Mutations in DNAH17, Encoding a Sperm-Specific Axonemal Outer Dynein Arm Heavy Chain, Cause Isolated Male Infertility Due to Asthenozoospermia.


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:
03 07 2019
Historique:
received: 03 03 2019
accepted: 22 04 2019
pubmed: 11 6 2019
medline: 12 3 2020
entrez: 11 6 2019
Statut: ppublish

Résumé

Motile cilia and sperm flagella share an evolutionarily conserved axonemal structure. Their structural and/or functional defects are associated with primary ciliary dyskinesia (PCD), a genetic disease characterized by chronic respiratory-tract infections and in which most males are infertile due to asthenozoospermia. Among the well-characterized axonemal protein complexes, the outer dynein arms (ODAs), through ATPase activity of their heavy chains (HCs), play a major role for cilia and flagella beating. However, the contribution of the different HCs (γ-type: DNAH5 and DNAH8 and β-type: DNAH9, DNAH11, and DNAH17) in ODAs from both organelles is unknown. By analyzing five male individuals who consulted for isolated infertility and displayed a loss of ODAs in their sperm cells but not in their respiratory cells, we identified bi-allelic mutations in DNAH17. The isolated infertility phenotype prompted us to compare the protein composition of ODAs in the sperm and ciliary axonemes from control individuals. We show that DNAH17 and DNAH8, but not DNAH5, DNAH9, or DNAH11, colocalize with α-tubulin along the sperm axoneme, whereas the reverse picture is observed in respiratory cilia, thus explaining the phenotype restricted to sperm cells. We also demonstrate the loss of function associated with DNAH17 mutations in two unrelated individuals by performing immunoblot and immunofluorescence analyses on sperm cells; these analyses indicated the absence of DNAH17 and DNAH8, whereas DNAH2 and DNALI, two inner dynein arm components, were present. Overall, this study demonstrates that mutations in DNAH17 are responsible for isolated male infertility and provides information regarding ODA composition in human spermatozoa.

Identifiants

pubmed: 31178125
pii: S0002-9297(19)30163-6
doi: 10.1016/j.ajhg.2019.04.015
pmc: PMC6612517
pii:
doi:

