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X-chromosome and kidney function: evidence from a multi-trait genetic analysis of 908,697 individuals reveals sex-specific and sex-differential findings in genes regulated by androgen response elements

Author

Listed:
  • Markus Scholz

    (Statistics and Epidemiology, University of Leipzig
    University of Leipzig)

  • Katrin Horn

    (Statistics and Epidemiology, University of Leipzig
    University of Leipzig)

  • Janne Pott

    (Statistics and Epidemiology, University of Leipzig
    University of Leipzig)

  • Matthias Wuttke

    (Faculty of Medicine and Medical Center–University of Freiburg
    University of Freiburg)

  • Andreas Kühnapfel

    (Statistics and Epidemiology, University of Leipzig
    University of Leipzig)

  • M. Kamal Nasr

    (University Medicine Greifswald
    partner site Greifswald
    University Medicine Greifswald)

  • Holger Kirsten

    (Statistics and Epidemiology, University of Leipzig
    University of Leipzig)

  • Yong Li

    (Faculty of Medicine and Medical Center–University of Freiburg)

  • Anselm Hoppmann

    (Faculty of Medicine and Medical Center–University of Freiburg)

  • Mathias Gorski

    (University of Regensburg
    University Hospital Regensburg)

  • Sahar Ghasemi

    (University Medicine Greifswald
    partner site Greifswald)

  • Man Li

    (University of Utah)

  • Adrienne Tin

    (University of Mississippi Medical Center
    University of Mississippi Medical Center)

  • Jin-Fang Chai

    (National University of Singapore and National University Health System)

  • Massimiliano Cocca

    (IRCCS ‘Burlo Garofolo’)

  • Judy Wang

    (Washington University School of Medicine)

  • Teresa Nutile

    (Institute of Genetics and Biophysics ‘Adriano Buzzati-Traverso’-CNR)

  • Masato Akiyama

    (RIKEN Center for Integrative Medical Sciences (IMS)
    Kyushu University)

  • Bjørn Olav Åsvold

    (Norwegian University of Science and Technology
    Trondheim University Hospital)

  • Nisha Bansal

    (University of Washington
    University of Washington)

  • Mary L. Biggs

    (University of Washington
    University of Washington)

  • Thibaud Boutin

    (University of Edinburgh)

  • Hermann Brenner

    (German Cancer Research Center (DKFZ)
    Heidelberg University)

  • Ben Brumpton

    (Norwegian University of Science and Technology
    University of Bristol
    Trondheim University Hospital)

  • Ralph Burkhardt

    (University of Leipzig
    University Hospital Regensburg)

  • Jianwen Cai

    (University of North Carolina at Chapel Hill)

  • Archie Campbell

    (University of Edinburgh)

  • Harry Campbell

    (University of Edinburgh, Teviot Place)

  • John Chalmers

    (University of New South Wales)

  • Daniel I. Chasman

    (Brigham and Women’s Hospital
    Harvard Medical School)

  • Miao Ling Chee

    (Singapore National Eye Center)

  • Miao Li Chee

    (Singapore National Eye Center)

  • Xu Chen

    (Karolinska Institutet)

  • Ching-Yu Cheng

    (Singapore National Eye Center
    Duke-NUS Medical School
    National University of Singapore and National University Health System)

  • Renata Cifkova

    (Charles University in Prague, First Faculty of Medicine and Thomayer University Hospital
    Charles University in Prague, First Faculty of Medicine)

  • Martha Daviglus

    (University of Illinois at Chicago)

  • Graciela Delgado

    (University of Heidelberg)

  • Katalin Dittrich

    (University of Leipzig)

  • Todd L. Edwards

    (Tennessee Valley Healthcare System (626)/Vanderbilt University
    Vanderbilt University Medical Center)

  • Karlhans Endlich

    (partner site Greifswald
    University Medicine Greifswald)

  • J. Michael Gaziano

    (VA Boston Healthcare System)

  • Ayush Giri

    (Vanderbilt University Medical Center
    Tennessee Valley Healthcare System (626)/Vanderbilt University)

  • Franco Giulianini

    (Brigham and Women’s Hospital)

  • Scott D. Gordon

    (QIMR Berghofer Medical Research Institute)

