Phosphorylation of GATA4 serine 105 but not serine 261 is required for testosterone production in the male mouse.


Journal

Andrology
ISSN: 2047-2927
Titre abrégé: Andrology
Pays: England
ID NLM: 101585129

Informations de publication

Date de publication:
05 2019
Historique:
received: 17 11 2018
revised: 28 01 2019
accepted: 30 01 2019
pubmed: 23 2 2019
medline: 15 5 2020
entrez: 23 2 2019
Statut: ppublish

Résumé

GATA4 is a transcription factor essential for male sex determination, testicular differentiation during fetal development, and male fertility in the adult. GATA4 exerts part of its function by regulating multiple genes in the steroidogenic enzyme pathway. In spite of these crucial roles, how the activity of this factor is regulated remains unclear. Studies in gonadal cell lines have shown that GATA4 is phosphorylated on at least two serine residues-serine 105 (S105) and serine 261 (S261)-and that this phosphorylation is important for GATA4 activity. The objective of the present study is to characterize the endogenous role of GATA4 S105 and S261 phosphorylation in the mouse testis. We examined both previously described GATA4 S105A mice and a novel GATA4 S261A knock-in mouse that we generated by CRISPR/Cas9 gene editing. The male phenotype of the mutants was characterized by assessing androgen-dependent organ weights, hormonal profiles, and expression of multiple testicular target genes using standard biochemical and molecular biology techniques. The fecundity of crosses between GATA4 S105A mice was reduced but without a change in sex ratio. The weight of androgen-dependent organs was smaller when compared to wild-type controls. Plasma testosterone levels showed a 70% decrease in adult GATA4 S105A males. This decrease was associated with a reduction in Cyp11a1, Cyp17a1, and Hsd17b3 expression. GATA4 S261A mice were viable and testis morphology appeared normal. Testosterone production and steroidogenic enzyme expression were not altered in GATA4 S261A males. Our analysis showed that blocking GATA4 S105 phosphorylation is associated with decreased androgen production in males. In contrast, S261 phosphorylation by itself is dispensable for GATA4 function. These results confirm that endogenous GATA4 action is essential for normal steroid production in males and that this activity requires phosphorylation on at least one serine residue.

Sections du résumé

BACKGROUND
GATA4 is a transcription factor essential for male sex determination, testicular differentiation during fetal development, and male fertility in the adult. GATA4 exerts part of its function by regulating multiple genes in the steroidogenic enzyme pathway. In spite of these crucial roles, how the activity of this factor is regulated remains unclear.
OBJECTIVES
Studies in gonadal cell lines have shown that GATA4 is phosphorylated on at least two serine residues-serine 105 (S105) and serine 261 (S261)-and that this phosphorylation is important for GATA4 activity. The objective of the present study is to characterize the endogenous role of GATA4 S105 and S261 phosphorylation in the mouse testis.
MATERIALS AND METHODS
We examined both previously described GATA4 S105A mice and a novel GATA4 S261A knock-in mouse that we generated by CRISPR/Cas9 gene editing. The male phenotype of the mutants was characterized by assessing androgen-dependent organ weights, hormonal profiles, and expression of multiple testicular target genes using standard biochemical and molecular biology techniques.
RESULTS
The fecundity of crosses between GATA4 S105A mice was reduced but without a change in sex ratio. The weight of androgen-dependent organs was smaller when compared to wild-type controls. Plasma testosterone levels showed a 70% decrease in adult GATA4 S105A males. This decrease was associated with a reduction in Cyp11a1, Cyp17a1, and Hsd17b3 expression. GATA4 S261A mice were viable and testis morphology appeared normal. Testosterone production and steroidogenic enzyme expression were not altered in GATA4 S261A males.
DISCUSSION AND CONCLUSION
Our analysis showed that blocking GATA4 S105 phosphorylation is associated with decreased androgen production in males. In contrast, S261 phosphorylation by itself is dispensable for GATA4 function. These results confirm that endogenous GATA4 action is essential for normal steroid production in males and that this activity requires phosphorylation on at least one serine residue.

Identifiants

pubmed: 30793514
doi: 10.1111/andr.12601
doi:

Substances chimiques

GATA4 Transcription Factor 0
Gata4 protein, mouse 0
Testosterone 3XMK78S47O
Serine 452VLY9402

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

357-372

Subventions

Organisme : Canadian Institutes of Health Research (CIHR)
ID : MOP-14796
Pays : International
Organisme : Fonds de la Recherche du Québec - Santé (FRQS)
Pays : International

Informations de copyright

© 2019 American Society of Andrology and European Academy of Andrology.

Auteurs

F Bergeron (F)

Reproduction, Mother and Child Health, Centre de Recherche du CHU de Québec-Université Laval, Quebec, QC, Canada.
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle (CRDSI), Quebec, QC, Canada.

A Boulende Sab (A)

Département des Sciences Biologiques and Centre d'excellence en Recherche sur les Maladies Orphelines - Fondation Courtois (CERMO-FC), Université du Québec à Montréal (UQAM), Montreal, QC, Canada.

M F Bouchard (MF)

Reproduction, Mother and Child Health, Centre de Recherche du CHU de Québec-Université Laval, Quebec, QC, Canada.
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle (CRDSI), Quebec, QC, Canada.

H Taniguchi (H)

Institute of Genetics and Animal Breeding of the Polish Academy of Sciences, Jastrzebiec, Poland.

O Souchkova (O)

Département des Sciences Biologiques and Centre d'excellence en Recherche sur les Maladies Orphelines - Fondation Courtois (CERMO-FC), Université du Québec à Montréal (UQAM), Montreal, QC, Canada.

C Brousseau (C)

Reproduction, Mother and Child Health, Centre de Recherche du CHU de Québec-Université Laval, Quebec, QC, Canada.
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle (CRDSI), Quebec, QC, Canada.

J J Tremblay (JJ)

Reproduction, Mother and Child Health, Centre de Recherche du CHU de Québec-Université Laval, Quebec, QC, Canada.
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle (CRDSI), Quebec, QC, Canada.
Department of Obstetrics, Gynecology, and Reproduction, Université Laval, Quebec, QC, Canada.

N Pilon (N)

Département des Sciences Biologiques and Centre d'excellence en Recherche sur les Maladies Orphelines - Fondation Courtois (CERMO-FC), Université du Québec à Montréal (UQAM), Montreal, QC, Canada.

R S Viger (RS)

Reproduction, Mother and Child Health, Centre de Recherche du CHU de Québec-Université Laval, Quebec, QC, Canada.
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle (CRDSI), Quebec, QC, Canada.
Department of Obstetrics, Gynecology, and Reproduction, Université Laval, Quebec, QC, Canada.

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Classifications MeSH