C-Type Natriuretic Peptide/Natriuretic Peptide Receptor 2 Is Involved in Cell Proliferation and Testosterone Production in Mouse Leydig Cells

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Abstract

Purpose

This study investigated the role of natriuretic peptide receptor 2 (NPR2) on cell proliferation and testosterone secretion in mouse Leydig cells.

Materials and Methods

Mouse testis of different postnatal stages was isolated to detect the expression C-type natriuretic peptide (CNP) and its receptor NPR2 by quantitative reverse transcription polymerase chain reaction (RT-qPCR). Leydig cells isolated from mouse testis were cultured and treated with shNPR2 lentiviruses or CNP. And then the cyclic guanosine monophosphate production, testosterone secretion, cell proliferation, cell cycle and cell apoptosis in mouse Leydig cells were analyzed by ELISA, RT-qPCR, Cell Counting Kit-8, and flow cytometry. Moreover, the expression of NPR2, cell cycle, apoptosis proliferation and cell cycle related gene were detected by RT-qPCR and Western blot.

Results

Knockdown of NPR2 by RNAi resulted in S phase cell cycle arrest, cell apoptosis, and decreased testosterone secretion in mouse Leydig cells.

Conclusions

Our study provides more evidences to better understand the function of CNP/NPR2 pathway in male reproduction, which may help us to treat male infertility.

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Most cited references 28

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Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes.

Meijia Zhang, You-Qiang Su, Koji Sugiura … (2010)

Granulosa cells of mammalian Graafian follicles maintain oocytes in meiotic arrest, which prevents their precocious maturation. We show that mouse mural granulosa cells, which line the follicle wall, express natriuretic peptide precursor type C (Nppc) messenger RNA (mRNA), whereas cumulus cells surrounding oocytes express mRNA of the NPPC receptor NPR2, a guanylyl cyclase. NPPC increased cGMP levels in cumulus cells and oocytes and inhibited meiotic resumption in vitro. Meiotic arrest was not sustained in most Graafian follicles of Nppc or Npr2 mutant mice, and meiosis resumed precociously. Oocyte-derived paracrine factors promoted cumulus cell expression of Npr2 mRNA. Therefore, the granulosa cell ligand NPPC and its receptor NPR2 in cumulus cells prevent precocious meiotic maturation, which is critical for maturation and ovulation synchrony and for normal female fertility.

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Estradiol promotes and maintains cumulus cell expression of natriuretic peptide receptor 2 (NPR2) and meiotic arrest in mouse oocytes in vitro.

Qiang Su, Koji Sugiura, Karen Wigglesworth … (2011)

Natriuretic peptide type C (NPPC) and its cognate receptor natriuretic peptide receptor 2 (NPR2) are essential for maintaining meiotic arrest in mouse oocytes residing in Graafian follicles. Cumulus cells, which are associated with the oocyte, express the receptor NPR2, a guanylyl cyclase, whereas mural granulosa cells express ligand NPPC. This study determined the temporal expression of Npr2 and the hormonal factors that participate in regulating its expression and, thereby, in oocyte meiotic arrest. Stimulation of follicular development in vivo with equine chorionic gonadotropin (eCG) promoted expression of Npr2 mRNA by cumulus cells and some periantral mural granulosa cells. However, FSH did not elevate the levels of Npr2 mRNA in cultured cumulus-oocyte complexes (COCs) isolated from mice not stimulated in vivo with eCG. Nevertheless, estradiol elevated expression of this transcript in vitro to the same steady-state level found in COCs isolated from eCG-stimulated follicles in vivo. Expression of Npr2 mRNA was rapidly reduced in COCs in vitro after isolation from eCG-primed mice unless maintained in culture with estradiol. The ability of NPPC to maintain meiotic arrest in cultured COCs was transient unless culture was in estradiol-containing medium. Ability of cumulus cells to produce cyclic GMP, which is required for the maintenance of meiotic arrest, was also lost in the absence of estradiol, indicating that estradiol is required to maintain functional NPR2 receptors on cumulus cells in vitro. It is concluded that estradiol promotes and maintains expression of NPR2 in cumulus cells and participates in NPPC-mediated maintenance of oocyte meiotic arrest in vitro.

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Molecular regulation of steroidogenesis in endocrine Leydig cells.

Jacques J Tremblay (2015)

Steroid hormones regulate essential physiological processes and inadequate levels are associated with various pathological conditions. Consequently, the process of steroid hormone biosynthesis is finely regulated. In the testis, the main steroidogenic cells are the Leydig cells. There are two distinct populations of Leydig cells that arise during development: fetal and adult Leydig cells. Fetal Leydig cells are responsible for masculinizing the male urogenital tract and inducing testis descent. These cells atrophy shortly after birth and do not contribute to the adult Leydig cell population. Adult Leydig cells derive from undifferentiated precursors present after birth and become fully steroidogenic at puberty. The differentiation of both Leydig cell populations is controlled by locally produced paracrine factors and by endocrine hormones. In fully differentially and steroidogenically active Leydig cells, androgen production and hormone-responsiveness involve various signaling pathways and downstream transcription factors. This review article focuses on recent developments regarding the origin and function of Leydig cells, the regulation of their differentiation by signaling molecules, hormones, and structural changes, the signaling pathways, kinases, and transcription factors involved in their differentiation and in mediating LH-responsiveness, as well as the fine-tuning mechanisms that ensure adequate production steroid hormones.

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Author and article information

Journal

Journal ID (nlm-ta): World J Mens Health

Journal ID (iso-abbrev): World J Mens Health

Journal ID (publisher-id): WJMH

Title: The World Journal of Men's Health

Publisher: Korean Society for Sexual Medicine and Andrology

ISSN (Print): 2287-4208

ISSN (Electronic): 2287-4690

Publication date (Print): May 2019

Publication date (Electronic): 23 October 2018

Volume: 37

Issue: 2

Pages: 186-198

Affiliations

[1 ]College of Basic Medical Science, Jiujiang, China.

[2 ]Clinical Skills Center, Affiliated Hospital of Jiujiang University, Jiujiang, China.

[3 ]Key Laboratory of System Bio-medicine of Jiangxi Province, Jiujiang University, Jiujiang, China.

Author notes

Correspondence to: Lei Yang. College of Basic Medical Science, Jiujiang University, 17 Lufeng Rd, Xunyang Qu, Jiujiang Shi, Jiangxi Sheng 332000, China. Tel: +86-0792-8570043, Fax: +86-0792-8577050, yangleigeili@ 123456163.com

Correspondence to: Shaoxin Huang. College of Basic Medical Science, Jiujiang University, 17 Lufeng Rd, Xunyang Qu, Jiujiang Shi, Jiangxi Sheng 332000, China. Tel: +86-0792-8570043, Fax: +86-0792-8577050, 517159865@ 123456qq.com

Author information

Lei Yang https://orcid.org/0000-0001-8859-9692

Lanjie Lei https://orcid.org/0000-0003-1773-1646

Qihan Zhao https://orcid.org/0000-0003-0357-8863

Ying Gong https://orcid.org/0000-0003-1451-4902

Gaopeng Guan https://orcid.org/0000-0001-9946-2712

Shaoxin Huang https://orcid.org/0000-0001-9801-4133

Article

DOI: 10.5534/wjmh.180041

PMC ID: 6479080

PubMed ID: 30358184

SO-VID: b6f74ead-449d-42be-9664-9685c3993b0e

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

History

Date received : 21 May 2018

Date revision received : 10 September 2018

Date accepted : 10 September 2018

Funding

Funded by: National Natural Science Foundation of China, CrossRef https://doi.org/10.13039/501100001809;

Award ID: 81660535

Funded by: Education Department of Jiangxi Province, CrossRef https://doi.org/10.13039/501100009102;

C-Type Natriuretic Peptide/Natriuretic Peptide Receptor 2 Is Involved in Cell Proliferation and Testosterone Production in Mouse Leydig Cells

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Abstract

Purpose

Materials and Methods

Results

Conclusions

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Most cited references 28

Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes.

Estradiol promotes and maintains cumulus cell expression of natriuretic peptide receptor 2 (NPR2) and meiotic arrest in mouse oocytes in vitro.

Molecular regulation of steroidogenesis in endocrine Leydig cells.

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