Gper and ESRs are expressed in rat round spermatids and mediate oestrogen-dependent rapid pathways modulating expression of cyclin B1 and Bax

A. Chimento, R. Sirianni, F. Zolea, C. Bois, C. Delalande, S. Andò, M. Maggiolini, S. Aquila, S. Carreau, V. Pezzi

Research output: Contribution to journalArticle

48 Citations (Scopus)

Abstract

Spermatogenesis is a precisely controlled and timed process, comprising mitotic divisions of spermatogonia, meiotic divisions of spermatocytes, maturation and differentiation of haploid spermatids giving rise to spermatozoa. It is well known that the maintenance of spermatogenesis is controlled by gonadotrophins and testosterone, the effects of which are modulated by a complex network of locally produced factors, including oestrogens. However, it remains uncertain whether oestrogens are able to activate rapid signalling pathways directly in male germ cells. Classically, oestrogens act by binding to oestrogen receptors (ESRs) 1 and 2. Recently, it has been demonstrated that rapid oestrogen action can also be mediated by the G-protein-coupled oestrogen receptor 1 (Gper). The aim of the present study was to investigate ESRs and Gper expression in primary cultures of adult rat round spermatids (RS) and define if oestradiol (E2) is able to activate, through these receptors, pathways involved in the regulation of genes controlling rat RS apoptosis and/or maturation. In this study, we demonstrated that rat RS express ESR1, ESR2 and Gper. Short-time treatment of RS with E2, the selective Gper agonist G1 and the selective ESR1 and ERβ agonists, 4,4',4″-(4-propyl-[1H]pyrazole-1,3,5-triyl) trisphenol (PPT) and 2,3-bis(4-hydroxyphenyl)-propionitrile (DPN), respectively, determined activation of Extra-cellular signal-regulated kinase (ERK1/2) through the involvement of epidermal growth factor receptor transactivation. In addition, we investigated the effects of ESRs and Gper pathway activation on factors involved in RS maturation. Expression of cyclin B1 mRNA was downregulated by E2, G1 and PPT, but not by DPN. A concomitant and inverse regulation of the pro-apoptotic factor Bax mRNA expression was observed in the same conditions, with DPN being the only one determining an increase in this factor expression. Collectively, these data demonstrate that E2 activates, through ESRs and Gper, pathways involved in the regulation of genes controlling rat RS apoptosis and differentiation such as cyclin B1 and Bax.

Original languageEnglish (US)
Pages (from-to)420-429
Number of pages10
JournalInternational Journal of Andrology
Volume34
Issue number5 PART 1
DOIs
StatePublished - Oct 2011

Fingerprint

Cyclin B1
Spermatids
Estrogen Receptor alpha
G-Protein-Coupled Receptors
Estrogens
Spermatogenesis
Apoptosis
Estrogen Receptor beta
Messenger RNA
Spermatogonia
Spermatocytes
Mitogen-Activated Protein Kinase 3
Haploidy
Gonadotropins
Epidermal Growth Factor Receptor
Germ Cells
Transcriptional Activation
Genes
Testosterone
Spermatozoa

Keywords

  • Gper
  • Oestrogen
  • Oestrogen receptors
  • Rat
  • Round spermatids

ASJC Scopus subject areas

  • Urology
  • Reproductive Medicine
  • Endocrinology, Diabetes and Metabolism

Cite this

Gper and ESRs are expressed in rat round spermatids and mediate oestrogen-dependent rapid pathways modulating expression of cyclin B1 and Bax. / Chimento, A.; Sirianni, R.; Zolea, F.; Bois, C.; Delalande, C.; Andò, S.; Maggiolini, M.; Aquila, S.; Carreau, S.; Pezzi, V.

In: International Journal of Andrology, Vol. 34, No. 5 PART 1, 10.2011, p. 420-429.

