Sjogrens s (2002) A major susceptibility locus for systemic lupus erythemathosus maps to chromosome 1q31. Am J Hum Genet 71(5):1060–1071. https://doi.org/10.1086/344289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Cunninghame Graham DS, Graham RR, Manku H, Wong AK, Whittaker JC, Gaffney PM, Moser KL, Rioux JD, Altshuler D, Behrens TW, Vyse TJ (2008) Polymorphism at the TNF superfamily gene TNFSF4 confers susceptibility to systemic lupus erythematosus. Nat Genet 40(1):83–89. https://doi.org/10.1038/ng.2007.47

    Article  CAS  PubMed  Google Scholar 

  6. Yang W, Shen N, Ye DQ, Liu Q, Zhang Y, Qian XX, Hirankarn N, Ying D, Pan HF, Mok CC, Chan TM, Wong RW, Lee KW, Mok MY, Wong SN, Leung AM, Li XP, Avihingsanon Y, Wong CM, Lee TL, Ho MH, Lee PP, Chang YK, Li PH, Li RJ, Zhang L, Wong WH, Ng IO, Lau CS, Sham PC, Lau YL, Asian Lupus Genetics C (2010) Genome-wide association study in Asian populations identifies variants in ETS1 and WDFY4 associated with systemic lupus erythematosus. PLoS Genet 6(2):e1000841. https://doi.org/10.1371/journal.pgen.1000841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Langefeld CD, Ainsworth HC, Cunninghame Graham DS, Kelly JA, Comeau ME, Marion MC, Howard TD, Ramos PS, Croker JA, Morris DL, Sandling JK, Almlof JC, Acevedo-Vasquez EM, Alarcon GS, Babini AM, Baca V, Bengtsson AA, Berbotto GA, Bijl M, Brown EE, Brunner HI, Cardiel MH, Catoggio L, Cervera R, Cucho-Venegas JM, Dahlqvist SR, D'Alfonso S, Da Silva BM, de la Rua FI, Doria A, Edberg JC, Endreffy E, Esquivel-Valerio JA, Fortin PR, Freedman BI, Frostegard J, Garcia MA, de la Torre IG, Gilkeson GS, Gladman DD, Gunnarsson I, Guthridge JM, Huggins JL, James JA, Kallenberg CGM, Kamen DL, Karp DR, Kaufman KM, Kottyan LC, Kovacs L, Laustrup H, Lauwerys BR, Li QZ, Maradiaga-Cecena MA, Martin J, McCune JM, McWilliams DR, Merrill JT, Miranda P, Moctezuma JF, Nath SK, Niewold TB, Orozco L, Ortego-Centeno N, Petri M, Pineau CA, Pons-Estel BA, Pope J, Raj P, Ramsey-Goldman R, Reveille JD, Russell LP, Sabio JM, Aguilar-Salinas CA, Scherbarth HR, Scorza R, Seldin MF, Sjowall C, Svenungsson E, Thompson SD, Toloza SMA, Truedsson L, Tusie-Luna T, Vasconcelos C, Vila LM, Wallace DJ, Weisman MH, Wither JE, Bhangale T, Oksenberg JR, Rioux JD, Gregersen PK, Syvanen AC, Ronnblom L, Criswell LA, Jacob CO, Sivils KL, Tsao BP, Schanberg LE, Behrens TW, Silverman ED, Alarcon-Riquelme ME, Kimberly RP, Harley JB, Wakeland EK, Graham RR, Gaffney PM, Vyse TJ (2017) Transancestral mapping and genetic load in systemic lupus erythematosus. Nat Commun 8:16021. https://doi.org/10.1038/ncomms16021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Lee HS, Kim T, Bang SY, Na YJ, Kim I, Kim K, Kim JH, Chung YJ, Shin HD, Kang YM, Shim SC, Suh CH, Park YB, Kim JS, Kang C, Bae SC (2014) Ethnic specificity of lupus-associated loci identified in a genome-wide association study in Korean women. Ann Rheum Dis 73(6):1240–1245. https://doi.org/10.1136/annrheumdis-2012-202675

