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Association of a functional variant downstream of TNFAIP3 with systemic lupus erythematosus

Nature Genetics volume 43, pages 253–258 (2011)Cite this article

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Abstract

Systemic lupus erythematosus (SLE, MIM152700) is an autoimmune disease characterized by self-reactive antibodies resulting in systemic inflammation and organ failure. TNFAIP3, encoding the ubiquitin-modifying enzyme A20, is an established susceptibility locus for SLE. By fine mapping and genomic re-sequencing in ethnically diverse populations, we fully characterized the TNFAIP3 risk haplotype and identified a TT>A polymorphic dinucleotide (deletion T followed by a T to A transversion) associated with SLE in subjects of European (P = 1.58 × 10−8, odds ratio = 1.70) and Korean (P = 8.33 × 10−10, odds ratio = 2.54) ancestry. This variant, located in a region of high conservation and regulatory potential, bound a nuclear protein complex composed of NF-κB subunits with reduced avidity. Further, compared with the non-risk haplotype, the haplotype carrying this variant resulted in reduced TNFAIP3 mRNA and A20 protein expression. These results establish this TT>A variant as the most likely functional polymorphism responsible for the association between TNFAIP3 and SLE.

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Figure 1: Variants in the TNFAIP3 region associated with SLE.
Figure 2: TNFAIP3 haplotype and conditional association analyses.
Figure 3: Functional characterization of the TT>A polymorphic dinucleotide and TNFAIP3 risk haplotype.

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Acknowledgements

We are thankful to all the individuals with SLE and to the controls that participated in this study. We are grateful to the research assistants, coordinators and physicians that helped in the recruitment of subjects. We would like to thank the following individuals for contributing samples genotyped in this study: S. D'Alfonso (Italy), R. Scorza (Italy), P. Junker and H. Laustrup (Denmark), M. Bijl (Holland), E. Endreffy (Hungary), C. Vasconcelos and B.M. da Silva (Portugal), A. Suarez and C. Gutierrez (Spain), I. Rúa-Figueroa (Spain) and C. Garcilazo (Argentina). For the Asociación Andaluza de Enfermedades Autoimmunes (AADEA) collaboration: N. Ortego-Centeno (Spain), J. Jimenez-Alonso (Spain), E. de Ramon (Spain) and J. Sanchez-Roman (Spain). For the collaboration on Hispanic populations enriched for Amerindian-European admixture: M. Cardiel (Mexico), I.G. de la Torre (Mexico), M. Maradiaga (Mexico), J.F. Moctezuma (Mexico), E. Acevedo (Peru), C. Castel and M. Busajm (Argentina), and J. Musuruana (Argentina). Other participants from the Argentine Collaborative Group are: H.R. Scherbarth, P.C. Marino, E.L. Motta, S. Gamron, C. Drenkard, E. Menso, A. Allievi, G.A. Tate, J.L. Presas, S.A. Palatnik, M. Abdala, M. Bearzotti, A. Alvarellos, F. Caeiro, A. Bertoli, S. Paira, S. Roverano, C.E. Graf, E. Bertero, C. Guillerón, S. Grimaudo, J. Manni, L.J. Catoggio, E.R. Soriano, C.D. Santos, C. Prigione, F.A. Ramos, S.M. Navarro, G.A. Berbotto, M. Jorfen, E.J. Romero, M.A. Garcia, J.C. Marcos, A.I. Marcos, C.E. Perandones, A. Eimon and C.G. Battagliotti.

