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Kleine Levin Syndrome Is Associated with Birth Difficulties and Genetic Variants in the TRANK1 Gene Loci

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Kleine Levin Syndrome Is Associated with Birth Difficulties and Genetic Variants in the TRANK1 Gene Loci medRxiv preprint doi: https://doi.org/10.1101/2021.01.08.20249006; this version posted January 16, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license . Kleine Levin syndrome is associated with birth difficulties and genetic variants in the TRANK1 gene loci. Aditya Ambati1*, Ryan Hillary1*, Smaranda Leu-Semenescu2†, Hanna M. Ollila1,3†, Ling Lin1, Emmanuel During1, Neal Farber4, Thomas J Rico1, Juliette Faraco1, Eileen Leary1, Andrea Goldstein-Piekarski1, Yu-Shu Huang5, Fang Han6, Yakov Sivan7, Michel Lecendreux8, Pauline Dodet2, Makoto Honda9, Natan Gadoth10, Sona Nevsimalova11, Fabio Pizza12, Takashi Kanbayashi13, Rosa Peraita Adrados14, Guy Leschziner15, Rosa Hasan16, Francesca Canellas17, Kazuhiko Kume18, Makrina Daniilidou19, Patrice Bourgin20, David Rye21, José L Vicario22, Birgit Högl23, Seung Chul Hong24, Guiseppe Plazzi12, Geert Mayer25, Anne Marie Landtblom20, Yves Dauvilliers26, Isabelle Arnulf2*, Emmanuel Mignot1* 1. Stanford University Center for Sleep Sciences and Medicine, Department of Psychiatry and Behavioral Sciences. 3165 Porter Drive, Palo Alto, CA 94304, USA. 2. Sleep Disorders Unit (Department “R3S”), Pitié-Salpêtrière Hospital, APHP, National Reference Center for Narcolepsy, Idiopathic Hypersomnia and Kleine–Levin Syndrome, Sorbonne University, IHU@ICM, INSERM, CNRS UMR7225, MOV’IT team, F-75013 Paris, France. 3. Institute for Molecular Medicine Finland, HiLIFE, University of Helsinki, Helsinki, Finland. 4. Kleine-Levin Syndrome Foundation, Boston, MA, USA. 5. Department of Child Psychiatry and Sleep Center, Chang Gung Memorial Hospital and University, Taoyuan, Taiwan. 6. Department of Pulmonary Medicine, the Peking University People's Hospital, Beijing, China. 7. Safra Children's Hospital, Sheba Medical Center, Tel Aviv University, Sackler Faculty of Medicine, Tel Aviv, Israel. 8. Pediatric Sleep Center and National Reference Center for Narcolepsy and Idiopathic Hypersomnia Hospital Robert Debre, Paris, France. 9. Tokyo Metropolitan Institute of Medical Science, Sleep Disorders project, Tokyo, Japan. 10. Dept Neurology, Maynei Hayeshua Medical Center, Bnei Barak , and Sackler Faculty of Medicine , Tel-Aviv University , Israel. 11. Department of Neurology, Charles University, 1st Faculty of Medicine and General Teaching Hospital, Prague, Czech Republic. 12. Department of Biomedical and Neuromotor Sciences, University of Bologna and IRCCS Institute of Neurological Sciences, Bologna, Italy. 13. Akita University, Department of Neuropsychiatry, Akita-City, Akita, 010-8543, Japan. 14. Sleep and Epilepsy Unit – Clinical Neurophysiology Service, University General Hospital Gregorio Marañón, Research Institute Gregorio Marañón. University Complutense of Madrid, Spain. 15. Sleep Disorders Centre, Guy's Hospital, London SE1 9RT, England. 16. Institute of Psychiatry, Hospital das Clinicas, Faculty of Medicine, University of Sao Paulo. Dr Ovidio Pires de Campos n. 785, 05403-010, Brazil. 17. Department of Psychiatry, Hospital Universitari Son Espases, Palma de Mallorca, Health Research Institute of the Balearic Islands (IdISBa), Spain. 18. Department of Neuropharmacology, Graduate School of Pharmaceutical Sciences, Nagoya, Japan. 19. Division of Neurology, Department of Clinical and Experimental Medicine, University of Linköping, Linköping, Sweden/Department of Neuroscience/Neurology, Uppsala University, Uppsala, Sweden. 20. Sleep disorders Center-CIRCSom, CHU Strasbourg & CNRS - Institute for Cellular and Integrative Neurosciences, University of Strasbourg. 21. Emory Program in Sleep, Brain Health Center, Atlanta, GA USA. 1 NOTE: This preprint reports new research that has not been certified by peer review and should not be used to guide clinical practice. medRxiv preprint doi: https://doi.org/10.1101/2021.01.08.20249006; this version posted January 16, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license . 22. JLV Histocompatibility, Blood Center of the Community of Madrid, Madrid, Spain 23. Department of Neurology, Innsbruck Medical University, Austria. 24. Department of Neuropsychiatry, St. Vincent’s Hospital, Catholic University of Korea, College of Medicine, Seoul, Korea. 25. Hephata Klinik, Schimmelpfengstr. 6, 34613 Schwalmstadt, Germany; Philipps Universität Marburg, Baldinger Str., 35043 Marburg, Germany. 