    Article  CAS  PubMed  Google Scholar 

  9. Alarcon-Riquelme ME, Ziegler JT, Molineros J, Howard TD, Moreno-Estrada A, Sanchez-Rodriguez E, Ainsworth HC, Ortiz-Tello P, Comeau ME, Rasmussen A, Kelly JA, Adler A, Acevedo-Vazquez EM, Cucho-Venegas JM, Garcia-De la Torre I, Cardiel MH, Miranda P, Catoggio LJ, Maradiaga-Cecena M, Gaffney PM, Vyse TJ, Criswell LA, Tsao BP, Sivils KL, Bae SC, James JA, Kimberly RP, Kaufman KM, Harley JB, Esquivel-Valerio JA, Moctezuma JF, Garcia MA, Berbotto GA, Babini AM, Scherbarth H, Toloza S, Baca V, Nath SK, Aguilar Salinas C, Orozco L, Tusie-Luna T, Zidovetzki R, Pons-Estel BA, Langefeld CD, Jacob CO (2016) Genome-wide association study in an Amerindian ancestry population reveals novel systemic lupus erythematosus risk loci and the role of European admixture. Arthritis Rheum 68(4):932–943. https://doi.org/10.1002/art.39504

    Article  CAS  Google Scholar 

  10. Manku H, Langefeld CD, Guerra SG, Malik TH, Alarcon-Riquelme M, Anaya JM, Bae SC, Boackle SA, Brown EE, Criswell LA, Freedman BI, Gaffney PM, Gregersen PA, Guthridge JM, Han SH, Harley JB, Jacob CO, James JA, Kamen DL, Kaufman KM, Kelly JA, Martin J, Merrill JT, Moser KL, Niewold TB, Park SY, Pons-Estel BA, Sawalha AH, Scofield RH, Shen N, Stevens AM, Sun C, Gilkeson GS, Edberg JC, Kimberly RP, Nath SK, Tsao BP, Vyse TJ (2013) Trans-ancestral studies fine map the SLE-susceptibility locus TNFSF4. PLoS Genet 9(7):e1003554. https://doi.org/10.1371/journal.pgen.1003554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Sanchez E, Webb RD, Rasmussen A, Kelly JA, Riba L, Kaufman KM, Garcia-de la Torre I, Moctezuma JF, Maradiaga-Cecena MA, Cardiel-Rios MH, Acevedo E, Cucho-Venegas M, Garcia MA, Gamron S, Pons-Estel BA, Vasconcelos C, Martin J, Tusie-Luna T, Harley JB, Richardson B, Sawalha AH, Alarcon-Riquelme ME (2010) Genetically determined Amerindian ancestry correlates with increased frequency of risk alleles for systemic lupus erythematosus. Arthritis Rheum 62(12):3722–3729. https://doi.org/10.1002/art.27753

    Article  PubMed  PubMed Central  Google Scholar 

  12. Jenkins SJ, Perona-Wright G, Worsley AG, Ishii N, MacDonald AS (2007) Dendritic cell expression of OX40 ligand acts as a costimulatory, not polarizing, signal for optimal Th2 priming and memory induction in vivo. J Immunol 179(6):3515–3523. https://doi.org/10.4049/jimmunol.179.6.3515

    Article  CAS  PubMed  Google Scholar 

  13. Linton PJ, Bautista B, Biederman E, Bradley ES, Harbertson J, Kondrack RM, Padrick RC, Bradley LM (2003) Costimulation via OX40L expressed by B cells is sufficient to determine the extent of primary CD4 cell expansion and Th2 cytokine secretion in vivo. J Exp Med 197(7):875–883. https://doi.org/10.1084/jem.20021290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Karulf M, Kelly A, Weinberg AD, Gold JA (2010) OX40 ligand regulates inflammation and mortality in the innate immune response to sepsis. J Immunol 185(8):4856–4862. https://doi.org/10.4049/jimmunol.1000404