Substances chimiques

DNAH17 protein, human EC 3.6.1.-
Axonemal Dyneins EC 3.6.4.2

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

198-212

Informations de copyright

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

Références

Am J Hum Genet. 1999 Dec;65(6):1508-19
pubmed: 10577904
Am J Hum Genet. 2001 Apr;68(4):1030-5
pubmed: 11231901
Pediatrics. 2001 Nov;108(5):E86
pubmed: 11694670
Nat Genet. 2002 Feb;30(2):143-4
pubmed: 11788826
Proc Natl Acad Sci U S A. 2002 Aug 6;99(16):10282-6
pubmed: 12142464
Am J Respir Crit Care Med. 2004 Feb 15;169(4):459-67
pubmed: 14656747
Am J Respir Crit Care Med. 2005 Jun 15;171(12):1343-9
pubmed: 15750039
J Am Chem Soc. 2005 Mar 16;127(10):3346-52
pubmed: 15755151
J Med Genet. 2006 Jan;43(1):62-73
pubmed: 15937072
Andrologia. 2006 Apr;38(2):54-60
pubmed: 16529576
Am J Respir Crit Care Med. 2006 Jul 15;174(2):120-6
pubmed: 16627867
Fertil Steril. 2006 Jul;86(1):219.e1-9
pubmed: 16750828
Science. 2006 Aug 18;313(5789):944-8
pubmed: 16917055
Development. 2006 Nov;133(21):4131-43
pubmed: 17021045
Hum Mutat. 2008 Feb;29(2):289-98
pubmed: 18022865
Am J Hum Genet. 2008 Nov;83(5):547-58
pubmed: 18950741
Hum Reprod. 2009 Jun;24(6):1296-303
pubmed: 19221096
Eur Respir J. 2010 May;35(5):1057-63
pubmed: 19840971
Hum Reprod Update. 2010 May-Jun;16(3):231-45
pubmed: 19934213
Am J Hum Genet. 2011 May 13;88(5):599-607
pubmed: 21496787
Cytoskeleton (Hoboken). 2011 Oct;68(10):555-65
pubmed: 21953912
Thorax. 2012 May;67(5):433-41
pubmed: 22184204
Mol Cell Proteomics. 2013 Feb;12(2):330-42
pubmed: 23161514
Am J Hum Genet. 2013 Jan 10;92(1):99-106
pubmed: 23261302
Am J Hum Genet. 2013 Jan 10;92(1):88-98
pubmed: 23261303
J Proteomics. 2013 Feb 21;79:114-22
pubmed: 23268119
Am J Hum Genet. 2013 Aug 8;93(2):357-67
pubmed: 23849778
Am J Hum Genet. 2014 Jan 2;94(1):95-104
pubmed: 24360805
Am J Hum Genet. 2014 Sep 4;95(3):257-74
pubmed: 25192045
Nucleic Acids Res. 2015 Jul 1;43(W1):W109-16
pubmed: 25883147
Pediatr Pulmonol. 2016 Feb;51(2):115-32
pubmed: 26418604
Hum Reprod. 2016 Jan;31(1):10-23
pubmed: 26472152
Am J Respir Cell Mol Biol. 2016 Aug;55(2):213-24
pubmed: 26909801
Hum Reprod. 2016 Jun;31(6):1164-72
pubmed: 27094479
Hum Mutat. 2016 Aug;37(8):776-85
pubmed: 27120127
Cold Spring Harb Perspect Biol. 2016 Nov 1;8(11):null
pubmed: 27527589
Clin Genet. 2017 Feb;91(2):313-321
pubmed: 27573432
Cold Spring Harb Perspect Biol. 2017 Jan 3;9(1):null
pubmed: 27601632
Hum Reprod. 2016 Dec;31(12):2872-2880
pubmed: 27798045
Eur Respir J. 2017 Jan 4;49(1):
pubmed: 27836958
J Pathol. 2017 Jan;241(2):294-309
pubmed: 27859258
J Proteome Res. 2017 Apr 7;16(4):1579-1592
pubmed: 28282151
Fertil Steril. 2017 Jun;107(6):1312-1318.e2
pubmed: 28577616
Cold Spring Harb Perspect Biol. 2017 Aug 1;9(8):null
pubmed: 28765157
Eur Respir J. 2017 Nov 9;50(5):
pubmed: 29122913
Cell Stem Cell. 2018 Oct 4;23(4):599-614.e4
pubmed: 30174296
Am J Hum Genet. 2018 Dec 6;103(6):984-994
pubmed: 30471717
Am J Hum Genet. 2018 Dec 6;103(6):995-1008
pubmed: 30471718
Bioinformatics. 2019 Jan 22;:null
pubmed: 30668675
Am J Hum Genet. 2019 Feb 7;104(2):331-340
pubmed: 30686508
Basic Clin Androl. 2019 Mar 4;29:2
pubmed: 30867909
Fertil Steril. 1987 Oct;48(4):664-9
pubmed: 3653424

Auteurs

Marjorie Whitfield (M)

Institut National de la Santé et de la Recherche Médicale U1016, Institut Cochin, Paris 75014, France; Centre National de la Recherche Scientifique UMR8104, Paris 75014, France; Faculté de Médecine, Université Paris Descartes, Sorbonne Paris Cité, Paris 75014, France.

Lucie Thomas (L)

Sorbonne Université, Institut National de la Santé et de la Recherche Médicale U933, Hôpital Trousseau, Paris 75012, France.

Emilie Bequignon (E)

Assistance Publique-Hôpitaux de Paris, Hôpital Henri Mondor et Centre Hospitalier Intercommunal de Créteil, Service d'Oto-Rhino-Laryngologie et de Chirurgie Cervico-Faciale, Créteil 94000, France; Institut National de la Santé et de la Recherche Médicale U955, Centre National de la Recherche Scientifique, Equipe de Recherche Labellisée 7240, Université Paris-Est, Faculté de Médecine, Créteil 94010, France.

Alain Schmitt (A)

Institut National de la Santé et de la Recherche Médicale U1016, Institut Cochin, Paris 75014, France; Centre National de la Recherche Scientifique UMR8104, Paris 75014, France; Faculté de Médecine, Université Paris Descartes, Sorbonne Paris Cité, Paris 75014, France.

Laurence Stouvenel (L)

Institut National de la Santé et de la Recherche Médicale U1016, Institut Cochin, Paris 75014, France; Centre National de la Recherche Scientifique UMR8104, Paris 75014, France; Faculté de Médecine, Université Paris Descartes, Sorbonne Paris Cité, Paris 75014, France.

