Bi-allelic Mutations in ARMC2 Lead to Severe Astheno-Teratozoospermia Due to Sperm Flagellum Malformations in Humans and Mice.


Journal

American journal of human genetics
ISSN: 1537-6605
Titre abrégé: Am J Hum Genet
Pays: United States
ID NLM: 0370475

Informations de publication

Date de publication:
07 02 2019
Historique:
received: 05 10 2018
accepted: 18 12 2018
pubmed: 29 1 2019
medline: 20 11 2019
entrez: 29 1 2019
Statut: ppublish

Résumé

Male infertility is a major health concern. Among its different causes, multiple morphological abnormalities of the flagella (MMAF) induces asthenozoospermia and is one of the most severe forms of qualitative sperm defects. Sperm of affected men display short, coiled, absent, and/or irregular flagella. To date, six genes (DNAH1, CFAP43, CFAP44, CFAP69, FSIP2, and WDR66) have been found to be recurrently associated with MMAF, but more than half of the cases analyzed remain unresolved, suggesting that many yet-uncharacterized gene defects account for this phenotype. Here, whole-exome sequencing (WES) was performed on 168 infertile men who had a typical MMAF phenotype. Five unrelated affected individuals carried a homozygous deleterious mutation in ARMC2, a gene not previously linked to the MMAF phenotype. Using the CRISPR-Cas9 technique, we generated homozygous Armc2 mutant mice, which also presented an MMAF phenotype, thus confirming the involvement of ARMC2 in human MMAF. Immunostaining experiments in AMRC2-mutated individuals and mutant mice evidenced the absence of the axonemal central pair complex (CPC) proteins SPAG6 and SPEF2, whereas the other tested axonemal and peri-axonemal components were present, suggesting that ARMC2 is involved in CPC assembly and/or stability. Overall, we showed that bi-allelic mutations in ARMC2 cause male infertility in humans and mice by inducing a typical MMAF phenotype, indicating that this gene is necessary for sperm flagellum structure and assembly.

Identifiants

pubmed: 30686508
pii: S0002-9297(18)30466-X
doi: 10.1016/j.ajhg.2018.12.013
pmc: PMC6372258
pii:
doi:

Substances chimiques

ARMC2 protein, human 0
Armc2 protein, mouse 0
Cell Cycle Proteins 0
Cytoskeletal Proteins 0
Microtubule Proteins 0
Proteins 0
SPAG6 protein, human 0
SPAG6 protein, mouse 0
SPEF2 protein, human 0
SPEF2 protein, mouse 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

331-340

Informations de copyright

Copyright © 2019 American Society of Human Genetics. Published by Elsevier Inc. All rights reserved.

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Auteurs

Charles Coutton (C)

Team Genetics Epigenetics and Therapies of Infertility, Institute for Advanced Biosciences, Université Grenoble Alpes, Inserm U1209, Centre National de la Recherche Scientifique UMR 5309, Grenoble 38000, France; Unité Médicale (UM) de Génétique Chromosomique, Centre Hospitalier Universitaire Grenoble Alpes, Grenoble 38000, France. Electronic address: ccoutton@chu-grenoble.fr.

Guillaume Martinez (G)

Team Genetics Epigenetics and Therapies of Infertility, Institute for Advanced Biosciences, Université Grenoble Alpes, Inserm U1209, Centre National de la Recherche Scientifique UMR 5309, Grenoble 38000, France; Unité Médicale (UM) de Génétique Chromosomique, Centre Hospitalier Universitaire Grenoble Alpes, Grenoble 38000, France.

Zine-Eddine Kherraf (ZE)

Team Genetics Epigenetics and Therapies of Infertility, Institute for Advanced Biosciences, Université Grenoble Alpes, Inserm U1209, Centre National de la Recherche Scientifique UMR 5309, Grenoble 38000, France; Unité Médicale de génétique de l'infertilité et de diagnostic pré-implantatoire (GI-DPI), Centre Hospitalier Universitaire Grenoble Alpes, Grenoble 38000, France.

Amir Amiri-Yekta (A)

Team Genetics Epigenetics and Therapies of Infertility, Institute for Advanced Biosciences, Université Grenoble Alpes, Inserm U1209, Centre National de la Recherche Scientifique UMR 5309, Grenoble 38000, France; Unité Médicale de génétique de l'infertilité et de diagnostic pré-implantatoire (GI-DPI), Centre Hospitalier Universitaire Grenoble Alpes, Grenoble 38000, France; Department of Genetics, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, the Academic Center for Education, Culture, and Research, PO Box 16635-148, Tehran, Iran.

Magalie Boguenet (M)

Team Genetics Epigenetics and Therapies of Infertility, Institute for Advanced Biosciences, Université Grenoble Alpes, Inserm U1209, Centre National de la Recherche Scientifique UMR 5309, Grenoble 38000, France.

Antoine Saut (A)

Team Genetics Epigenetics and Therapies of Infertility, Institute for Advanced Biosciences, Université Grenoble Alpes, Inserm U1209, Centre National de la Recherche Scientifique UMR 5309, Grenoble 38000, France.

Xiaojin He (X)

Department of Obstetrics and Gynecology, Reproductive Medicine Center, the First Affiliated Hospital of Anhui Medical University, Hefei 230022, China.

Feng Zhang (F)

Institute of Metabolism and Integrative Biology, Obstetrics and Gynecology Hospital, School of Life Sciences, Fudan University, Shanghai 200011, China.

Marie Cristou-Kent (M)

Team Genetics Epigenetics and Therapies of Infertility, Institute for Advanced Biosciences, Université Grenoble Alpes, Inserm U1209, Centre National de la Recherche Scientifique UMR 5309, Grenoble 38000, France.