  • Daniel F. Gudbjartsson

    (deCODE Genetics/Amgen, Inc.
    University of Iceland)

  • Stein Hallan

    (Norwegian University of Science and Technology
    Trondheim University Hospital)

  • Pavel Hamet

    (Montreal University Hospital Research Center, CHUM
    Medpharmgene)

  • Catharina A. Hartman

    (University of Groningen, University Medical Center Groningen)

  • Caroline Hayward

    (University of Edinburgh)

  • Iris M. Heid

    (University of Regensburg)

  • Jacklyn N. Hellwege

    (Tennessee Valley Healthcare System (626)/Vanderbilt University
    Vanderbilt University Medical Center
    Vanderbilt University Medical Center)

  • Bernd Holleczek

    (German Cancer Research Center (DKFZ))

  • Hilma Holm

    (deCODE Genetics/Amgen, Inc.)

  • Nina Hutri-Kähönen

    (Tampere University)

  • Kristian Hveem

    (Norwegian University of Science and Technology)

  • Berend Isermann

    (University of Leipzig
    University of Leipzig)

  • Jost B. Jonas

    (University Heidelberg
    Capital Medical University
    Institute of Molecular and Clinical Ophthalmology
    Privatpraxis Prof Jonas und Dr Panda-Jonas)

  • Peter K. Joshi

    (University of Edinburgh, Teviot Place)

  • Yoichiro Kamatani

    (RIKEN Center for Integrative Medical Sciences (IMS)
    The University of Tokyo)

  • Masahiro Kanai

    (RIKEN Center for Integrative Medical Sciences (IMS)
    Broad Institute of Harvard and MIT
    Harvard Medical School)

  • Mika Kastarinen

    (Finnish Medicines Agency)

  • Chiea Chuen Khor

    (Agency for Science Technology and Research
    National University of Singapore and National University Health System)

  • Wieland Kiess

    (University of Leipzig
    University of Leipzig)

  • Marcus E. Kleber

    (University of Heidelberg
    SYNLAB MVZ Humangenetik Mannheim)

  • Antje Körner

    (University of Leipzig
    University of Leipzig
    Helmholtz Institute for Metabolic, Obesity and Vascular Research (HI-MAG) of the Helmholtz Zentrum München at the University of Leipzig and University Hospital Leipzig)

  • Peter Kovacs

    (University of Leipzig)

  • Alena Krajcoviechova

    (Charles University in Prague, First Faculty of Medicine and Thomayer University Hospital)

  • Holly Kramer

    (Loyola University Chicago
    Loyola University Chicago)

  • Bernhard K. Krämer

    (University of Heidelberg)

  • Mikko Kuokkanen

    (Finnish Institute for Health and Welfare
    University of Helsinki
    University of Texas Rio Grande Valley School of Medicine)

  • Mika Kähönen

    (Tampere University Hospital
    Tampere University)

  • Leslie A. Lange

    (University of Colorado Denver-Anschutz Medical Campus)

  • James P. Lash

    (University of Illinois at Chicago)

  • Terho Lehtimäki

    (Fimlab Laboratories, and The Wellbeing Services County of Pirkanmaa
    Tampere University)

  • Hengtong Li

    (National University of Singapore and National University Health System)

  • Bridget M. Lin

    (University of North Carolina at Chapel Hill)

  • Jianjun Liu

    (Agency for Science Technology and Research
    National University of Singapore and National University Health System)

  • Markus Loeffler

    (Statistics and Epidemiology, University of Leipzig
    University of Leipzig)

  • Leo-Pekka Lyytikäinen

    (Fimlab Laboratories, and The Wellbeing Services County of Pirkanmaa
    Tampere University)

  • Patrik K. E. Magnusson

    (Karolinska Institutet)

  • Nicholas G. Martin

    (QIMR Berghofer Medical Research Institute)

  • Koichi Matsuda

    (The University of Tokyo)

  • Yuri Milaneschi

    (Amsterdam UMC/Vrije Universiteit and GGZ inGeest)

  • Pashupati P. Mishra

    (Fimlab Laboratories, and The Wellbeing Services County of Pirkanmaa
    Tampere University)

  • Nina Mononen

    (Fimlab Laboratories, and The Wellbeing Services County of Pirkanmaa
    Tampere University)

