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GWA study data mining and independent replication identify cardiomyopathy-associated 5 (CMYA5) as a risk gene for schizophrenia

Molecular Psychiatry volume 16, pages 1117–1129 (2011)Cite this article

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Abstract

We conducted data-mining analyses using the Clinical Antipsychotic Trials of Intervention Effectiveness (CATIE) and molecular genetics of schizophrenia genome-wide association study supported by the genetic association information network (MGS-GAIN) schizophrenia data sets and performed bioinformatic prioritization for all the markers with P-values ⩽0.05 in both data sets. In this process, we found that in the CMYA5 gene, there were two non-synonymous markers, rs3828611 and rs10043986, showing nominal significance in both the CATIE and MGS-GAIN samples. In a combined analysis of both the CATIE and MGS-GAIN samples, rs4704591 was identified as the most significant marker in the gene. Linkage disequilibrium analyses indicated that these markers were in low LD (3 828 611–rs10043986, r2=0.008; rs10043986–rs4704591, r2=0.204). In addition, CMYA5 was reported to be physically interacting with the DTNBP1 gene, a promising candidate for schizophrenia, suggesting that CMYA5 may be involved in the same biological pathway and process. On the basis of this information, we performed replication studies for these three single-nucleotide polymorphisms. The rs3828611 was found to have conflicting results in our Irish samples and was dropped out without further investigation. The other two markers were verified in 23 other independent data sets. In a meta-analysis of all 23 replication samples (family samples, 912 families with 4160 subjects; case–control samples, 11 380 cases and 15 021 controls), we found that both markers are significantly associated with schizophrenia (rs10043986, odds ratio (OR)=1.11, 95% confidence interval (CI)=1.04–1.18, P=8.2 × 10−4 and rs4704591, OR=1.07, 95% CI=1.03–1.11, P=3.0 × 10−4). The results were also significant for the 22 Caucasian replication samples (rs10043986, OR=1.11, 95% CI=1.03–1.17, P=0.0026 and rs4704591, OR=1.07, 95% CI=1.02–1.11, P=0.0015). Furthermore, haplotype conditioned analyses indicated that the association signals observed at these two markers are independent. On the basis of these results, we concluded that CMYA5 is associated with schizophrenia and further investigation of the gene is warranted.

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Acknowledgements

We thank the volunteers, patients and their family members for participating in this study. This study was supported in part by a research grant (07R-1770) from the Stanley Medical Research Institute and an Independent Investigator Award from NARSAD to XC, and by grants to investigators involved in the collection and analyses of the samples from CATIE, GAIN, the international schizophrenia consortium and other independent samples (National Institutes of Health (MH41953, MH63480, MH56242, MH078075); NARSAD Young Investigator Award; Donald & Barbara Zucker Foundation, USA; the Medical Research Council and the Wellcome Trust Foundation, UK; the Research Council of Norway (Grant No. 163070/V50, 167153/V50); the South-Eastern Norway Health Authority (123/2004); Science Foundation Ireland and Health Research Board, Ireland; the Lundbeck Foundation and Danish National Advanced Technology Foundation, Denmark). The Ashkenazi samples are part of the Hebrew University Genetic Resource (HUGR). The principal investigators of the CATIE trial were Jeffrey A Lieberman, T Scott Stroup and Joseph P McEvoy. The CATIE trial was funded by a grant from the National Institute of Mental Health (N01 MH900001) along with MH074027 (PI PF Sullivan). Genotyping was funded by Eli Lilly and Company. The principle investigators for the MGS were Pablo Gejman and Douglas Levinson. MGS study was supported by funding from the National Institute of Mental Health and the National Alliance for Research on Schizophrenia and Depression. Genotyping of part of the sample was supported by GAIN and the Paul Michael Donovan Charitable Foundation. Genotyping was carried out by the Center for Genotyping and Analysis at the Broad Institute of Harvard and MIT with support from the National Center for Research Resources.

