The alternative serotonin transporter promoter P2 impacts gene function in females with irritable bowel syndrome.


Journal

Journal of cellular and molecular medicine
ISSN: 1582-4934
Titre abrégé: J Cell Mol Med
Pays: England
ID NLM: 101083777

Informations de publication

Date de publication:
08 2021
Historique:
revised: 24 05 2021
received: 01 11 2020
accepted: 26 05 2021
pubmed: 25 6 2021
medline: 19 2 2022
entrez: 24 6 2021
Statut: ppublish

Résumé

Irritable bowel syndrome (IBS) is a gut-brain disorder in which symptoms are shaped by serotonin acting centrally and peripherally. The serotonin transporter gene SLC6A4 has been implicated in IBS pathophysiology, but the underlying genetic mechanisms remain unclear. We sequenced the alternative P2 promoter driving intestinal SLC6A4 expression and identified single nucleotide polymorphisms (SNPs) that were associated with IBS in a discovery sample. Identified SNPs built different haplotypes, and the tagging SNP rs2020938 seems to associate with constipation-predominant IBS (IBS-C) in females. rs2020938 validation was performed in 1978 additional IBS patients and 6,038 controls from eight countries. Meta-analysis on data from 2,175 IBS patients and 6,128 controls confirmed the association with female IBS-C. Expression analyses revealed that the P2 promoter drives SLC6A4 expression primarily in the small intestine. Gene reporter assays showed a functional impact of SNPs in the P2 region. In silico analysis of the polymorphic promoter indicated differential expression regulation. Further follow-up revealed that the major allele of the tagging SNP rs2020938 correlates with differential SLC6A4 expression in the jejunum and with stool consistency, indicating functional relevance. Our data consolidate rs2020938 as a functional SNP associated with IBS-C risk in females, underlining the relevance of SLC6A4 in IBS pathogenesis.

Identifiants

pubmed: 34165249
doi: 10.1111/jcmm.16736
pmc: PMC8358858
doi:

Substances chimiques

Biomarkers 0
SLC6A4 protein, human 0
Serotonin Plasma Membrane Transport Proteins 0
Serotonin 333DO1RDJY

Types de publication

Journal Article Multicenter Study Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

8047-8061

Subventions

Organisme : Science Foundation Ireland
ID : SFI/12/RC/2273 P2
Pays : Ireland
Organisme : Health Research Board
ID : POR/2011/23
Pays : Ireland

Informations de copyright

© 2021 The Authors. Journal of Cellular and Molecular Medicine published by Foundation for Cellular and Molecular Medicine and John Wiley & Sons Ltd.

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Auteurs

Sandra Mohr (S)

Department of Human Molecular Genetics, Institute of Human Genetics, Heidelberg University Hospital, Heidelberg, Germany.

Nikola Fritz (N)

Department of Human Molecular Genetics, Institute of Human Genetics, Heidelberg University Hospital, Heidelberg, Germany.

Christian Hammer (C)

Department of Cancer Immunology, Genentech, South San Francisco, CA, USA.
Department of Human Genetics, Genentech, South San Francisco, CA, USA.

Cristina Martínez (C)

Department of Human Molecular Genetics, Institute of Human Genetics, Heidelberg University Hospital, Heidelberg, Germany.
Institut de Recerca Biomèdica de Lleida (IRBLleida), Lleida, Spain.
Lleida Institute for Biomedical Research, Dr. Pifarré Foundation (IRBLleida), Lleida, Spain.

Sabrina Berens (S)

Department of General Internal Medicine and Psychosomatics, Heidelberg University Hospital, Heidelberg, Germany.

Stefanie Schmitteckert (S)

Department of Human Molecular Genetics, Institute of Human Genetics, Heidelberg University Hospital, Heidelberg, Germany.

Verena Wahl (V)

Department of Human Molecular Genetics, Institute of Human Genetics, Heidelberg University Hospital, Heidelberg, Germany.

