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LRRTM1 on chromosome 2p12 is a maternally suppressed gene that is associated paternally with handedness and schizophrenia

Molecular Psychiatry volume 12, pages 1129–1139 (2007)Cite this article

Abstract

Left–right asymmetrical brain function underlies much of human cognition, behavior and emotion. Abnormalities of cerebral asymmetry are associated with schizophrenia and other neuropsychiatric disorders. The molecular, developmental and evolutionary origins of human brain asymmetry are unknown. We found significant association of a haplotype upstream of the gene LRRTM1 (Leucine-rich repeat transmembrane neuronal 1) with a quantitative measure of human handedness in a set of dyslexic siblings, when the haplotype was inherited paternally (P=0.00002). While we were unable to find this effect in an epidemiological set of twin-based sibships, we did find that the same haplotype is overtransmitted paternally to individuals with schizophrenia/schizoaffective disorder in a study of 1002 affected families (P=0.0014). We then found direct confirmatory evidence that LRRTM1 is an imprinted gene in humans that shows a variable pattern of maternal downregulation. We also showed that LRRTM1 is expressed during the development of specific forebrain structures, and thus could influence neuronal differentiation and connectivity. This is the first potential genetic influence on human handedness to be identified, and the first putative genetic effect on variability in human brain asymmetry. LRRTM1 is a candidate gene for involvement in several common neurodevelopmental disorders, and may have played a role in human cognitive and behavioral evolution.

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Acknowledgements

We thank the families who took part in this study; David Smith, Catherine Joachim and OPTIMA (Oxford Project to Investigate Memory and Ageing) for access to post-mortem brain tissue; Xiayi Ke for testing his screening algorithm for imprinted genes; Phil Burnet for plasmids and samples; Dianne Gerelli and the Human Developmental Brain Resource (London, UK) for pilot in situ hybridization studies; Jordana Tsenova for ideas on genetic analysis; Eris Duro for help with mutation screening; Abigail Woodroffe for handling genotype data; Julie V Perederiy for help with in situ experiments; Drs Dermot Walsh and F Anthony O'Neill made critical contributions to the collection of the Irish Study of High Density Schizophrenia Families (ISHDSF). Drs Enn Jõeste and Liina Kiho from North Estonian Regional Hospital, Tallinn, helped in collecting human brain tissue. David Goldstein, Kevin Shianna and Dongliang Ge provided genotype data. Han Chinese Schizophrenia Sample data and biomaterials were collected as a part of the National Institute of Mental Health (NIMH) Schizophrenia Genetics Initiative. A complete list of the people who contributed on the NIMH project is in the Supplementary material. CF was a NARSAD Young Investigator (National Alliance for Research on Schizophrenia and Depression). APM is a Wellcome Principal Research Fellow. RW-M is a Wellcome Trust Research Career Development Fellow. SEF is a Royal Society Research Fellow. TT is a Wellcome Trust International Senior Research Fellow in Biomedical Science in Central Europe. JN is supported by the Swiss National Science Foundation and by a Marie Curie Intra-European Fellowship. BSA was supported by a Fellowship from the Tourette Syndrome Association. This research was funded additionally by The Wellcome Trust (UK); the Schizophrenia Research Fund (UK); the Academy of Finland and the Sigrid Juselius Foundation (Finland); the Graham Boeckh Chair Program in Schizophrenia to GAR at McGill University; Warner-Lambert, Parke-Davis Pharmaceuticals Company, and National Institute of Mental Health grant R01 MH-44245 (LED); National Institute of Health grants MH41953 (collection and analysis of the ISHDSF) and MH61399 (MK); and by grant ‘Research on Psychiatric and Neurological disorders and Mental Health’ from the ministry of Health, Labor and Welfare of Japan (H14-Kokoro-002), and Grant-in-Aid for Scientific Research on Priority Areas (C) Medical Genome Science from the Ministry of Education, Culture, Sports, Science and Technology of Japan. Clyde Francks conceived and directed this research.