Author information

Author notes

  1. X Chen, G Lee, B S Maher, A H Fanous, J Chen, Z Zhao, A Guo, E van den Oord, P F Sullivan, J Shi, D F Levinson, P V Gejman, A Sanders, J Duan, M J Owen, N J Craddock, M C O'Donovan, J Blackman, D Lewis, G K Kirov, W Qin, S Schwab, D Wildenauer, K Chowdari, V Nimgaonkar, R E Straub, D R Weinberger, F A O'Neill, D Walsh, M Bronstein, A Darvasi, T Lencz, A K Malhotra, D Rujescu, I Giegling, T Werge, T Hansen, A Ingason, M M Nöethen, M Rietschel, S Cichon, S Djurovic, O A Andreassen, R M Cantor, R Ophoff, A Corvin, D W Morris, M Gill, C N Pato, M T Pato, A Macedo, H M D Gurling, A McQuillin, J Pimm, C Hultman, P Lichtenstein, P Sklar, S M Purcell, E Scolnick, D St Clair, D H R Blackwood and K S Kendler: Members of the GROUP Investigators and the International Schizophrenia Consortium are listed in Appendix.

Authors and Affiliations

  1. Department of Psychiatry, Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond, VA, USA

    X Chen, G Lee, B S Maher, A H Fanous, J Chen, E van den Oord & K S Kendler

  2. Department of Molecular and Human Genetics, Virginia Commonwealth University, Richmond, VA, USA

    X Chen & K S Kendler

  3. Washington VA Medical Center, Washington, DC, USA

    A H Fanous

  4. Department of Psychiatry, Georgetown University School of Medicine, Washington, DC, USA

    A H Fanous

  5. Departments of Biomedical Informatics, Vanderbilt University, Nashville, TN, USA

    Z Zhao & A Guo

  6. Department of Pharmacy, Virginia Commonwealth University, Richmond, VA, USA

    E van den Oord

  7. Departments of Genetics, Psychiatry, and Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

    P F Sullivan

  8. Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA

    J Shi & D F Levinson

  9. Center for Psychiatric Genetics, NorthShore University HealthSystem Research Institute, Evanston, IL, USA

    P V Gejman, A Sanders & J Duan

  10. Department of Psychological Medicine, MRC Centre for Neuropsychiatric Genetics and Genomics, School of Medicine, Cardiff University, Cardiff, UK

    M J Owen, N J Craddock, M C O'Donovan, J Blackman, D Lewis & G K Kirov

  11. School of Psychiatry, University of Western Australia and Western Australian Institute for Medical Research, Perth, WA, Australia

    W Qin, S Schwab & D Wildenauer

  12. Department of Psychiatry, University of Pittsburgh School of Medicine and Graduate School of Public Health, Pittsburgh, PA, USA

    K Chowdari & V Nimgaonkar

  13. Genes Cognition and Psychosis Program, Clinical Brain Disorders Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA

    R E Straub & D R Weinberger

  14. The Department of Psychiatry, The Queens University, Belfast, Northern Ireland, UK

    F A O'Neill

  15. The Health Research Board, Dublin, Ireland

    D Walsh

  16. Department of Genetics, The Hebrew University of Jerusalem, Jerusalem, Israel

    M Bronstein & A Darvasi

  17. Zucker Hillside Hospital, Psychiatry Research, North Shore-Long Island Jewish Health System, Glen Oaks, NY, USA

    T Lencz & A K Malhotra

  18. Division of Molecular and Clinical Neurobiology, Ludwig-Maximilians-University, Munich, Germany

    D Rujescu & I Giegling

  19. Institute of Psychiatry, Mental Health Center Sct. Hans, Copenhagen University Hospital, Roskilde, Denmark

    T Werge, T Hansen & A Ingason

  20. Department of Genomics, Life & Brain Center, Institute of Human Genetics, University of Bonn, Bonn, Germany

    M M Nöethen & S Cichon

  21. Department of Genetic Epidemiology in Psychiatry, Central Institute of Mental Health Mannheim, University of Heidelberg, Mannheim, Germany

    M Rietschel

  22. Department of Psychiatry, University of Bonn, Bonn, Germany

    M Rietschel

  23. Institute of Neuroscience and Medicine (INM-1), Research Center Juelich, Juelich, Germany

    S Cichon

  24. Institute of Psychiatry, University of Oslo and Oslo University Hospital, Oslo, Norway

    S Djurovic & O A Andreassen

  25. Department of Human Genetics, UCLA Center for Neurobehavioral Genetics, Los Angeles, CA, USA

    R M Cantor & R Ophoff

  26. Department of Medical Genetics, University Medical Center Utrecht, CG Utrecht, The Netherlands

    R Ophoff

  27. Department of Psychiatry and Institute of Molecular Medicine, Neuropsychiatric Genetics Research Group, Trinity College Dublin, Dublin, Ireland

    A Corvin, D W Morris & M Gill

  28. Center for Genomic Psychiatry, University of Southern California, Los Angeles, CA, USA

    C N Pato & M T Pato

  29. Department of Psychiatry University of Coimbra, Coimbra, Portugal

    A Macedo

  30. Research Department of Mental Health Sciences, Molecular Psychiatry laboratory, Windeyer Institute of Medical Sciences, University College London Medical School, London, UK

    H M D Gurling, A McQuillin & J Pimm

  31. Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden

    C Hultman & P Lichtenstein

  32. Psychiatric and Neurodevelopmental Genetics Unit, Boston, MA, USA

    P Sklar, S M Purcell & E Scolnick

  33. Center for Human Genetic Research, Massachusetts General Hospital, Boston, MA, USA

    P Sklar, S M Purcell & E Scolnick

  34. Institute of Medical Sciences, University of Aberdeen, Aberdeen, UK

    D St Clair

  35. Division of Psychiatry, University of Edinburgh, Royal Edinburgh Hospital, Edinburgh, UK

    D H R Blackwood

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  1. X Chen
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  2. G Lee
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  4. A H Fanous
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  5. J Chen
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  6. Z Zhao
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  7. A Guo
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  8. E van den Oord
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  9. P F Sullivan
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  10. J Shi
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  11. D F Levinson
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  12. P V Gejman
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  13. A Sanders
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  14. J Duan
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  15. M J Owen
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  19. D Lewis
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  20. G K Kirov
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  21. W Qin
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  22. S Schwab
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  30. M Bronstein
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  31. A Darvasi
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  40. M Rietschel
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  41. S Cichon
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  42. S Djurovic
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  43. O A Andreassen
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  44. R M Cantor
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  46. A Corvin
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Consortia

and the GROUP investigators, the International Schizophrenia Consortium

Corresponding author

Correspondence to X Chen.

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The authors declare no conflict of interest.

Additional information

Supplementary Information accompanies the paper on the Molecular Psychiatry website

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Appendix

Appendix

The members of the Genetic Risk and Outcome in Psychosis (GROUP):

René S Kahn1, Don H Linszen2, Jim van Os3, Durk Wiersma4, Richard Bruggeman4, Wiepke Cahn1, Lieuwe de Haan2, Lydia Krabbendam3 and Inez Myin-Germeys3

1Department of Psychiatry, Rudolf Magnus Institute of Neuroscience, University Medical Center Utrecht, Postbus 85060, 3508 AB, Utrecht, The Netherlands; 2Department of Psychiatry, Academic Medical Centre University of Amsterdam, Amsterdam, NL326 Groot-Amsterdam, The Netherlands; 3Maastricht University Medical Centre, South Limburg Mental Health Research and Teaching Network, P. Debyelaan 25, 6229 HX Maastricht, Maastricht, The Netherlands; 4Department of Psychiatry, University Medical Center Groningen, University of Groningen, PO Box 30.001, 9700 RB Groningen, The Netherlands.

The members of the International schizophrenia consortium:

Cardiff University: Michael C O’Donovan6, George K Kirov6, Nick J Craddock6, Peter A Holmans6, Nigel M Williams6, Lyudmila Georgieva6, Ivan Nikolov6, N Norton6, H Williams6, Draga Toncheva16, Vihra Milanova17, Michael J Owen6; Karolinska Institutet/University of North Carolina at Chapel Hill: Christina M Hultman11,12, Paul Lichtenstein11, Emma F Thelander11, Patrick Sullivan7; Trinity College Dublin: Derek W Morris9, Colm T O’Dushlaine9, Elaine Kenny9, Emma M Quinn9, Michael Gill9, Aiden Corvin9; University College London: Andrew McQuillin8, Khalid Choudhury8, Susmita Datta8, Jonathan Pimm8, Srinivasa Thirumalai18, Vinay Puri8, Robert Krasucki8, Jacob Lawrence8, Digby Quested19, Nicholas Bass8, Hugh Gurling8; University of Aberdeen: Caroline Crombie15, Gillian Fraser15, Soh Leh Kuan14, Nicholas Walker20, David St Clair14; University of Edinburgh: Douglas HR Blackwood10, Walter J Muir10, Kevin A McGhee10, Ben Pickard10, Pat Malloy10, Alan W Maclean10, Margaret Van Beck10; Queensland Institute of Medical Research: Naomi R Wray5, Stuart Macgregor5, Peter M Visscher5; University of Southern California: Michele T Pato13, Helena Medeiros13, Frank Middleton21, Celia Carvalho13, Christopher Morley21, Ayman Fanous13,22,23,24, David Conti13, James A Knowles13, Carlos Paz Ferreira25, Antonio Macedo26, M Helena Azevedo26, Carlos N Pato13; Massachusetts General Hospital: Jennifer L Stone1,2,3,4, Douglas M Ruderfer1,2,3,4, Andrew N Kirby2,3,4, Manuel AR Ferreira1,2,3,4, Mark J Daly2,3,4, Shaun M Purcell1,2,3,4, Pamela Sklar1,2,3,4; Stanley Center for Psychiatric Research and Broad Institute of MIT and Harvard: Shaun M Purcell1,2,3,4, Jennifer L Stone1,2,3,4, Kimberly Chambert3,4, Douglas M Ruderfer1,2,3,4, Finny Kuruvilla4, Stacey B Gabriel4, Kristin Ardlie4, Jennifer L Moran4, Mark J Daly2,3,4, Edward M Scolnick3,4, Pamela Sklar1,2,3,4.

1Psychiatric and Neurodevelopmental Genetics Unit, 2Center for Human Genetic Research, Massachusetts General Hospital, 185 Cambridge Street, Boston, MA 02114, USA; 3Stanley Center for Psychiatric Research, The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA; 4The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA; 5Queensland Institute of Medical Research, 300 Herston Road, Brisbane, Queensland 4006, Australia; 6Department of Psychological Medicine, MRC Centre for Neuropsychiatric Genetics and Genomics, School of Medicine, Cardiff University, Cardiff C14 4XN, UK; 7Departments of Genetics, Psychiatry, and Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA; 8Research Department of Mental Health Sciences, Molecular Psychiatry Laboratory, University College London Medical School, Windeyer Institute of Medical Sciences, 46 Cleveland Street, LondonW1T4JF, UK; 9Department of Psychiatry and Institute of Molecular Medicine, NeuropsychiatricGenetics Research Group, Trinity College Dublin, Dublin 2, Ireland; 10Division of Psychiatry, University of Edinburgh, Royal Edinburgh Hospital, Edinburgh EH10 5HF, UK; 11Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, SE-171 77 Stockholm, Sweden; 12Department of Neuroscience, Psychiatry, Ulleråker, Uppsala University, SE-750 17 Uppsala, Sweden; 13Center for Genomic Psychiatry, University of Southern California, Los Angeles, CA 90033, USA; 14Institute of Medical Sciences, 15Department of Mental Health, University of Aberdeen, Aberdeen AB25 2ZD, UK; 16Department of Medical Genetics, University Hospital Maichin Dom, Sofia 1431, Bulgaria; 17Department of Psychiatry, First Psychiatric Clinic, Alexander University Hospital, Sofia 1431, Bulgaria; 18West Berkshire NHS Trust, 25 Erleigh Road, Reading RG3 5LR, UK; 19Department of Psychiatry, University of Oxford, Warneford Hospital, Headington, Oxford OX3 7JX, UK; 20Ravenscraig Hospital, Inverkip Road, Greenock PA16 9HA, UK; 21State University of New York—Upstate Medical University, Syracuse, NY 13210, USA; 22Washington VA Medical Center, Washington DC 20422, USA; 23Department of Psychiatry, Georgetown University School of Medicine, Washington DC 20057, USA; 24Department of Psychiatry, Virginia Commonwealth University, Richmond, VA 23298, USA; 25Department of Psychiatry, Sao Miguel, 9500-310 Azores, Portugal; 26Department of Psychiatry University of Coimbra, 3004-504 Coimbra, Portugal.

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Chen, X., Lee, G., Maher, B. et al. GWA study data mining and independent replication identify cardiomyopathy-associated 5 (CMYA5) as a risk gene for schizophrenia. Mol Psychiatry 16, 1117–1129 (2011). https://doi.org/10.1038/mp.2010.96

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