We thank M.C. Comeau, M.C. Marion, P.S. Ramos, A. Williams, J. Zigler, A. Adler, S. Frank, S. Glenn and M.L. Zhu for their assistance in genotyping, quality control analyses and clinical data management; R. Lu and N. Dominguez for their assistance with EMSA; J.D. Capra for his critical reading of the manuscript; and the staff of the Lupus Family Registry and Repository (LFRR) for collecting and maintaining SLE samples. Support for this work was obtained from the US National Institutes of Health grants R01 AI063274 and R01 AR056360 (P.M.G.); R01 AR043274 (K.L.M.); N01 AR62277, R37 24717, R01 AR042460, P01 AI083194, P20 RR020143, R01 DE018209 (J.B.H.); P01 AR49084 (R.P.K. and E.E.B); R01 AR33062 (R.P.K.); P30 AR055385 (E.E.B); K08 AI083790, LRP AI071651, UL1 RR024999 (T.B.N.); R01CA141700, RC1 AR058621 (M.E.A.-R.); R01AR051545-01A2, ULI RR025014-02 (A.M.S.); P30 AR053483, N01 AI50026 (J.A.J. and J.M.G.); P20 RR015577 (J.A.J.); R21 AI070304, R01 AI070983 (S.A.B.); R01 AR43814 (B.P.T.); P60 AR053308, M01 RR-00079 (L.A.C.); R01 AR043727, UL1 RR025005 (M.A.P.). A portion of this study was supported by a grant of the Korea Healthcare Technology Research and Development Project, Ministry for Health and Welfare, Republic of Korea (A010252, A080588; S.-C.B.). Additional support was granted from the Alliance for Lupus Research (K.L.M.); Merit Award from the US Department of Veterans Affairs (J.B.H. and G.S.G.); the Swedish Research Council for Medicine, Gustaf Vth-80th Jubilee Fund and Swedish Association Against Rheumatism, Instituto de Salud Carlos III, Oklahoma Center for Advancement of Science and Technology (OCAST) HR09-106 (M.E.A.-R.); the European Science Foundation funds the BIOLUPUS network (M.E.A.-R. coordinator); the Barrett Scholarship Fund Oklahoma Medical Research Foundation (OMRF) (C.J.L.); Lupus Research Institute (T.B.N.); The Alliance for Lupus Research (T.B.N., L.A.C. and C.O.J.); the Arthritis National Research Foundation Eng Tan Scholar Award (T.B.N.); Arthritis Foundation (P.M.G. and A.M.S.); the Lupus Foundation of Minnesota (P.M.G. and K.L.M.); the Wellcome Trust (T.J.V.); Arthritis Research UK (T.J.V.); Kirkland Scholar Award (L.A.C.); and Wake Forest University Health Sciences Center for Public Health Genomics (C.D.L.). The work reported on in this publication has been in part financially supported by the European Science Foundation (ESF), in the framework of the Research Networking Programme European Science Foundation-The Identification of Novel Genes and Biomarkers for Systemic Lupus Erythematosus (BIOLUPUS) 07-RNP-083.

Author information

Author notes

  1. Mary Beth Humphrey, Courtney Gray Montgomery and Patrick M Gaffney: These authors jointly directed this work.

Authors and Affiliations

  1. Arthritis and Clinical Immunology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, Oklahoma, USA

    Indra Adrianto, Feng Wen, Graham Wiley, Christopher J Lessard, Jared S Bates, Jennifer A Kelly, Kenneth M Kaufman, Joel M Guthridge, Marta E Alarcón-Riquelme, Judith A James, R Hal Scofield, Kathy L Moser, Courtney Gray Montgomery & Patrick M Gaffney

  2. College of Medicine, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma, USA

    Amanda Templeton, Jarrod B King, Christopher J Lessard, Yanqing Hu, Kenneth M Kaufman, Judith A James, R Hal Scofield, Kathy L Moser & Mary Beth Humphrey

  3. US Department of Veterans Affairs Medical Center, Oklahoma City, Oklahoma, USA

    Kenneth M Kaufman & John B Harley

  4. Center for Genomics and Oncological Research (GENyO), Granada, Spain

    Marta E Alarcón-Riquelme

  5. Center for Autoimmune Diseases Research (CREA), Universidad del Rosario, Bogotá, Colombia

    Juan-Manuel Anaya

  6. Department of Rheumatology, Hanyang University Hospital for Rheumatic Diseases, Seoul, Korea

    Sang-Cheol Bae, So-Young Bang & So-Yeon Park

  7. Division of Rheumatology, University of Colorado Denver, Aurora, Colorado, USA

    Susan A Boackle

  8. Department of Epidemiology, University of Alabama at Birmingham, Birmingham, Alabama, USA

    Elizabeth E Brown

  9. Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA

    Michelle A Petri

  10. Department of Genetics and Pathology, Rudbeck Laboratory, Uppsala University, Uppsala, Sweden

    Caroline Gallant

  11. Division of Rheumatology, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA

    Rosalind Ramsey-Goldman

  12. Rheumatology and Clinical Immunogenetics, University of Texas Health Science Center at Houston, Houston, Texas, USA

    John D Reveille

  13. Department of Medicine, Division of Rheumatology, University of Puerto Rico Medical Sciences Campus, San Juan, Puerto Rico