Guy Montantin (G)

Assistance Publique-Hôpitaux de Paris, Département de Génétique Médicale, Hôpital Trousseau, Paris 75012, France.

Sylvie Tissier (S)

Assistance Publique-Hôpitaux de Paris, Département de Génétique Médicale, Hôpital Trousseau, Paris 75012, France.

Philippe Duquesnoy (P)

Sorbonne Université, Institut National de la Santé et de la Recherche Médicale U933, Hôpital Trousseau, Paris 75012, France.

Bruno Copin (B)

Assistance Publique-Hôpitaux de Paris, Département de Génétique Médicale, Hôpital Trousseau, Paris 75012, France.

Sandra Chantot (S)

Assistance Publique-Hôpitaux de Paris, Département de Génétique Médicale, Hôpital Trousseau, Paris 75012, France.

Florence Dastot (F)

Assistance Publique-Hôpitaux de Paris, Département de Génétique Médicale, Hôpital Trousseau, Paris 75012, France.

Catherine Faucon (C)

Centre Hospitalier Intercommunal de Créteil, Laboratoire de Microscopie Électronique, Service d'Anatomopathologie, Créteil 94010, France.

Anne Laure Barbotin (AL)

Centre Hospitalier Universitaire de Lille, Reproductive Biology - Spermiology - Centres d'Etudes et de Conservation des Oeufs et du Sperme Institute, Jeanne de Flandre Hospital, F-59000 Lille, France; EA4308: Gametogenesis and Gamete Quality, Lille University, F-59000 Lille, France.

Anne Loyens (A)

Jean-Pierre Aubert Research Center, Laboratory of Development and Plasticity of the Neuroendocrine Brain, Institut National de la Santé et de la Recherche Médicale U1172, Lille University, F59000 Lille, France.

Jean-Pierre Siffroi (JP)

Sorbonne Université, Institut National de la Santé et de la Recherche Médicale U933, Hôpital Trousseau, Paris 75012, France; Assistance Publique-Hôpitaux de Paris, Département de Génétique Médicale, Hôpital Trousseau, Paris 75012, France.

Jean-François Papon (JF)

Institut National de la Santé et de la Recherche Médicale U955, Centre National de la Recherche Scientifique, Equipe de Recherche Labellisée 7240, Université Paris-Sud, Faculté de Médecine, Créteil 94010, France; Assistance Publique-Hôpitaux de Paris, Service d'Oto-Rhino-Laryngologie et de Chirurgie Cervico-Faciale, Hôpital Bicêtre, Le Kremlin-Bicêtre F-94275, France.

Estelle Escudier (E)

Sorbonne Université, Institut National de la Santé et de la Recherche Médicale U933, Hôpital Trousseau, Paris 75012, France; Assistance Publique-Hôpitaux de Paris, Département de Génétique Médicale, Hôpital Trousseau, Paris 75012, France.

Serge Amselem (S)

Sorbonne Université, Institut National de la Santé et de la Recherche Médicale U933, Hôpital Trousseau, Paris 75012, France; Assistance Publique-Hôpitaux de Paris, Département de Génétique Médicale, Hôpital Trousseau, Paris 75012, France.

Valérie Mitchell (V)

Centre Hospitalier Universitaire de Lille, Reproductive Biology - Spermiology - Centres d'Etudes et de Conservation des Oeufs et du Sperme Institute, Jeanne de Flandre Hospital, F-59000 Lille, France; EA4308: Gametogenesis and Gamete Quality, Lille University, F-59000 Lille, France.

Aminata Touré (A)

Institut National de la Santé et de la Recherche Médicale U1016, Institut Cochin, Paris 75014, France; Centre National de la Recherche Scientifique UMR8104, Paris 75014, France; Faculté de Médecine, Université Paris Descartes, Sorbonne Paris Cité, Paris 75014, France. Electronic address: aminata.toure@inserm.fr.

Marie Legendre (M)

Sorbonne Université, Institut National de la Santé et de la Recherche Médicale U933, Hôpital Trousseau, Paris 75012, France; Assistance Publique-Hôpitaux de Paris, Département de Génétique Médicale, Hôpital Trousseau, Paris 75012, France.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH