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Evaluation of the TREX1 gene in a large multi-ancestral lupus cohort

Genes & Immunity volume 12, pages 270–279 (2011)Cite this article

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Abstract

Systemic lupus erythematosus (SLE) is a prototypic autoimmune disorder with a complex pathogenesis in which genetic, hormonal and environmental factors have a role. Rare mutations in the TREX1 gene, the major mammalian 3′–5′ exonuclease, have been reported in sporadic SLE cases. Some of these mutations have also been identified in a rare pediatric neurological condition featuring an inflammatory encephalopathy known as Aicardi–Goutières syndrome (AGS). We sought to investigate the frequency of these mutations in a large multi-ancestral cohort of SLE cases and controls. A total of 40 single-nucleotide polymorphisms (SNPs), including both common and rare variants, across the TREX1 gene, were evaluated in ∼8370 patients with SLE and ∼7490 control subjects. Stringent quality control procedures were applied, and principal components and admixture proportions were calculated to identify outliers for removal from analysis. Population-based case–control association analyses were performed. P-values, false-discovery rate q values, and odds ratios (OR) with 95% confidence intervals (CI) were calculated. The estimated frequency of TREX1 mutations in our lupus cohort was 0.5%. Five heterozygous mutations were detected at the Y305C polymorphism in European lupus cases but none were observed in European controls. Five African cases incurred heterozygous mutations at the E266G polymorphism and, again, none were observed in the African controls. A rare homozygous R114H mutation was identified in one Asian SLE patient, whereas all genotypes at this mutation in previous reports for SLE were heterozygous. Analysis of common TREX1 SNPs (minor allele frequency (MAF)>10%) revealed a relatively common risk haplotype in European SLE patients with neurological manifestations, especially seizures, with a frequency of 58% in lupus cases compared with 45% in normal controls (P=0.0008, OR=1.73, 95% CI=1.25–2.39). Finally, the presence or absence of specific autoantibodies in certain populations produced significant genetic associations. For example, a strong association with anti-nRNP was observed in the European cohort at a coding synonymous variant rs56203834 (P=2.99E−13, OR=5.2, 95% CI=3.18–8.56). Our data confirm and expand previous reports and provide additional support for the involvement of TREX1 in lupus pathogenesis.