    Luis M Vila

  14. Rosalind Russell Medical Research Center for Arthritis, University of California San Francisco, San Francisco, California, USA

    Lindsey A Criswell

  15. Department of Medicine, University of Alabama at Birmingham, Birmingham, Alabama, USA

    Jeffrey C Edberg & Robert P Kimberly

  16. Department of Internal Medicine, Wake Forest University Health Sciences, Winston-Salem, North Carolina, USA

    Barry I Freedman

  17. The Robert S. Boas Center for Genomics and Human Genetics, Feinstein Institute for Medical Research, North Shore Long Island Jewish (LIJ) Health System, Manhasset, New York, USA

    Peter K Gregersen

  18. Division of Rheumatology, Medical University of South Carolina, Charleston, South Carolina, USA

    Gary S Gilkeson & Diane L Kamen

  19. Department of Medicine, University of Southern California, Los Angeles, California, USA

    Chaim O Jacob

  20. Instituto de Parasitología y Biomedicina 'López-Neyra', Consejo Superior de Investigaciones Científicas (CSIC), Granada, Spain

    Javier Martin

  21. Clinical Pharmacology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, Oklahoma, USA

    Joan T Merrill

  22. Section of Rheumatology and Gwen Knapp Center for Lupus and Immunology Research, University of Chicago, Chicago, Illinois, USA

    Timothy B Niewold

  23. Sanatorio Parque, Rosario, Argentina

    Bernardo A Pons-Estel

  24. Division of Rheumatology, Department of Pediatrics, University of Washington, Seattle, Washington, USA

    Anne M Stevens

  25. Center for Immunity and Immunotherapies, Seattle Children's Research Institute, Seattle, Washington, USA

    Anne M Stevens

  26. Division of Rheumatology, Department of Medicine, University of California Los Angeles, Los Angeles, California, USA

    Betty P Tsao

  27. Division of Genetics and Molecular Medicine, King's College London, London, UK

    Timothy J Vyse

  28. Division of Immunology, Infection and Inflammatory Diseases, Kings College London, London, UK

    Timothy J Vyse

  29. Department of Biostatistical Sciences, Wake Forest University Health Sciences, Winston-Salem, North Carolina, USA

    Carl D Langefeld

  30. Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA

    John B Harley

  31. Immunobiology and Cancer Research Program, Oklahoma Medical Research Foundation, Oklahoma City, Oklahoma, USA

    Carol F Webb

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  1. Indra Adrianto
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  2. Feng Wen
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  4. Graham Wiley
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  17. Elizabeth E Brown
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  47. Patrick M Gaffney
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Contributions

P.M.G., C.G.M., K.L.M., C.J.L., J.A.K., K.M.K., C.D.L. and J.B.H. selected SNPs and were responsible for the study design. J.M.G., M.E.A.-R., J.-M.A., S.-C.B., S.-Y.B., S.A.B., E.E.B., M.A.P., C.G., R.R.-G., J.D.R., L.M.V., L.A.C., J.C.E., B.I.F., P.K.G., G.S.G., C.O.J., J.A.J., D.L.K., R.P.K., J.M., J.T.M., T.B.N., S.-Y.P., B.A.P.-E., R.H.S., A.M.S., B.P.T., L.M.V., T.J.V., J.B.H., K.L.M. and P.M.G. assisted in the collection and characterization of the SLE cases and controls. K.M.K. and P.M.G. performed the genotyping. K.M.K. and C.D.L. performed quality control analyses. I.A. and J.S.B. performed association analyses and imputation under the guidance of C.G.M. and P.M.G. F.W., G.W. and P.M.G. performed the sequencing. F.W., A.T., J.B.K., Y.H., C.F.W., M.B.H. and P.M.G. performed functional studies. I.A., C.G.M. and P.M.G. prepared the manuscript. All authors approved the final draft.

Corresponding author

Correspondence to Patrick M Gaffney.

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Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–7 and Supplementary Tables 1–3 and 5–8 (PDF 6722 kb)

Supplementary Table 4

Genotyping results of all observed and imputed markers (XLS 647 kb)

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Adrianto, I., Wen, F., Templeton, A. et al. Association of a functional variant downstream of TNFAIP3 with systemic lupus erythematosus. Nat Genet 43, 253–258 (2011). https://doi.org/10.1038/ng.766

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