    Article  CAS  PubMed  Google Scholar 

  15. Kashiwakura J, Yokoi H, Saito H, Okayama Y (2004) T cell proliferation by direct cross-talk between OX40 ligand on human mast cells and OX40 on human T cells: comparison of gene expression profiles between human tonsillar and lung-cultured mast cells. J Immunol 173(8):5247–5257. https://doi.org/10.4049/jimmunol.173.8.5247

    Article  CAS  PubMed  Google Scholar 

  16. Zingoni A, Sornasse T, Cocks BG, Tanaka Y, Santoni A, Lanier LL (2004) Cross-talk between activated human NK cells and CD4+ T cells via OX40-OX40 ligand interactions. J Immunol 173(6):3716–3724. https://doi.org/10.4049/jimmunol.173.6.3716

    Article  CAS  PubMed  Google Scholar 

  17. Imura A, Hori T, Imada K, Ishikawa T, Tanaka Y, Maeda M, Imamura S, Uchiyama T (1996) The human OX40/gp34 system directly mediates adhesion of activated T cells to vascular endothelial cells. J Exp Med 183(5):2185–2195. https://doi.org/10.1084/jem.183.5.2185

    Article  CAS  PubMed  Google Scholar 

  18. Lin W, Voskens CJ, Zhang X, Schindler DG, Wood A, Burch E, Wei Y, Chen L, Tian G, Tamada K, Wang LX, Schulze DH, Mann D, Strome SE (2008) Fc-dependent expression of CD137 on human NK cells: insights into "agonistic" effects of anti-CD137 monoclonal antibodies. Blood 112(3):699–707. https://doi.org/10.1182/blood-2007-11-122465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Klinger M, Kim JK, Chmura SA, Barczak A, Erle DJ, Killeen N (2009) Thymic OX40 expression discriminates cells undergoing strong responses to selection ligands. J Immunol 182(8):4581–4589. https://doi.org/10.4049/jimmunol.0900010

    Article  CAS  PubMed  Google Scholar 

  20. Croft M (2010) Control of immunity by the TNFR-related molecule OX40 (CD134). Annu Rev Immunol 28:57–78. https://doi.org/10.1146/annurev-immunol-030409-101243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Sugamura K, Ishii N, Weinberg AD (2004) Therapeutic targeting of the effector T-cell co-stimulatory molecule OX40. Nat Rev Immunol 4(6):420–431. https://doi.org/10.1038/nri1371

    Article  CAS  PubMed  Google Scholar 

  22. Ishii N, Takahashi T, Soroosh P, Sugamura K (2010) OX40-OX40 ligand interaction in T-cell-mediated immunity and immunopathology. Adv Immunol 105:63–98. https://doi.org/10.1016/S0065-2776(10)05003-0

    Article  CAS  PubMed  Google Scholar 

  23. Croft M, So T, Duan W, Soroosh P (2009) The significance of OX40 and OX40L to T-cell biology and immune disease. Immunol Rev 229(1):173–191. https://doi.org/10.1111/j.1600-065X.2009.00766.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 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(11):1271–1277. https://doi.org/10.1002/art.1780251101

    Article  CAS  PubMed  Google Scholar 

  25. Boyle AP, Hong EL, Hariharan M, Cheng Y, Schaub MA, Kasowski M, Karczewski KJ, Park J, Hitz BC, Weng S, Cherry JM, Snyder M (2012) Annotation of functional variation in personal genomes using RegulomeDB. Genome Res 22(9):1790–1797. https://doi.org/10.1101/gr.137323.112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Ward LD, Kellis M (2012) HaploReg: a resource for exploring chromatin states, conservation, and regulatory motif alterations within sets of genetically linked variants. Nucleic Acids Res 40(Database issue):D930–D934. https://doi.org/10.1093/nar/gkr917