Research output: Contribution to journalArticle

Chimento, A, Sirianni, R, Zolea, F, Bois, C, Delalande, C, Andò, S, Maggiolini, M, Aquila, S, Carreau, S & Pezzi, V 2011, 'Gper and ESRs are expressed in rat round spermatids and mediate oestrogen-dependent rapid pathways modulating expression of cyclin B1 and Bax', International Journal of Andrology, vol. 34, no. 5 PART 1, pp. 420-429. https://doi.org/10.1111/j.1365-2605.2010.01100.x
Chimento, A. ; Sirianni, R. ; Zolea, F. ; Bois, C. ; Delalande, C. ; Andò, S. ; Maggiolini, M. ; Aquila, S. ; Carreau, S. ; Pezzi, V. / Gper and ESRs are expressed in rat round spermatids and mediate oestrogen-dependent rapid pathways modulating expression of cyclin B1 and Bax. In: International Journal of Andrology. 2011 ; Vol. 34, No. 5 PART 1. pp. 420-429.
@article{ba64dfdfbfd444afba888ba9f3651a8f,
title = "Gper and ESRs are expressed in rat round spermatids and mediate oestrogen-dependent rapid pathways modulating expression of cyclin B1 and Bax",
abstract = "Spermatogenesis is a precisely controlled and timed process, comprising mitotic divisions of spermatogonia, meiotic divisions of spermatocytes, maturation and differentiation of haploid spermatids giving rise to spermatozoa. It is well known that the maintenance of spermatogenesis is controlled by gonadotrophins and testosterone, the effects of which are modulated by a complex network of locally produced factors, including oestrogens. However, it remains uncertain whether oestrogens are able to activate rapid signalling pathways directly in male germ cells. Classically, oestrogens act by binding to oestrogen receptors (ESRs) 1 and 2. Recently, it has been demonstrated that rapid oestrogen action can also be mediated by the G-protein-coupled oestrogen receptor 1 (Gper). The aim of the present study was to investigate ESRs and Gper expression in primary cultures of adult rat round spermatids (RS) and define if oestradiol (E2) is able to activate, through these receptors, pathways involved in the regulation of genes controlling rat RS apoptosis and/or maturation. In this study, we demonstrated that rat RS express ESR1, ESR2 and Gper. Short-time treatment of RS with E2, the selective Gper agonist G1 and the selective ESR1 and ERβ agonists, 4,4',4″-(4-propyl-[1H]pyrazole-1,3,5-triyl) trisphenol (PPT) and 2,3-bis(4-hydroxyphenyl)-propionitrile (DPN), respectively, determined activation of Extra-cellular signal-regulated kinase (ERK1/2) through the involvement of epidermal growth factor receptor transactivation. In addition, we investigated the effects of ESRs and Gper pathway activation on factors involved in RS maturation. Expression of cyclin B1 mRNA was downregulated by E2, G1 and PPT, but not by DPN. A concomitant and inverse regulation of the pro-apoptotic factor Bax mRNA expression was observed in the same conditions, with DPN being the only one determining an increase in this factor expression. Collectively, these data demonstrate that E2 activates, through ESRs and Gper, pathways involved in the regulation of genes controlling rat RS apoptosis and differentiation such as cyclin B1 and Bax.",
keywords = "Gper, Oestrogen, Oestrogen receptors, Rat, Round spermatids",
author = "A. Chimento and R. Sirianni and F. Zolea and C. Bois and C. Delalande and S. And{\`o} and M. Maggiolini and S. Aquila and S. Carreau and V. Pezzi",
year = "2011",
month = "10",
doi = "10.1111/j.1365-2605.2010.01100.x",
language = "English (US)",
volume = "34",
pages = "420--429",
journal = "International Journal of Andrology",
issn = "0105-6263",
publisher = "Wiley-Blackwell",
number = "5 PART 1",

}

TY - JOUR

T1 - Gper and ESRs are expressed in rat round spermatids and mediate oestrogen-dependent rapid pathways modulating expression of cyclin B1 and Bax

AU - Chimento, A.

AU - Sirianni, R.

AU - Zolea, F.

AU - Bois, C.

AU - Delalande, C.

AU - Andò, S.

AU - Maggiolini, M.

AU - Aquila, S.

AU - Carreau, S.

AU - Pezzi, V.