26. Centre de référence nationale narcolepsie et hypersomnies rares, 34295 Montpellier cedex 5, France; Unité des troubles du sommeil et de l'éveil, hôpital Gui-De- Chauliac, 80, avenue Augustin-Fliche, 34295 Montpellier cedex 5, France; Inserm U1061, 34295 Montpellier, France. *,†=Equally contributing Corresponding author: Emmanuel Mignot, Stanford University Center for Sleep Sciences and Medicine, 3165 Porter Drive, Palo Alto, CA. Email: [email protected] Classification Biological Sciences/Genetics Keywords Kleine-Levin Syndrome, KLS, Bipolar disorder, Schizophrenia, TRANK1, Birth Difficulties Author Contributions Aditya Ambati - analysis, interpretation of the data, input on the manuscript, manuscript writing Ryan Hillary - analysis, interpretation of the data, input on the manuscript, manuscript writing Smaranda Leu-Semenescu - analysis, interpretation of the data, input on the manuscript, manuscript writing Hanna M. Ollila- analysis, interpretation of the data, input on the manuscript Ling Lin- analysis, interpretation of the data, input on the manuscript Emmanuel During- acquisition of data Neal Farber- acquisition of data, interpretation of the data, input on the manuscript. Thomas J Rico- acquisition of data Juliette Faraco - acquisition of data Eileen Leary - acquisition of data Andrea Goldstein-Piekarski – input on manuscript Yu-Shu Huang - acquisition of data Fang Han - acquisition of data Yakov Sivan - acquisition of data Michel Lecendreux - acquisition of data Pauline Dodet - acquisition of data Makoto Honda - acquisition of data Natan Gadoth - acquisition of data Sona Nevsimalova - acquisition of data Fabio Pizza - acquisition of data. Takashi Kanbayahsi- acquisition of data Rosa Peraita Adrados- acquisition of data Guy Leschziner - acquisition of data Rosa Hasan- acquisition of data Francesca Canellas- acquisition of data Kazuhiko Kume- acquisition of data Makrina Daniilidou- acquisition of data 2 medRxiv preprint doi: https://doi.org/10.1101/2021.01.08.20249006; this version posted January 16, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license . Patrice Bourgin- acquisition of data David Rye- acquisition of data José L Vicario- acquisition of data Birgit Högl- acquisition of data Seung Chul Hong- acquisition of data Guiseppe Plazzi- acquisition of data Geert Mayer- acquisition of data Anne Marie Landtblom- acquisition of data Yves Dauvilliers- acquisition of data Isabelle Arnulf- acquisition of data, analysis, and interpretation of data, input on the manuscript. Emmanuel Mignot- acquisition of data, analysis, and interpretation of data, manuscript writing, study supervision This PDF file includes: Main Text –10835 words Figures 1 to 4 Tables 1 to 4 Supplementary Appendix Abstract Kleine-Levin Syndrome (KLS) is a rare disorder characterized by severe episodic hypersomnia, with cognitive impairment accompanied by apathy or disinhibition. Pathophysiology is unknown, although imaging studies indicate decreased activity in hypothalamic/thalamic areas during episodes. Familial occurrence is increased, and risk is associated with reports of a difficult birth. We conducted a worldwide case-control genome wide association study in 673 KLS cases collected over 14 years, and ethnically matched 15,341 control individuals. We found a strong genome-wide significant association (OR=1.48,rs71947865,p=8.6x10-9) with 20 single nucleotide polymorphisms encompassing a 35kb region located in the 3’ region of TRANK1 gene, previously associated with bipolar disorder and schizophrenia. Strikingly, KLS cases with TRANK1 rs71947865 variant had significantly increased reports of a difficult birth. As perinatal outcomes have dramatically improved over the last 40 years, we further stratified our sample by birth years and found that recent cases had a significantly reduced TRANK1 rs71947865 association. While theTRANK1 rs71947865 association did not replicate in the entire follow-up sample of 171 KLS cases, the TRANK1 rs71947865 was significantly associated with KLS in the subset follow-up sample of 59 KLS cases who reported birth difficulties (OR=1.54;p=0.01). Genetic liability of KLS as explained by polygenic risk scores was increased (pseudo r2=0.15;p<2.0x10-22 at p=0.5 threshold) in the follow-up sample. Pathway analysis of genetic associations identified enrichment of circadian regulation pathway genes in KLS cases. Our results suggest links between KLS, behavioral rhythmicity, and bipolar disorder, and indicates that the TRANK1 polymorphisms in conjunction with reported birth difficulties may predispose to KLS. Significance Statement Genetic markers in TRANK1 gene and its vicinity have been weakly associated with bipolar disorder and
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