    Article  CAS  PubMed  Google Scholar 

  27. Consortium GT (2013) The Genotype-Tissue Expression (GTEx) project. Nat Genet 45(6):580–585. https://doi.org/10.1038/ng.2653

    Article  CAS  Google Scholar 

  28. Martorell-Marugan J, Toro-Dominguez D, Alarcon-Riquelme ME, Carmona-Saez P (2017) MetaGenyo: a web tool for meta-analysis of genetic association studies. BMC Bioinformatics 18(1):563. https://doi.org/10.1186/s12859-017-1990-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Chua KH, Ooh YY, Chai HC (2016) TNFSF4 polymorphisms are associated with systemic lupus erythematosus in the Malaysian population. Int J Immunogenet 43(5):303–309. https://doi.org/10.1111/iji.12287

    Article  CAS  PubMed  Google Scholar 

  30. Zuo XB, Sheng YJ, Hu SJ, Gao JP, Li Y, Tang HY, Tang XF, Cheng H, Yin XY, Wen LL, Sun LD, Yang S, Cui Y, Zhang XJ (2014) Variants in TNFSF4, TNFAIP3, TNIP1, BLK, SLC15A4 and UBE2L3 interact to confer risk of systemic lupus erythematosus in Chinese population. Rheumatol Int 34(4):459–464. https://doi.org/10.1007/s00296-013-2864-3

    Article  CAS  PubMed  Google Scholar 

  31. Gupta V, Kumar S, Pratap A, Singh R, Kumari R, Kumar S, Aggarwal A, Misra R (2018) Association of ITGAM, TNFSF4, TNFAIP3 and STAT4 gene polymorphisms with risk of systemic lupus erythematosus in a North Indian population. Lupus 27(12):1973–1979. https://doi.org/10.1177/0961203318786432

    Article  CAS  PubMed  Google Scholar 

  32. 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(11):1234–1237. https://doi.org/10.1038/ng.472

    Article  CAS  PubMed  Google Scholar 

  33. Gateva V, Sandling JK, Hom G, Taylor KE, Chung SA, Sun X, Ortmann W, Kosoy R, Ferreira RC, Nordmark G, Gunnarsson I, Svenungsson E, Padyukov L, Sturfelt G, Jonsen A, Bengtsson AA, Rantapaa-Dahlqvist S, Baechler EC, Brown EE, Alarcon GS, Edberg JC, Ramsey-Goldman R, McGwin G Jr, Reveille JD, Vila LM, Kimberly RP, Manzi S, Petri MA, Lee A, Gregersen PK, Seldin MF, Ronnblom L, Criswell LA, Syvanen AC, Behrens TW, Graham RR (2009) A large-scale replication study identifies TNIP1, PRDM1, JAZF1, UHRF1BP1 and IL10 as risk loci for systemic lupus erythematosus. Nat Genet 41(11):1228–1233. https://doi.org/10.1038/ng.468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Zhang SQ, Han JW, Sun LD, Lu WS, Yin XY, Zhang XJ, Yang S (2011) A single-nucleotide polymorphism of the TNFSF4 gene is associated with systemic lupus erythematosus in Chinese Han population. Rheumatol Int 31(2):227–231. https://doi.org/10.1007/s00296-009-1247-2

    Article  CAS  PubMed  Google Scholar 

  35. Delgado-Vega AM, Abelson AK, Sanchez E, Witte T, D'Alfonso S, Galeazzi M, Jimenez-Alonso J, Pons-Estel BA, Martin J, Alarcon-Riquelme ME (2009) Replication of the TNFSF4 (OX40L) promoter region association with systemic lupus erythematosus. Genes Immun 10(3):248–253. https://doi.org/10.1038/gene.2008.95