Malin Schmidt (M)

Department of Human Molecular Genetics, Institute of Human Genetics, Heidelberg University Hospital, Heidelberg, Germany.
Department of Translational Brain Research, Central Institute of Mental Health.

Lesley A Houghton (LA)

St. James's University Hospital, University of Leeds, Leeds, UK.
Mayo Clinic, Jacksonville, FL, USA.

Miriam Goebel-Stengel (M)

Department of Psychosomatic Medicine, University Hospital Tübingen, Tübingen, Germany.
Department of Internal Medicine and Gastroenterology, HELIOS Clinic Rottweil, Rottweil, Germany.

Maria Kabisch (M)

Institute of Medical Biometry and Informatics, Heidelberg University, Heidelberg, Germany.

Dorothea Götze (D)

Department of Human Molecular Genetics, Institute of Human Genetics, Heidelberg University Hospital, Heidelberg, Germany.

Irina Milovač (I)

Faculty of Medicine, University Banja Luka, Banja Luka, Bosnia and Herzegovina.

Mauro D'Amato (M)

School of Biological Sciences, Monash University, Clayton, VIC, Australia.
Unit of Clinical Epidemiology, Department of Medicine Solna, Karolinska Institutet, Stockholm, Sweden.
Department of Gastrointestinal and Liver Diseases, Biodonostia HRI, San Sebastián, Spain.
IKERBASQUE, Basque Foundation for Science, Bilbao, Spain.

Tenghao Zheng (T)

School of Biological Sciences, Monash University, Clayton, VIC, Australia.
Unit of Clinical Epidemiology, Department of Medicine Solna, Karolinska Institutet, Stockholm, Sweden.

Ralph Röth (R)

Department of Human Molecular Genetics, Institute of Human Genetics, Heidelberg University Hospital, Heidelberg, Germany.
nCounter Core Facility, Department of Human Molecular Genetics, Heidelberg University Hospital, Heidelberg, Germany.

Hubert Mönnikes (H)

Martin-Luther-Hospital, Berlin, Germany.

Felicitas Engel (F)

Department of General Internal Medicine and Psychosomatics, Heidelberg University Hospital, Heidelberg, Germany.

Annika Gauss (A)

Department of Gastroenterology, Infectious Diseases and Intoxications, Heidelberg University, Heidelberg, Germany.

Jonas Tesarz (J)

Department of General Internal Medicine and Psychosomatics, Heidelberg University Hospital, Heidelberg, Germany.

Martin Raithel (M)

University of Erlangen, Erlangen, Germany.

Viola Andresen (V)

Israelitisches Krankenhaus, Hamburg, Germany.

Thomas Frieling (T)

Helios Klinik Krefeld, Krefeld, Germany.

Jutta Keller (J)

Israelitisches Krankenhaus, Hamburg, Germany.

Christian Pehl (C)

Krankenhaus Vilsbiburg, Vilsbiburg, Germany.

Christoph Stein-Thöringer (C)

German Cancer Research Center, Heidelberg, Germany.

Gerard Clarke (G)

Department of Psychiatry and Neurobehavioral Science, University College Cork, Cork, Ireland.
APC Microbiome Ireland, University College Cork, Cork, Ireland.

Paul J Kennedy (PJ)

Department of Psychiatry and Neurobehavioral Science, University College Cork, Cork, Ireland.
APC Microbiome Ireland, University College Cork, Cork, Ireland.

John F Cryan (JF)

Department of Psychiatry and Neurobehavioral Science, University College Cork, Cork, Ireland.
APC Microbiome Ireland, University College Cork, Cork, Ireland.
Department of Anatomy and Neuroscience, University College Cork, Cork, Ireland.

Timothy G Dinan (TG)

Department of Psychiatry and Neurobehavioral Science, University College Cork, Cork, Ireland.
APC Microbiome Ireland, University College Cork, Cork, Ireland.

Eamonn M M Quigley (EMM)

APC Microbiome Ireland, University College Cork, Cork, Ireland.
Lynda K. and David M. Underwood Center for Digestive Disorders, Houston Methodist Hospital, Weill Cornell Medical College, Houston, TX, USA.