PY - 2011/10

Y1 - 2011/10

N2 - Spermatogenesis is a precisely controlled and timed process, comprising mitotic divisions of spermatogonia, meiotic divisions of spermatocytes, maturation and differentiation of haploid spermatids giving rise to spermatozoa. It is well known that the maintenance of spermatogenesis is controlled by gonadotrophins and testosterone, the effects of which are modulated by a complex network of locally produced factors, including oestrogens. However, it remains uncertain whether oestrogens are able to activate rapid signalling pathways directly in male germ cells. Classically, oestrogens act by binding to oestrogen receptors (ESRs) 1 and 2. Recently, it has been demonstrated that rapid oestrogen action can also be mediated by the G-protein-coupled oestrogen receptor 1 (Gper). The aim of the present study was to investigate ESRs and Gper expression in primary cultures of adult rat round spermatids (RS) and define if oestradiol (E2) is able to activate, through these receptors, pathways involved in the regulation of genes controlling rat RS apoptosis and/or maturation. In this study, we demonstrated that rat RS express ESR1, ESR2 and Gper. Short-time treatment of RS with E2, the selective Gper agonist G1 and the selective ESR1 and ERβ agonists, 4,4',4″-(4-propyl-[1H]pyrazole-1,3,5-triyl) trisphenol (PPT) and 2,3-bis(4-hydroxyphenyl)-propionitrile (DPN), respectively, determined activation of Extra-cellular signal-regulated kinase (ERK1/2) through the involvement of epidermal growth factor receptor transactivation. In addition, we investigated the effects of ESRs and Gper pathway activation on factors involved in RS maturation. Expression of cyclin B1 mRNA was downregulated by E2, G1 and PPT, but not by DPN. A concomitant and inverse regulation of the pro-apoptotic factor Bax mRNA expression was observed in the same conditions, with DPN being the only one determining an increase in this factor expression. Collectively, these data demonstrate that E2 activates, through ESRs and Gper, pathways involved in the regulation of genes controlling rat RS apoptosis and differentiation such as cyclin B1 and Bax.

AB - Spermatogenesis is a precisely controlled and timed process, comprising mitotic divisions of spermatogonia, meiotic divisions of spermatocytes, maturation and differentiation of haploid spermatids giving rise to spermatozoa. It is well known that the maintenance of spermatogenesis is controlled by gonadotrophins and testosterone, the effects of which are modulated by a complex network of locally produced factors, including oestrogens. However, it remains uncertain whether oestrogens are able to activate rapid signalling pathways directly in male germ cells. Classically, oestrogens act by binding to oestrogen receptors (ESRs) 1 and 2. Recently, it has been demonstrated that rapid oestrogen action can also be mediated by the G-protein-coupled oestrogen receptor 1 (Gper). The aim of the present study was to investigate ESRs and Gper expression in primary cultures of adult rat round spermatids (RS) and define if oestradiol (E2) is able to activate, through these receptors, pathways involved in the regulation of genes controlling rat RS apoptosis and/or maturation. In this study, we demonstrated that rat RS express ESR1, ESR2 and Gper. Short-time treatment of RS with E2, the selective Gper agonist G1 and the selective ESR1 and ERβ agonists, 4,4',4″-(4-propyl-[1H]pyrazole-1,3,5-triyl) trisphenol (PPT) and 2,3-bis(4-hydroxyphenyl)-propionitrile (DPN), respectively, determined activation of Extra-cellular signal-regulated kinase (ERK1/2) through the involvement of epidermal growth factor receptor transactivation. In addition, we investigated the effects of ESRs and Gper pathway activation on factors involved in RS maturation. Expression of cyclin B1 mRNA was downregulated by E2, G1 and PPT, but not by DPN. A concomitant and inverse regulation of the pro-apoptotic factor Bax mRNA expression was observed in the same conditions, with DPN being the only one determining an increase in this factor expression. Collectively, these data demonstrate that E2 activates, through ESRs and Gper, pathways involved in the regulation of genes controlling rat RS apoptosis and differentiation such as cyclin B1 and Bax.

KW - Gper

KW - Oestrogen

KW - Oestrogen receptors

KW - Rat

KW - Round spermatids

UR - http://www.scopus.com/inward/record.url?scp=80053329514&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=80053329514&partnerID=8YFLogxK

U2 - 10.1111/j.1365-2605.2010.01100.x

DO - 10.1111/j.1365-2605.2010.01100.x

M3 - Article

C2 - 20969598

AN - SCOPUS:80053329514

VL - 34

SP - 420

EP - 429

JO - International Journal of Andrology

JF - International Journal of Andrology

SN - 0105-6263

IS - 5 PART 1

ER -