  • Grant W. Montgomery

    (University of Queensland)

  • Dennis O. Mook-Kanamori

    (Leiden University Medical Center
    Leiden University Medical Center)

  • Josyf C. Mychaleckyj

    (University of Virginia, Charlottesville)

  • Winfried März

    (University of Heidelberg
    Medical University Graz
    Synlab Holding Deutschland GmbH)

  • Matthias Nauck

    (partner site Greifswald
    University Medicine Greifswald)

  • Kjell Nikus

    (Tampere University Hospital
    Tampere University)

  • Ilja M. Nolte

    (University of Groningen, University Medical Center Groningen)

  • Raymond Noordam

    (Leiden University Medical Center)

  • Yukinori Okada

    (RIKEN Center for Integrative Medical Sciences (IMS)
    Osaka University Graduate School of Medicine
    the University of Tokyo)

  • Isleifur Olafsson

    (Landspitali University Hospital)

  • Albertine J. Oldehinkel

    (University of Groningen, University Medical Center Groningen)

  • Brenda W. J. H. Penninx

    (Amsterdam UMC/Vrije Universiteit and GGZ inGeest)

  • Markus Perola

    (Finnish Institute for Health and Welfare
    University of Helsinki)

  • Nicola Pirastu

    (University of Edinburgh, Teviot Place
    Genomics Research Centre, Human Technopole Palazzo Italia)

  • Ozren Polasek

    (University of Split Medical School)

  • David J. Porteous

    (University of Edinburgh)

  • Tanja Poulain

    (University of Leipzig
    University of Leipzig)

  • Bruce M. Psaty

    (University of Washington)

  • Ton J. Rabelink

    (Leiden University Medical Center
    Leiden University Medical Center)

  • Laura M. Raffield

    (University of North Carolina)

  • Olli T. Raitakari

    (University of Turku and Turku University Hospital
    Turku University Hospital
    University of Turku)

  • Humaira Rasheed

    (Norwegian University of Science and Technology
    University of Bristol
    University of Oslo)

  • Dermot F. Reilly

    (Janssen Pharmaceuticals Inc.)

  • Kenneth M. Rice

    (University of Washington)

  • Anne Richmond

    (University of Edinburgh)

  • Paul M. Ridker

    (Brigham and Women’s Hospital
    Harvard Medical School)

  • Jerome I. Rotter

    (The Lundquist Institute for Biomedical Innovation at Harbor-UCLA Medical Center)

  • Igor Rudan

    (University of Edinburgh, Teviot Place)

  • Charumathi Sabanayagam

    (Singapore National Eye Center
    Duke-NUS Medical School)

  • Veikko Salomaa

    (Finnish Institute for Health and Welfare)

  • Neil Schneiderman

    (University of Miami)

  • Ben Schöttker

    (German Cancer Research Center (DKFZ)
    Heidelberg University)

  • Mario Sims

    (University of California at Riverside School of Medicine)

  • Harold Snieder

    (University of Groningen, University Medical Center Groningen)

  • Klaus J. Stark

    (University of Regensburg)

  • Kari Stefansson

    (deCODE Genetics/Amgen, Inc.
    University of Iceland)

  • Hannah Stocker

    (German Cancer Research Center (DKFZ)
    Heidelberg University)

  • Michael Stumvoll

    (University of Leipzig)

  • Patrick Sulem

    (deCODE Genetics/Amgen, Inc.)

  • Gardar Sveinbjornsson

    (deCODE Genetics/Amgen, Inc.)

  • Per O. Svensson

    (Karolinska Institutet
    Södersjukhuset)

  • E-Shyong Tai

    (National University of Singapore and National University Health System
    National University of Singapore and National University Health System
    Duke-NUS Medical School)

  • Kent D. Taylor

    (The Lundquist Institute for Biomedical Innovation at Harbor-UCLA Medical Center)

  • Bamidele O. Tayo

    (Loyola University Chicago)

  • Andrej Teren

    (University of Leipzig
    University Hospital OWL of Bielefeld University, Campus Klinikum Bielefeld)

  • Yih-Chung Tham

    (Singapore National Eye Center
    National University of Singapore and National University Health System)