Robin Spiller (R)

Nottingham Digestive Diseases Centre, University of Nottingham, Nottingham, UK.

Caroll Beltrán (C)

Gastroenterology Unit, Hospital Clínico Universidad de Chile, Medicine Department, Universidad de Chile, Santiago de Chile, Chile.

Ana María Madrid (AM)

Gastroenterology Unit, Hospital Clínico Universidad de Chile, Medicine Department, Universidad de Chile, Santiago de Chile, Chile.

Verónica Torres (V)

Gastroenterology Unit, Hospital Clínico Universidad de Chile, Medicine Department, Universidad de Chile, Santiago de Chile, Chile.

Edith Pérez de Arce (E)

Gastroenterology Unit, Hospital Clínico Universidad de Chile, Medicine Department, Universidad de Chile, Santiago de Chile, Chile.

Wolfgang Herzog (W)

Department of General Internal Medicine and Psychosomatics, Heidelberg University Hospital, Heidelberg, Germany.

Emeran A Mayer (EA)

Oppenheimer Center for Neurobiology of Stress, University of California, Los Angeles, CA, USA.

Gregory Sayuk (G)

Washington University School of Medicine, St. Louis, MO, USA.

Maria Gazouli (M)

Laboratory of Biology, Medical School, National and Kapodistrian University of Athens, Athens, Greece.

George Karamanolis (G)

Academic Department of Gastroenterology, Medical School, National and Kapodistrian University of Athens, "Laikon" General Hospital, Athens, Greece.

Lejla Kapur-Pojskič (L)

Institute for Genetic Engineering and Biotechnology, University of Sarajevo, Sarajevo, Bosnia and Herzegovina.

Mariona Bustamante (M)

CRG, Centre for Genomic Regulation, Barcelona, Spain.
ISGlobal, Barcelona, Spain.

Raquel Rabionet (R)

Department of Genetics, Microbiology and Statistics, Faculty of Biology, IBUB, CIBERER, IRSJD, Universitat de Barcelona, Barcelona, Spain.

Xavier Estivil (X)

CRG, Centre for Genomic Regulation, Barcelona, Spain.

André Franke (A)

Institute of Clinical Molecular Biology, Kiel, Germany.

Wolfgang Lieb (W)

Institute of Epidemiology, Kiel, Germany.

Guy Boeckxstaens (G)

TARGID, University Hospital Leuven, Leuven, Belgium.

Mira M Wouters (MM)

TARGID, University Hospital Leuven, Leuven, Belgium.

Magnus Simrén (M)

Institute of Medicine, University of Gothenburg, Gothenburg, Sweden.

Gudrun A Rappold (GA)

Department of Human Molecular Genetics, Institute of Human Genetics, Heidelberg University Hospital, Heidelberg, Germany.
Interdisciplinary Center for Neurosciences (IZN), Heidelberg University, Heidelberg, Germany.

Maria Vicario (M)

Institut de Recerca Vall d'Hebron, Hospital Vall d'Hebron, Barcelona, Spain.

Javier Santos (J)

Institut de Recerca Vall d'Hebron, Hospital Vall d'Hebron, Barcelona, Spain.

Rainer Schaefert (R)

Department of Psychosomatic Medicine, Division of Internal Medicine, University Hospital Basel, Basel, Switzerland.
Faculty of Medicine, University of Basel, Basel, Switzerland.

Justo Lorenzo-Bermejo (J)

Institute of Medical Biometry and Informatics, Heidelberg University, Heidelberg, Germany.

Beate Niesler (B)

Department of Human Molecular Genetics, Institute of Human Genetics, Heidelberg University Hospital, Heidelberg, Germany.
nCounter Core Facility, Department of Human Molecular Genetics, Heidelberg University Hospital, Heidelberg, Germany.
Interdisciplinary Center for Neurosciences (IZN), Heidelberg University, Heidelberg, Germany.

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