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Author notes

  1. S Maegawa and J Laurén: These authors contributed equally to this work.

Authors and Affiliations

  1. Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, UK

    C Francks, A Velayos-Baeza, S Colella, M Groszer, E Z McAuley, T M Caffrey, J Nicod, S E Fisher, R Wade-Martins, J Ragoussis & A P Monaco

  2. GlaxoSmithKline SpA, Research Centre, Verona, Italy

    C Francks & P Muglia

  3. Division of Functional Genomics, Research Center for Bioscience and Technology, Tottori University, Yonago, Tottori, Japan

    S Maegawa & E Nanba

  4. Department of Neurology, Yale University School of Medicine, New Haven, CT, USA

    J Laurén & S M Strittmatter

  5. Department of Neurology, David Geffen School of Medicine, University of California at Los Angeles, Los Angeles, CA, USA

    B S Abrahams, B P Riley, D H Geschwind & K S Kendler

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

    S E Medland & N G Martin

  7. Queensland Institute of Medical Research, Brisbane, QLD, Australia

    S E Medland & P A Lind

  8. Department of Gene Technology, Tallinn University of Technology, Tallinn, Estonia

    T Timmusk, P Pruunsild & I Koppel

  9. Department of Biomedical Science, Regenerative Medicine and Biofunction, Graduate School of Medical Science, Tottori University, Yonago, Tottori, Japan

    N Matsumoto-Itaba & M Oshimura

  10. Center for the Study of Brain Diseases, CHUM Research Center, Montreal University, Montreal, QC, Canada

    L Xiong & G A Rouleau

  11. Departments of Psychiatry, Neurology and Human Genetics, McGill University, Douglas Hospital Research Centre, Montreal, QC, Canada

    R Joober

  12. Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany

    W Enard & B Krinsky

  13. Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, UK

    A J Richardson & J F Stein

  14. Department of Psychiatry, Ludwig Maximilians University, Munich, Germany

    H-J Möller & D Rujescu

  15. Institute of Medical Sciences, University of Aberdeen, Aberdeen, Scotland

    D St Clair

  16. Department of Psychiatry, Weskoppies Hospital, University of Pretoria, Pretoria, Republic of South Africa

    J L Roos

  17. Laboratory of Human Neurogenetics, Rockefeller University, New York, NY, USA

    M Karayiorgou

  18. Neuroscience Center, University of Helsinki, Helsinki, Finland

    M S Airaksinen

  19. Department of Psychiatry, New York University, New York, NY, USA

    L E DeLisi

  20. The Nathan S Kline Institute for Psychiatric Research, Orangeburg, New York, NY, USA

    L E DeLisi

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  1. C Francks
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  2. S Maegawa
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  3. J Laurén
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  7. S Colella
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  8. M Groszer
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  9. E Z McAuley
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  10. T M Caffrey
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  14. P A Lind
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  20. B Krinsky
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  21. E Nanba
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  22. A J Richardson
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  23. B P Riley
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  24. N G Martin
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  25. S M Strittmatter
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  26. H-J Möller
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  27. D Rujescu
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  28. D St Clair
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  29. P Muglia
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  30. J L Roos
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  31. S E Fisher
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  32. R Wade-Martins
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  33. G A Rouleau
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  34. J F Stein
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  35. M Karayiorgou
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  36. D H Geschwind
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  37. J Ragoussis
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  38. K S Kendler
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  39. M S Airaksinen
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  40. M Oshimura
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  41. L E DeLisi
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  42. A P Monaco
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Corresponding author

Correspondence to C Francks.

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Supplementary Information accompanies the paper on the Molecular Psychiatry website (http://www.nature.com/mp)

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Francks, C., Maegawa, S., Laurén, J. et al. LRRTM1 on chromosome 2p12 is a maternally suppressed gene that is associated paternally with handedness and schizophrenia. Mol Psychiatry 12, 1129–1139 (2007). https://doi.org/10.1038/sj.mp.4002053

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