  • Joachim Thiery

    (University of Leipzig
    University of Leipzig)

  • Chris H. L. Thio

    (University of Groningen, University Medical Center Groningen)

  • Laurent F. Thomas

    (Norwegian University of Science and Technology
    Norwegian University of Science and Technology
    Norwegian University of Science and Technology
    Trondheim University Hospital)

  • Johanne Tremblay

    (Montreal University Hospital Research Center, CHUM)

  • Anke Tönjes

    (University of Leipzig)

  • Peter J. Most

    (University of Groningen, University Medical Center Groningen)

  • Veronique Vitart

    (University of Edinburgh)

  • Uwe Völker

    (partner site Greifswald
    University Medicine Greifswald)

  • Ya Xing Wang

    (Capital Medical University)

  • Chaolong Wang

    (Agency for Science Technology and Research
    Huazhong University of Science and Technology)

  • Wen Bin Wei

    (Capital Medical University)

  • John B. Whitfield

    (QIMR Berghofer Medical Research Institute)

  • Sarah H. Wild

    (University of Edinburgh, Teviot Place)

  • James F. Wilson

    (University of Edinburgh
    University of Edinburgh, Teviot Place)

  • Thomas W. Winkler

    (University of Regensburg)

  • Tien-Yin Wong

    (Singapore National Eye Center
    Duke-NUS Medical School
    Tsinghua University)

  • Mark Woodward

    (University of New South Wales
    Imperial College London)

  • Xueling Sim

    (National University of Singapore and National University Health System)

  • Audrey Y. Chu

    (Genetics, Merck & Co., Inc)

  • Mary F. Feitosa

    (Washington University School of Medicine)

  • Unnur Thorsteinsdottir

    (deCODE Genetics/Amgen, Inc.
    University of Iceland)

  • Adriana M. Hung

    (Tennessee Valley Healthcare System (626)/Vanderbilt University
    Division of Nephrology & Hypertension)

  • Alexander Teumer

    (University Medicine Greifswald
    partner site Greifswald
    University Medicine Greifswald
    Medical University of Bialystok)

  • Nora Franceschini

    (University of North Carolina at Chapel Hill)

  • Afshin Parsa

    (National Institutes of Health)

  • Anna Köttgen

    (Faculty of Medicine and Medical Center–University of Freiburg
    Johns Hopkins Bloomberg School of Public Health)

  • Pascal Schlosser

    (Faculty of Medicine and Medical Center–University of Freiburg
    Johns Hopkins Bloomberg School of Public Health)

  • Cristian Pattaro

    (Eurac Research, Institute for Biomedicine (affiliated with the University of Lübeck))

Abstract

X-chromosomal genetic variants are understudied but can yield valuable insights into sexually dimorphic human traits and diseases. We performed a sex-stratified cross-ancestry X-chromosome-wide association meta-analysis of seven kidney-related traits (n = 908,697), identifying 23 loci genome-wide significantly associated with two of the traits: 7 for uric acid and 16 for estimated glomerular filtration rate (eGFR), including four novel eGFR loci containing the functionally plausible prioritized genes ACSL4, CLDN2, TSPAN6 and the female-specific DRP2. Further, we identified five novel sex-interactions, comprising male-specific effects at FAM9B and AR/EDA2R, and three sex-differential findings with larger genetic effect sizes in males at DCAF12L1 and MST4 and larger effect sizes in females at HPRT1. All prioritized genes in loci showing significant sex-interactions were located next to androgen response elements (ARE). Five ARE genes showed sex-differential expressions. This study contributes new insights into sex-dimorphisms of kidney traits along with new prioritized gene targets for further molecular research.

Suggested Citation

  • Markus Scholz & Katrin Horn & Janne Pott & Matthias Wuttke & Andreas Kühnapfel & M. Kamal Nasr & Holger Kirsten & Yong Li & Anselm Hoppmann & Mathias Gorski & Sahar Ghasemi & Man Li & Adrienne Tin & J, 2024. "X-chromosome and kidney function: evidence from a multi-trait genetic analysis of 908,697 individuals reveals sex-specific and sex-differential findings in genes regulated by androgen response element," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-44709-1
    DOI: 10.1038/s41467-024-44709-1
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    as
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