    Article  CAS  PubMed  Google Scholar 

  36. Taylor KE, Chung SA, Graham RR, Ortmann WA, Lee AT, Langefeld CD, Jacob CO, Kamboh MI, Alarcon-Riquelme ME, Tsao BP, Moser KL, Gaffney PM, Harley JB, Petri M, Manzi S, Gregersen PK, Behrens TW, Criswell LA (2011) Risk alleles for systemic lupus erythematosus in a large case-control collection and associations with clinical subphenotypes. PLoS Genet 7(2):e1001311. https://doi.org/10.1371/journal.pgen.1001311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Sanchez E, Comeau ME, Freedman BI, Kelly JA, Kaufman KM, Langefeld CD, Brown EE, Alarcon GS, Kimberly RP, Edberg JC, Ramsey-Goldman R, Petri M, Reveille JD, Vila LM, Merrill JT, Tsao BP, Kamen DL, Gilkeson GS, James JA, Vyse TJ, International Consortium on the Genetics of Systemic Lupus E, Gaffney PM, Jacob CO, Niewold TB, Richardson BC, Harley JB, Alarcon-Riquelme ME, Sawalha AH (2011) Identification of novel genetic susceptibility loci in African American lupus patients in a candidate gene association study. Arthritis Rheum 63(11):3493–3501. https://doi.org/10.1002/art.30563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Chang YK, Yang W, Zhao M, Mok CC, Chan TM, Wong RW, Lee KW, Mok MY, Wong SN, Ng IO, Lee TL, Ho MH, Lee PP, Wong WH, Lau CS, Sham PC, Lau YL (2009) Association of BANK1 and TNFSF4 with systemic lupus erythematosus in Hong Kong Chinese. Genes Immun 10(5):414–420. https://doi.org/10.1038/gene.2009.16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Xu J, He Y, Wang J, Li X, Huang L, Li S, Qin X (2019) Influence of the TNFSF4 rs1234315 polymorphism in the susceptibility to systemic lupus erythematosus and rheumatoid arthritis. Hum Immunol 80(4):270–275. https://doi.org/10.1016/j.humimm.2018.11.006

    Article  CAS  PubMed  Google Scholar 

  40. Lettre G, Rioux JD (2008) Autoimmune diseases: insights from genome-wide association studies. Hum Mol Genet 17(R2):R116–R121. https://doi.org/10.1093/hmg/ddn246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Cordell HJ, Clayton DG (2005) Genetic association studies. Lancet 366(9491):1121–1131. https://doi.org/10.1016/S0140-6736(05)67424-7

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Facultad de Química, Universidad Nacional Autónoma de México (UNAM), Ciudad de México, México

    Mario Adán Moreno-Eutimio

  2. Unidad de Investigación, Hospital Juárez de México, Mexico City, Mexico

    Carmen Estefanía Martínez-Alemán, Ivan Sammir Aranda-Uribe & Julian Ramírez-Bello

  3. Laboratorio de Investigación en Genómica, Genética y Bioinformática, Hospital Infantil de México Federico Gómez, Mexico City, Mexico

    Guillermo Aquino-Jarquin

  4. Departamento de Investigación en Virología y Micología, Instituto Nacional de Enfermedades Respiratorias, Mexico City, Mexico

    Carlos Cabello-Gutierrez

  5. Departamento de Biología Molecular, Instituto Nacional de Cardiología, Mexico City, Mexico

    José Manuel Fragoso

  6. Servicio de Reumatología, Hospital Juárez de México, Mexico City, Mexico

    Rosa Elda Barbosa-Cobos

  7. Centro Médico Nacional “La Raza”, IMSS, Mexico City, Mexico

    Miguel A. Saavedra

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  1. Mario Adán Moreno-Eutimio
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Moreno-Eutimio, M.A., Martínez-Alemán, C.E., Aranda-Uribe, I.S. et al. TNFSF4 is a risk factor to systemic lupus erythematosus in a Latin American population. Clin Rheumatol 40, 929–939 (2021). https://doi.org/10.1007/s10067-020-05332-9

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