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A no-stop mutation in MAGEB4 is a possible cause of rare X-linked azoospermia and oligozoospermia in a consanguineous Turkish family

  • Genetics
  • Published:
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Abstract

Purpose

The purpose of this study was to identify mutations that cause non-syndromic male infertility using whole exome sequencing of family cases.

Methods

We recruited a consanguineous Turkish family comprising nine siblings with male triplets; two of the triplets were infertile as well as one younger infertile brother. Whole exome sequencing (WES) performed on two azoospermic brothers identified a mutation in the melanoma antigen family B4 (MAGEB4) gene which was confirmed via Sanger sequencing and then screened for on control groups and unrelated infertile subjects. The effect of the mutation on messenger RNA (mRNA) and protein levels was tested after in vitro cell transfection. Structural features of MAGEB4 were predicted throughout the conserved MAGE domain.

Results

The novel single-base substitution (c.1041A>T) in the X-linked MAGEB4 gene was identified as a no-stop mutation. The mutation is predicted to add 24 amino acids to the C-terminus of MAGEB4. Our functional studies were unable to detect any effect either on mRNA stability, intracellular localization of the protein, or the ability to homodimerize/heterodimerize with other MAGE proteins. We thus hypothesize that these additional amino acids may affect the proper protein interactions with MAGEB4 partners.

Conclusion

The whole exome analysis of a consanguineous Turkish family revealed MAGEB4 as a possible new X-linked cause of inherited male infertility. This study provides the first clue to the physiological function of a MAGE protein.

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Acknowledgements

We thank all patients for their participation and donation of samples. We would also like to thank Robert Drillien for his critical reading of the manuscript. We are grateful to the IGBMC platforms. We thank Anne-Lena Bröcher from the Institute of Human Genetics, University of Münster for her excellent technical support.

Author information

Author notes

  1. STéphane Viville

    Present address: Laboratoire de diagnostic génétique, UF3472-génétique de l’infertilité, Nouvel Hôpital Civil, Hôpitaux Universitaires de Strasbourg, 1 place de l’Hôpital, 67091, Strasbourg cedex, France

Authors and Affiliations

  1. Département Génomique Fonctionnelle et Cancer, Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Institut National de Santé et de Recherche Médicale (INSERM) U964/Centre National de Recherche Scientifique (CNRS) UMR 7104, Université de Strasbourg, 67404, Illkirch, France

    Ozlem Okutman, Valerie Skory, Marius Teletin & STéphane Viville

  2. Institut de Parasitologie et Pathologie Tropicale, EA 7292, Fédération de Médecine Translationelle, Université de Strasbourg, 3 rue Koeberlé, 67000, Strasbourg, France

    Ozlem Okutman & STéphane Viville

  3. Laboratoire de Diagnostic Génétique, UF3472-génétique de l’infertilité, Hôpitaux Universitaires de Strasbourg, 67000, Strasbourg, France

    Ozlem Okutman & STéphane Viville

  4. Laboratoire de Diagnostic Génétique, Hôpitaux Universitaires de Strasbourg, Strasbourg, France

    Jean Muller

  5. Laboratoire de Génétique Médicale, INSERM U1112, Fédération de Médecine Translationnelle de Strasbourg (FMTS), Université de Strasbourg, Strasbourg, France

    Jean Muller

  6. Biologie du développement et cellules souches, Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Institut National de Santé et de Recherche Médicale (INSERM) U964/Centre National de Recherche Scientifique (CNRS) UMR 7104, Université de Strasbourg, 67404, Illkirch, France

    Jean Marie Garnier

  7. Médecine translationnelle et neurogénétique, Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Institut National de Santé et de Recherche Médicale (INSERM) U964/Centre National de Recherche Scientifique (CNRS) UMR 7104, Université de Strasbourg, 67404, Illkirch, France

    Angeline Gaucherot & Nicolas Charlet-Berguerand

  8. Biology of the Testis, Research Laboratory for Reproduction, Genetics and Regenerative Medicine, Vrije Universiteit Brussel (VUB), Laarbeeklaan 103, 1090, Brussels, Belgium

    Yoni Baert & Ellen Goossens

  9. Département Biologie structurale intégrative, Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Institut National de Santé et de Recherche Médicale (INSERM) U964/Centre National de Recherche Scientifique (CNRS) UMR 7104, Université de Strasbourg, 67404, Illkirch, France

    Valérie Lamour

  10. Bahceci Health Group, Sisli, 34365, Istanbul, Turkey

    Munevver Serdarogullari, Meral Gultomruk & Mustafa Bahceci

  11. Institute of Human Genetics, University of Münster, Münster, Germany

    Albrecht Röpke & Frank Tüttelmann

  12. Centre of Reproductive Medicine and Andrology, University of Münster, Münster, Germany

    Sabine Kliesch

  13. Genetics Department, CHU-Hôpital Nord, Saint-Etienne, France

    Viviana Herbepin

  14. Reproductive Biology Unit, CHU-Hôpital Nord, Saint-Etienne, France

    Isabelle Aknin

  15. Médecine de la Reproduction et Cytogénétique Médicale CHU et Faculté de Médecine, Université de Picardie Jules Verne, 80000, Amiens, France

    Moncef Benkhalifa

  16. Unimed Center, Sisli, 34365, Istanbul, Turkey

    Emre Bakircioglu

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  1. Ozlem Okutman
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  2. Jean Muller
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  3. Valerie Skory
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  20. Frank Tüttelmann
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  21. STéphane Viville
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Corresponding author

Correspondence to STéphane Viville.

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Funding

The study was funded by Agence Nationale de la Recherché (ANR-11-BSV2-002 “TranspoFertil”), Fondation Maladies Rares (“High throughput sequencing and rare diseases”), and l’Agence de BioMédecine (“AMP, diagnostic prénatal et diagnostic génétique”). This work was supported by the French Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM), the Ministère de l’Education Nationale et de l’Enseignement Supérieur et de la Recherche, the University of Strasbourg, and Strasbourg University Hospital. The study was also supported by the German Research Foundation (DFG) (TU298/1-2 to FT and AR).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This project has been approved by the Comité de Protection de la Personne (CPP) of Strasbourg University Hospital, France (CPP 09/40—W AC-2008-438 1W DC-2009-I 002), the “Istanbul University, Faculty of Medicine, Ethics Committee for Clinical Research Faculty of Medicine” (2012/1671-1265), and the Ethics Committee of the Medical Faculty in Münster (2010-578-f-S).

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

Frank Tüttelmann and STéphane Viville are co-last authors.

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Okutman, O., Muller, J., Skory, V. et al. A no-stop mutation in MAGEB4 is a possible cause of rare X-linked azoospermia and oligozoospermia in a consanguineous Turkish family. J Assist Reprod Genet 34, 683–694 (2017). https://doi.org/10.1007/s10815-017-0900-z

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