Meta-Analysis

. 2022 Jun 2;109(6):1077-1091.

doi: 10.1016/j.ajhg.2022.04.010. Epub 2022 May 16.

Genome-wide association meta-analysis identifies 48 risk variants and highlights the role of the stria vascularis in hearing loss

Natalia Trpchevska¹, Maxim B Freidin², Linda Broer³, Berthe C Oosterloo⁴, Shuyang Yao⁵, Yitian Zhou¹, Barbara Vona⁶, Charles Bishop⁷, Argyro Bizaki-Vallaskangas⁸, Barbara Canlon¹, Fabio Castellana⁹, Daniel I Chasman¹⁰, Stacey Cherny¹¹, Kaare Christensen¹², Maria Pina Concas¹³, Adolfo Correa¹⁴, Ran Elkon¹⁵; Estonian Biobank Research Team¹⁶; Jonas Mengel-From¹⁷, Yan Gao¹⁸, Anne B S Giersch¹⁹, Giorgia Girotto²⁰, Alexander Gudjonsson²¹, Vilmundur Gudnason²², Nancy L Heard-Costa²³, Ronna Hertzano²⁴, Jacob V B Hjelmborg²⁵, Jens Hjerling-Leffler²⁶, Howard J Hoffman²⁷, Jaakko Kaprio²⁸, Johannes Kettunen²⁹, Kristi Krebs¹⁶, Anna K Kähler⁵, Francois Lallemend³⁰, Lenore J Launer³¹, I-Min Lee³², Hampton Leonard³³, Chuan-Ming Li²⁷, Hubert Lowenheim³⁴, Patrik K E Magnusson⁵, Joyce van Meurs³, Lili Milani¹⁶, Cynthia C Morton³⁵, Antti Mäkitie³⁶, Mike A Nalls³³, Giuseppe Giovanni Nardone¹³, Marianne Nygaard¹⁷, Teemu Palviainen²⁸, Sheila Pratt³⁷, Nicola Quaranta³⁸, Joel Rämö²⁸, Elmo Saarentaus²⁸, Rodolfo Sardone⁹, Claudia L Satizabal³⁹, John M Schweinfurth⁷, Sudha Seshadri³⁹, Eric Shiroma⁴⁰, Eldad Shulman¹⁵, Eleanor Simonsick⁴¹, Christopher Spankovich⁷, Anke Tropitzsch³⁴, Volker M Lauschke¹, Patrick F Sullivan⁴², Andre Goedegebure⁴, Christopher R Cederroth⁴³, Frances M K Williams², Andries Paul Nagtegaal⁴

Collaborators, Affiliations

Collaborators

Estonian Biobank Research Team:
Andres Metspalu, Mari Nelis, Reedik Mägi, Tõnu Esko

Affiliations

¹ Department of Physiology and Pharmacology, Karolinska Institutet, 17177 Stockholm, Sweden.
² Department of Twin Research and Genetic Epidemiology, King's College London, London, UK.
³ Department of Internal Medicine, Erasmus Medical Center, 3015 CE Rotterdam, the Netherlands.
⁴ Department of Otorhinolaryngology, Erasmus Medical Center, 3015 CE Rotterdam, the Netherlands.
⁵ Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, 17177 Stockholm, Sweden.
⁶ Institute of Human Genetics, University Medical Center Göttingen, 37073 Göttingen, Germany; Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, 37075 Göttingen, Germany; Department of Otolaryngology-Head & Neck Surgery, University of Tübingen Medical Center, 72076 Tübingen, Germany.
⁷ Department of Otolaryngology and Communicative Sciences, The University of Mississippi Medical Center, Jackson, MS 39216, USA.
⁸ Department of Otolaryngology, University of Tampere, 33100 Tampere, Finland; Pirkanmaan Sairaanhoitopiiri, 33520 Tampere, Finland.
⁹ Unit of Data Sciences and Technology Innovation for Population Health, National Institute of Gastroenterology "Saverio de Bellis", Research Hospital, Castellana Grotte, 70124 Bari, Italy.
¹⁰ Division of Preventative Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA; Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.
¹¹ Department of Anatomy and Anthropology and Department of Epidemiology and Preventive Medicine, Sackler Faculty of Medicine, Tel Aviv University, 69978 Tel Aviv, Israel.
¹² The Danish Twin Registry, Department of Public Health, University of Southern Denmark, 5000 Odense C, Denmark; Department of Clinical Genetics, Odense University Hospital, 5000 Odense C, Denmark; Department of Clinical Biochemistry and Pharmacology, Odense University Hospital, 5000 Odense C, Denmark.
¹³ Institute for Maternal and Child Health - IRCCS, Burlo Garofolo, 34127 Trieste, Italy.
¹⁴ Jackson Heart Study, The University of Mississippi Medical Center, Jackson, MS 39216, USA.
¹⁵ Department of Human Molecular Genetics & Biochemistry, Sackler School of Medicine, Tel Aviv University, 69978 Tel Aviv, Israel.
¹⁶ Estonian Genome Centre, Institute of Genomics, University of Tartu, Tartu, Estonia.
¹⁷ The Danish Twin Registry, Department of Public Health, University of Southern Denmark, 5000 Odense C, Denmark; Department of Clinical Genetics, Odense University Hospital, 5000 Odense C, Denmark.
¹⁸ Jackson Heart Study, The University of Mississippi Medical Center, Jackson, MS 39216, USA; Department of Population Health Science, University of Mississippi Medical Center, Jackson, MS 39216, USA.
¹⁹ Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.
²⁰ Institute for Maternal and Child Health - IRCCS, Burlo Garofolo, 34127 Trieste, Italy; Department of Medicine, Surgery and Health Sciences, University of Trieste, 34139 Trieste, Italy.
²¹ Icelandic Heart Association, 201 Kopavogur, Iceland.
²² Icelandic Heart Association, 201 Kopavogur, Iceland; Faculty of Medicine, University of Iceland, 101 Reykjavik, Iceland.
²³ Department of Neurology, Boston University School of Medicine, Boston, MA 02118, USA; Framingham Heart Study, Framingham, MA 01702, USA.
²⁴ Department of Otorhinolaryngology-Head and Neck Surgery, University of Maryland Baltimore, Baltimore, MD 21201, USA; Department of Anatomy and Neurobiology, University of Maryland Baltimore, Baltimore, MD 21201, USA; Institute for Genome Sciences, University of Maryland Baltimore, Baltimore, MD 21201, USA.
²⁵ The Danish Twin Registry, Department of Public Health, University of Southern Denmark, 5000 Odense C, Denmark.
²⁶ Department of Medical Biochemistry and Biophysics, Karolinska Institutet, 17177 Stockholm, Sweden.
²⁷ Division of Scientific Programs, Epidemiology and Statistics Program, National Institute on Deafness and Other Communications Disorders (NIDCD), NIH, Bethesda, MD 20892, USA.
²⁸ Institute for Molecular Medicine Finland (FIMM), University of Helsinki, 00014 Helsinki, Finland.
²⁹ Computational Medicine, Center for Life Course Health Research, Faculty of Medicine, University of Oulu, 90220 Oulu, Finland; Biocenter Oulu, University of Oulu, 90220 Oulu, Finland; Finnish Institute for Health and Welfare, 00271 Helsinki, Finland.
³⁰ Department of Neuroscience, Karolinska Institutet, 17177 Stockholm, Sweden.
³¹ Laboratory of Epidemiology and Population Sciences, Intramural Research Program National Institute on Aging, Bethesda, MD 20892, USA.
³² Division of Preventative Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.
³³ Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, MD 20892, USA; Center for Alzheimer's and Related Dementias, National Institutes of Health, Bethesda, MD 20892, USA; Data Tecnica International, Glen Echo, MD 20812, USA.
³⁴ Department of Otolaryngology-Head & Neck Surgery, University of Tübingen Medical Center, 72076 Tübingen, Germany.
³⁵ Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Department of Obstetrics and Gynecology and of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA; Manchester Centre for Audiology and Deafness, University of Manchester, Manchester M13 9PL, UK.
³⁶ Department of Otorhinolaryngology - Head and Neck Surgery, University of Helsinki and Helsinki University Hospital, 00029 Helsinki, Finland.
³⁷ Department of Communication Science & Disorders, University of Pittsburgh, Pittsburgh, PA 15260, USA.
³⁸ Otolaryngology Unit, Department of Basic Medical Science, Neuroscience and Sense Organs, University of Bari Aldo Moro, 70121 Bari, Italy.
³⁹ Department of Neurology, Boston University School of Medicine, Boston, MA 02118, USA; Framingham Heart Study, Framingham, MA 01702, USA; Glenn Biggs Institute for Alzheimer's & Neurodegenerative Diseases and Department of Population Health Sciences, University of Texas Health Sciences Center, San Antonio, TX 78229, USA.
⁴⁰ Laboratory of Epidemiology and Population Sciences, National Institute on Aging, Baltimore, MD 21224, USA.
⁴¹ Longitudinal Studies Section, Translational Gerontology Branch, National Institute on Aging, Baltimore, MD 21224, USA.
⁴² Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, 17177 Stockholm, Sweden; Department of Genetics, University of North Carolina, Chapel Hill, NC 27516, USA.
⁴³ Department of Physiology and Pharmacology, Karolinska Institutet, 17177 Stockholm, Sweden; National Institute for Health Research (NIHR) Nottingham Biomedical Research Centre, Nottingham University Hospitals NHS Trust, Ropewalk House, NG1 5DU Nottingham, UK; Hearing Sciences, Division of Clinical Neuroscience, School of Medicine, University of Nottingham, NG7 2UH Nottingham, UK. Electronic address: christopher.cederroth@ki.se.

PMID: 35580588
PMCID: PMC9247887
DOI: 10.1016/j.ajhg.2022.04.010

Meta-Analysis

Genome-wide association meta-analysis identifies 48 risk variants and highlights the role of the stria vascularis in hearing loss

Natalia Trpchevska et al. Am J Hum Genet. 2022.

. 2022 Jun 2;109(6):1077-1091.

doi: 10.1016/j.ajhg.2022.04.010. Epub 2022 May 16.

Authors

Collaborators

Estonian Biobank Research Team:
Andres Metspalu, Mari Nelis, Reedik Mägi, Tõnu Esko

Affiliations

¹ Department of Physiology and Pharmacology, Karolinska Institutet, 17177 Stockholm, Sweden.
² Department of Twin Research and Genetic Epidemiology, King's College London, London, UK.
³ Department of Internal Medicine, Erasmus Medical Center, 3015 CE Rotterdam, the Netherlands.
⁴ Department of Otorhinolaryngology, Erasmus Medical Center, 3015 CE Rotterdam, the Netherlands.
⁵ Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, 17177 Stockholm, Sweden.
⁶ Institute of Human Genetics, University Medical Center Göttingen, 37073 Göttingen, Germany; Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, 37075 Göttingen, Germany; Department of Otolaryngology-Head & Neck Surgery, University of Tübingen Medical Center, 72076 Tübingen, Germany.
⁷ Department of Otolaryngology and Communicative Sciences, The University of Mississippi Medical Center, Jackson, MS 39216, USA.
⁸ Department of Otolaryngology, University of Tampere, 33100 Tampere, Finland; Pirkanmaan Sairaanhoitopiiri, 33520 Tampere, Finland.
⁹ Unit of Data Sciences and Technology Innovation for Population Health, National Institute of Gastroenterology "Saverio de Bellis", Research Hospital, Castellana Grotte, 70124 Bari, Italy.
¹⁰ Division of Preventative Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA; Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.
¹¹ Department of Anatomy and Anthropology and Department of Epidemiology and Preventive Medicine, Sackler Faculty of Medicine, Tel Aviv University, 69978 Tel Aviv, Israel.
¹² The Danish Twin Registry, Department of Public Health, University of Southern Denmark, 5000 Odense C, Denmark; Department of Clinical Genetics, Odense University Hospital, 5000 Odense C, Denmark; Department of Clinical Biochemistry and Pharmacology, Odense University Hospital, 5000 Odense C, Denmark.
¹³ Institute for Maternal and Child Health - IRCCS, Burlo Garofolo, 34127 Trieste, Italy.
¹⁴ Jackson Heart Study, The University of Mississippi Medical Center, Jackson, MS 39216, USA.
¹⁵ Department of Human Molecular Genetics & Biochemistry, Sackler School of Medicine, Tel Aviv University, 69978 Tel Aviv, Israel.
¹⁶ Estonian Genome Centre, Institute of Genomics, University of Tartu, Tartu, Estonia.
¹⁷ The Danish Twin Registry, Department of Public Health, University of Southern Denmark, 5000 Odense C, Denmark; Department of Clinical Genetics, Odense University Hospital, 5000 Odense C, Denmark.
¹⁸ Jackson Heart Study, The University of Mississippi Medical Center, Jackson, MS 39216, USA; Department of Population Health Science, University of Mississippi Medical Center, Jackson, MS 39216, USA.
¹⁹ Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.
²⁰ Institute for Maternal and Child Health - IRCCS, Burlo Garofolo, 34127 Trieste, Italy; Department of Medicine, Surgery and Health Sciences, University of Trieste, 34139 Trieste, Italy.
²¹ Icelandic Heart Association, 201 Kopavogur, Iceland.
²² Icelandic Heart Association, 201 Kopavogur, Iceland; Faculty of Medicine, University of Iceland, 101 Reykjavik, Iceland.
²³ Department of Neurology, Boston University School of Medicine, Boston, MA 02118, USA; Framingham Heart Study, Framingham, MA 01702, USA.
²⁴ Department of Otorhinolaryngology-Head and Neck Surgery, University of Maryland Baltimore, Baltimore, MD 21201, USA; Department of Anatomy and Neurobiology, University of Maryland Baltimore, Baltimore, MD 21201, USA; Institute for Genome Sciences, University of Maryland Baltimore, Baltimore, MD 21201, USA.
²⁵ The Danish Twin Registry, Department of Public Health, University of Southern Denmark, 5000 Odense C, Denmark.
²⁶ Department of Medical Biochemistry and Biophysics, Karolinska Institutet, 17177 Stockholm, Sweden.
²⁷ Division of Scientific Programs, Epidemiology and Statistics Program, National Institute on Deafness and Other Communications Disorders (NIDCD), NIH, Bethesda, MD 20892, USA.
²⁸ Institute for Molecular Medicine Finland (FIMM), University of Helsinki, 00014 Helsinki, Finland.
²⁹ Computational Medicine, Center for Life Course Health Research, Faculty of Medicine, University of Oulu, 90220 Oulu, Finland; Biocenter Oulu, University of Oulu, 90220 Oulu, Finland; Finnish Institute for Health and Welfare, 00271 Helsinki, Finland.
³⁰ Department of Neuroscience, Karolinska Institutet, 17177 Stockholm, Sweden.
³¹ Laboratory of Epidemiology and Population Sciences, Intramural Research Program National Institute on Aging, Bethesda, MD 20892, USA.
³² Division of Preventative Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.
³³ Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, MD 20892, USA; Center for Alzheimer's and Related Dementias, National Institutes of Health, Bethesda, MD 20892, USA; Data Tecnica International, Glen Echo, MD 20812, USA.
³⁴ Department of Otolaryngology-Head & Neck Surgery, University of Tübingen Medical Center, 72076 Tübingen, Germany.
³⁵ Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Department of Obstetrics and Gynecology and of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA; Manchester Centre for Audiology and Deafness, University of Manchester, Manchester M13 9PL, UK.
³⁶ Department of Otorhinolaryngology - Head and Neck Surgery, University of Helsinki and Helsinki University Hospital, 00029 Helsinki, Finland.
³⁷ Department of Communication Science & Disorders, University of Pittsburgh, Pittsburgh, PA 15260, USA.
³⁸ Otolaryngology Unit, Department of Basic Medical Science, Neuroscience and Sense Organs, University of Bari Aldo Moro, 70121 Bari, Italy.
³⁹ Department of Neurology, Boston University School of Medicine, Boston, MA 02118, USA; Framingham Heart Study, Framingham, MA 01702, USA; Glenn Biggs Institute for Alzheimer's & Neurodegenerative Diseases and Department of Population Health Sciences, University of Texas Health Sciences Center, San Antonio, TX 78229, USA.
⁴⁰ Laboratory of Epidemiology and Population Sciences, National Institute on Aging, Baltimore, MD 21224, USA.
⁴¹ Longitudinal Studies Section, Translational Gerontology Branch, National Institute on Aging, Baltimore, MD 21224, USA.
⁴² Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, 17177 Stockholm, Sweden; Department of Genetics, University of North Carolina, Chapel Hill, NC 27516, USA.
⁴³ Department of Physiology and Pharmacology, Karolinska Institutet, 17177 Stockholm, Sweden; National Institute for Health Research (NIHR) Nottingham Biomedical Research Centre, Nottingham University Hospitals NHS Trust, Ropewalk House, NG1 5DU Nottingham, UK; Hearing Sciences, Division of Clinical Neuroscience, School of Medicine, University of Nottingham, NG7 2UH Nottingham, UK. Electronic address: christopher.cederroth@ki.se.

PMID: 35580588
PMCID: PMC9247887
DOI: 10.1016/j.ajhg.2022.04.010

Abstract

Hearing loss is one of the top contributors to years lived with disability and is a risk factor for dementia. Molecular evidence on the cellular origins of hearing loss in humans is growing. Here, we performed a genome-wide association meta-analysis of clinically diagnosed and self-reported hearing impairment on 723,266 individuals and identified 48 significant loci, 10 of which are novel. A large proportion of associations comprised missense variants, half of which lie within known familial hearing loss loci. We used single-cell RNA-sequencing data from mouse cochlea and brain and mapped common-variant genomic results to spindle, root, and basal cells from the stria vascularis, a structure in the cochlea necessary for normal hearing. Our findings indicate the importance of the stria vascularis in the mechanism of hearing impairment, providing future paths for developing targets for therapeutic intervention in hearing loss.

Keywords: ARHL; GWAS; basal cells; cochlea; genetics; hair cells; hearing loss; root cells; spindle cells; stria vascularis.

PubMed Disclaimer

Conflict of interest statement

Declaration of interests The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. C.R.C. is supported by the UK National Institute for Health Research (NIHR) Biomedical Research Center but the views expressed herein are his own and do not represent those of NIHR nor the UK Department of Health and Social Care. Y.Z. and V.M.L. are co-founders and shareholders of PersoMedix AB. In addition, V.M.L. is CEO and shareholder of HepaPredict AB and discloses support by the Robert Bosch Foundation, Merck KGaA, and Eli Lilly and Company. J.H.L. is co-founder and share-holder of Oscellaria AB. H.L. receives support from a consulting contract between Data Tecnica International and the National Institute on Aging (NIA), National Institutes of Health (NIH). M.A.N. received a competitive contract awarded to Data Tecnica International LLC by the National Institutes of Health to support open science research, and he also currently serves on the scientific advisory board for Clover Therapeutics and is an advisor to Neuron23 Inc as a data science fellow. P.F.S. is consultant and shareholder of Neumora.

Figures

**Figure 1**
GWAS meta-analysis for ARHI (n = 723,266) (A) Origin of the datasets used for the meta-analysis of the ARHI GWAS: 8 European countries and the United States. (B) Manhattan plot displays all associations per variant ordered according to their genomic position on the x axis and showing the strength of the association with the −log₁₀ transformed p values on the y axis. The threshold for genome-wide significance (p < 5 × 10⁻⁸) is indicated by the red line, while the blue line represents the suggestive threshold (p < 1 × 10⁻⁵).

**Figure 2**
Evaluation of enrichment of common-variant hearing loss GWAS results in scRNA-seq mouse datasets Schematic of the mouse cochlea (A) and the mouse brain (B) regions used for the enrichment analysis. Abbreviations: Amg, amygdala; Cbx, cerebellum; Ctx, cerebral cortex; DC, Deiters’ cells; Hi, hippocampus; Hy, hypothalamus; IHC, inner hair cells; Mb, midbrain; My, medulla; OB, olfactory bulb; OC, organ of Corti; OHC, outer hair cells; P, pons; Sc, spinal cord; Str, striatum; Th, thalamus. OC is magnified in box 1 and illustrates the IHC, OHC, and DC, whose enrichment is shown in (C). A color box links a specific cell to the schematic. The red line is the Bonferroni significance threshold (−log₁₀ p value 1.77). The enrichment analysis using cells from the stria vascularis (box 2) and the spiral ganglion neuron region (box 3) reveals a significant enrichment for spindle root cells and basal cells (D). All type 1 spiral ganglion neurons (type 1a, b, c) were all labeled the same color for sake of clarity. Given the broad and scarce distribution of immune cells (monocytes, neutrophils, and B cells), these are not shown on the schematic. The red line shows the Bonferroni significance threshold (−log₁₀ p value 2.42) (E). Mouse nervous system cell type enrichment showing no significant enrichment. The red line shows the Bonferroni significance threshold (−log₁₀ p value 2.89). Images from (A) and (B) were reproduced from previous work, , with permission from Nature Springer.

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Genome-wide association meta-analysis identifies 48 risk variants and highlights the role of the stria vascularis in hearing loss

Collaborators

Affiliations

Genome-wide association meta-analysis identifies 48 risk variants and highlights the role of the stria vascularis in hearing loss

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Abstract

Conflict of interest statement

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