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Acknowledgements

The cooperation of patients and normal control individuals involved in this study as well as physicians that provide samples is gratefully acknowledged. At the Oklahoma Medical Research Foundation, the work was supported by the NIH (AR042460, RR015577, AR048940, RR020143, AI24717, AR62277), Lupus Foundation of America, the Alliance for Lupus Research, the US Department of Veterans Affairs. At the Washington University School of Medicine (St Louis, MO, USA), the work was supported by grants (HL083822 (PHK), and NS062069 (JPA)), and the Cerebral Retinal Vasculopathy Fund. At the University of Alabama at Birmingham, the work was supported by grants AR33062 (RPK), AR49084 (RPK) and 5UL1RR02777. At the Johns Hopkins University School of Medicine, the work was supported by The Hopkins Lupus Cohort (NIH AR43727) and UL1RR025005 from the National Center for Research Resources (NCRR). At the University of Colorado, Denver School of Medicine, the work was supported by a NIH grant R21AI070304. At the Medical University of South Carolina, Charleston, USA, the project was supported by award number UL1RR029882 from the National Center for Research Resources. (The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Center for Research Resources or the National Institutes of Health). At the Rosalind Russell Medical Research Center for Arthritis, University of California, San Francisco, USA, the work was supported by Kirkland Scholar Award, US Public Health Service National Center for Research Resources, M01 RR-00079 and NIH grants AR044804, AR02175 and AR052300. At the Northwestern University, Feinberg School of Medicine, Chicago, IL, USA, the work was supported by NIH grants K24 AR 002138, P60 2 AR30692, PO1 AR49084 and UL1RR025741. At the Wake Forest University Health Sciences, Department of Biochemistry, the work was supported by R01GM069962 and Alliance for Lupus Research (67692) awards. We acknowledge grants from the European Science Foundation for the BIOLUPUS network, the Swedish Research Council, Swedish Association against Rheumatism, the Swedish International Development Agency (SIDA) and Gustaf Vth–80th jubilee Foundation to MEAR and the NIH grant CA141700-01. For GENLES: Argentina: Hugo R Scherbarth, MD; Pilar C Marino, MD; Estela L Motta, MD at Servicio de Reumatología, Hospital Interzonal General de Agudos ‘Dr Oscar Alende’, Mar del Plata, Argentina. Susana Gamron, MD; Cristina Drenkard, MD; Emilia Menso, MD at Servicio de Reumatología de la UHMI 1, Hospital Nacional de Clínicas, Universidad Nacional de Córdoba, Córdoba, Argentina. Alberto Allievi, MD; Guillermo A Tate, MD at Organización Médica de Investigación, Buenos Aires, Argentina. Jose L Presas, MD at Hospital General de Agudos Dr Juán A Fernandez, Buenos Aires, Argentina. Simon A Palatnik, MD; Marcelo Abdala, MD; Mariela Bearzotti, PhD at Facultad de Ciencias Medicas, Universidad Nacional de Rosario y Hospital Provincial del Centenario, Rosario, Argentina. Alejandro Alvarellos, MD; Francisco Caeiro, MD; Ana Bertoli, MD at Servicio de Reumatología, Hospital Privado, Centro Medico de Córdoba, Córdoba, Argentina. Sergio Paira, MD; Susana Roverano, MD at Hospital José M. Cullen, Santa Fe, Argentina. Cesar E Graf, MD; Estela Bertero, PhD at Hospital San Martín, Paraná. Cesar Caprarulo, MD; Griselda Buchanan, PhD at Hospital Felipe Heras, Concordia, Entre Ríos, Argentina. Carolina Guillerón, MD; Sebastian Grimaudo, PhD; Jorge Manni, MD at Departamento de Inmunología, Instituto de Investigaciones Médicas ‘Alfredo Lanari’, Buenos Aires, Argentina. Luis J Catoggio, MD; Enrique R Soriano, MD; Carlos D Santos, MD at Sección Reumatología, Servicio de Clínica Medica, Hospital Italiano de Buenos Aires y Fundación Dr Pedro M Catoggio para el Progreso de la Reumatología, Buenos Aires, Argentina. Cristina Prigione, MD; Fernando A Ramos, MD; Sandra M Navarro, MD at Servicio de Reumatología, Hospital Provincial de Rosario, Rosario, Argentina. Guillermo A Berbotto, MD; Marisa Jorfen, MD; Elisa J Romero, PhD at Servicio de Reumatología Hospital Escuela Eva Perón. Granadero Baigorria, Rosario, Argentina. Mercedes A Garcia, MD; Juan C Marcos MD; Ana I Marcos, MD at Servicio de Reumatología, Hospital Interzonal General de Agudos General San Martín, La Plata. Carlos E Perandones, MD; Alicia Eimon, MD at Centro de Educación Médica e Investigaciones Clínicas (CEMIC), Buenos Aires, Argentina. Cristina G Battagliotti, MD at Hospital de Niños Dr Orlando Alassia, Santa Fe, Argentina. Perú is represented by: Dr Eduardo Acevedo and Dr Mariano Cucho, Hospital Nacional Guillermo Almenara Irigoyen, Lima, Perú. Mexico is represented by Dr Ignacio García de la Torre, Hospital General de Occidente, Zapopan, Jalisco; Dr Mario Cardiel Ríos, Hospital General Dr Miguel Silva, Morelia, Michoacán; Dr José Francisco Moctezuma, Hospital General de México, México, DF; Dr Marco Maradiaga Ceceña, Hospital General de Culiacán, Culiacán, Sinaloa. The members of the BIOLUPUS network are: Sandra D’Alfonso, Department of Medical Sciences and IRCAD, University of Eastern Piedmont, Novara, Italy; Bernard R. Lauwerys, Cliniques Universitaires Saint-Luc, Université catholique de Louvain, Bruxells, Belgium; Emoke Endreffy, Department of Pediatrics and Health Center, University of Szeged, Szeged, Hungary; László Kovács, Department of Rheumatology, Albert Szent-Györgyi Clinical Centre, University of Szeged, Szeged, Hungary; Carlos Vasconcelos, Hospital Santo Antonio and ICBAS, Porto, Portugal; Berta Martins da Silva, UMIB/ICBAS, Immunogenetics laboratory, Universidado do Porto, Porto, Portugal; Iñigo Rúa Figueroa, Hospital Doctor Negrin, Las Palmas de Gran Canaria, Spain. Sandra D’Alfonso, Nadia Barizzone (Department of Medical Sciences and IRCAD, University of Eastern Piedmont, Novara, Italy); Gian Domenico Sebastiani (Azienda Ospedaliera San Camillo-Forlanini, Roma, Italy); Mauro Galeazzi, (Siena University, Siena, Italy) Maria Giovanna Danieli (Clinica Medica di Scienze Mediche e Chirurgiche, Universitá Politecnica delle Marche, Ancona, Italy); Giovanni La Montagna (Rheumatology Unit Second University of Naples, Naples, Italy) and Maria Grazia Sabbadini (Vita-Salute San Raffaele University of Milan, Italy).