Jessica Escoffier (J)

Team Genetics Epigenetics and Therapies of Infertility, Institute for Advanced Biosciences, Université Grenoble Alpes, Inserm U1209, Centre National de la Recherche Scientifique UMR 5309, Grenoble 38000, France.

Marie Bidart (M)

Clinatec, Pôle Recherche, Inserm UMR 1205, Centre Hospitalier Universitaire Grenoble, Alpes, Université Grenoble Alpes, Grenoble 38000, France.

Véronique Satre (V)

Team Genetics Epigenetics and Therapies of Infertility, Institute for Advanced Biosciences, Université Grenoble Alpes, Inserm U1209, Centre National de la Recherche Scientifique UMR 5309, Grenoble 38000, France; Unité Médicale (UM) de Génétique Chromosomique, Centre Hospitalier Universitaire Grenoble Alpes, Grenoble 38000, France.

Béatrice Conne (B)

Department of Genetic Medicine and Development, University of Geneva Medical School, Geneva 1211, Switzerland.

Selima Fourati Ben Mustapha (S)

Polyclinique les Jasmins, Centre d'Aide Médicale à la Procréation, Centre Urbain Nord, Tunis 1003, Tunisia.

Lazhar Halouani (L)

Polyclinique les Jasmins, Centre d'Aide Médicale à la Procréation, Centre Urbain Nord, Tunis 1003, Tunisia.

Ouafi Marrakchi (O)

Polyclinique les Jasmins, Centre d'Aide Médicale à la Procréation, Centre Urbain Nord, Tunis 1003, Tunisia.

Mounir Makni (M)

Polyclinique les Jasmins, Centre d'Aide Médicale à la Procréation, Centre Urbain Nord, Tunis 1003, Tunisia.

Habib Latrous (H)

Polyclinique les Jasmins, Centre d'Aide Médicale à la Procréation, Centre Urbain Nord, Tunis 1003, Tunisia.

Mahmoud Kharouf (M)

Polyclinique les Jasmins, Centre d'Aide Médicale à la Procréation, Centre Urbain Nord, Tunis 1003, Tunisia.

Karin Pernet-Gallay (K)

Grenoble Neuroscience Institute, Inserm 1216, Grenoble 38000, France.

Mélanie Bonhivers (M)

Microbiologie Fondamentale et Pathogénicité, Université de Bordeaux, Centre National de la Recherche Scientifique UMR 5234, Bordeaux 33000, France.

Sylviane Hennebicq (S)

Team Genetics Epigenetics and Therapies of Infertility, Institute for Advanced Biosciences, Université Grenoble Alpes, Inserm U1209, Centre National de la Recherche Scientifique UMR 5309, Grenoble 38000, France; Unité fonctionnelle de Biologie de la Procréation, Centre Hospitalier Universitaire de Grenoble, Grenoble 38000, France.

Nathalie Rives (N)

EA 4308 Gametogenesis and Gamete Quality, Department of Reproductive Biology-CECOS, Rouen University Hospital, UNIROUEN, Normandie Université, 76000 Rouen, France; Institut de Recherche en Santé, Environnement, et Travail, Inserm U1085, Université de Rennes 1, Rennes, France.

Emmanuel Dulioust (E)

Laboratoire d'Histologie Embryologie et de la Biologie de la Reproduction, Groupe Hospitalier Cochin, Broca, et Hôtel Dieu, Assistance Publique-Hôpitaux de Paris, Paris 75014, France; Faculté de Médecine, Université Paris Descartes, Sorbonne Paris Cité, Paris 75014, France.

Aminata Touré (A)

Faculté de Médecine, Université Paris Descartes, Sorbonne Paris Cité, Paris 75014, France; Inserm U1016, Institut Cochin, Paris 75014, France; Centre National de la Recherche Scientifique UMR 8104, Paris 75014, France.

Hamid Gourabi (H)

Department of Genetics, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, the Academic Center for Education, Culture, and Research, PO Box 16635-148, Tehran, Iran.

Yunxia Cao (Y)

Department of Obstetrics and Gynecology, Reproductive Medicine Center, the First Affiliated Hospital of Anhui Medical University, Hefei 230022, China.

Raoudha Zouari (R)

Polyclinique les Jasmins, Centre d'Aide Médicale à la Procréation, Centre Urbain Nord, Tunis 1003, Tunisia.

Seyedeh Hanieh Hosseini (SH)

Department of Andrology, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, the Academic Center for Education, Culture, and Research, Tehran, Iran.

Serge Nef (S)

Department of Genetic Medicine and Development, University of Geneva Medical School, Geneva 1211, Switzerland.

Nicolas Thierry-Mieg (N)

Université Grenoble Alpes, Centre National de la Recherche Scientifique, Téchniques de l'Ingénierie Médicale et de la Complexité et Informatiques, Mathématiques, Applications, Grenoble (TIMC-IMAG), Biologie Computationnelle et Mathématique (BCM), 38000 Grenoble 38000, France.

Christophe Arnoult (C)

Team Genetics Epigenetics and Therapies of Infertility, Institute for Advanced Biosciences, Université Grenoble Alpes, Inserm U1209, Centre National de la Recherche Scientifique UMR 5309, Grenoble 38000, France.

Pierre F Ray (PF)

Team Genetics Epigenetics and Therapies of Infertility, Institute for Advanced Biosciences, Université Grenoble Alpes, Inserm U1209, Centre National de la Recherche Scientifique UMR 5309, Grenoble 38000, France; Unité Médicale de génétique de l'infertilité et de diagnostic pré-implantatoire (GI-DPI), Centre Hospitalier Universitaire Grenoble Alpes, Grenoble 38000, France. Electronic address: pray@chu-grenoble.fr.

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Classifications MeSH