Author information

Author notes

  1. M E Alarcón-Riquelme: On behalf of the BIOLUPUS network. The members of this network are listed in acknowledgements.

  2. B A Pons-Estel: On behalf of the GENLES collaboration. The members of this collaboration are listed in acknowledgements.

Authors and Affiliations

  1. Oklahoma Medical Research Foundation, Oklahoma City, OK, USA

    B Namjou, J A Kelly, S B Glenn, J O Ojwang, A Adler, M E Alarcón-Riquelme, J T Merrill, R H Scofield, K L Moser, P M Gaffney, J A James & K M Kaufman

  2. Washington University School of Medicine, St Louis, MI, USA

    P H Kothari & J P Atkinson

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

    M E Alarcón-Riquelme & C J Gallant

  4. Center for Genomics and Oncological Research Pfizer-University of Granada-Junta de Andalucía, Granada, Spain

    M E Alarcón-Riquelme

  5. University of Colorado Denver School of Medicine, Aurora, CO, USA

    S A Boackle

  6. Department of Medicine, Rosalind Russell Medical Research Center for Arthritis, University of California, San Francisco, CA, USA

    L A Criswell

  7. Clinical Immunology and Rheumatology, University of Alabama at Birmingham, Birmingham, AL, USA

    R P Kimberly, E Brown & J Edberg

  8. University of Washington, Seattle Children's Hospital, Seattle, WA, USA

    A M Stevens

  9. The Lupus genetic Group, University of Southern California, Los Angeles, CA, USA

    C O Jacob

  10. Division of Rheumatology, Department of Medicine, David Geffen School of Medicine, UCLA, Los Angeles, CA, USA

    B P Tsao

  11. Medical University of South Carolina, Charleston, SC, USA

    G S Gilkeson & D L Kamen

  12. Johns Hopkins University School of Medicine, Baltimore, MD, USA

    M Petri

  13. Northwestern University, Feinberg School of Medicine, Chicago, IL, USA

    R R Goldman

  14. University of Puerto Rico School of Medicine, San Juan, Puerto Rico

    L M Vila

  15. Center for Autoimmune Diseases Research (CREA), Universidad del Rosario, Bogota, Colombia

    J-M Anaya

  16. University of Chicago, Section of Rheumatology, Chicago, IL, USA

    T B Niewold

  17. Instituto de Biomedicina y Parasitología López-Neyra, Armilla, Spain

    J Martin

  18. Sanatorio Parque, Rosario, Argentina

    B A Pons-Estel

  19. Department of Internal Medicine, Hospital Virgen de las Nieves, Granada, Spain

    J M Sabio

  20. Department of Internal Medicine, Hospital Clinico San Cecilio, Granada, Spain

    J L Callejas

  21. Imperial College London, Hammersmith Hospital, London, UK

    T J Vyse

  22. Division of Rheumatology, Department of Internal Medicine and the Hospital for Rheumatic Diseases, Hanyang University, Seoul, Republic of Korea

    S-C Bae

  23. Wake Forest University Health Sciences, Winston-Salem, NC, USA

    F W Perrino, B I Freedman & C D Langefeld

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

    K M Kaufman

  25. Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA

    J B Harley

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  1. B Namjou
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  2. P H Kothari
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  3. J A Kelly
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  4. S B Glenn
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  15. C O Jacob
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  19. J T Merrill
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  20. M Petri
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  21. R R Goldman
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  22. L M Vila
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  26. B A Pons-Estel
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  27. J M Sabio
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  28. J L Callejas
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  29. T J Vyse
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  30. S-C Bae
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  31. F W Perrino
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  32. B I Freedman
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  33. R H Scofield
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  34. K L Moser
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  35. P M Gaffney
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  36. J A James
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  37. C D Langefeld
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  38. K M Kaufman
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  39. J B Harley
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  40. J P Atkinson
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Corresponding author

Correspondence to B Namjou.

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Namjou, B., Kothari, P., Kelly, J. et al. Evaluation of the TREX1 gene in a large multi-ancestral lupus cohort. Genes Immun 12, 270–279 (2011). https://doi.org/10.1038/gene.2010.73

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