A transcriptome-wide screen for mRNAs enriched in fetal Leydig cells: CRHR1 agonism stimulates rat and mouse fetal testis steroidogenesis
Fetal testis steroidogenesis plays an important role in the reproductive development of the male fetus. While regulators of certain aspects of steroidogenesis are known, the initial driver of steroidogenesis in the human and rodent fetal testis is unclear. Through comparative analysis of rodent feta...
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| description | Fetal testis steroidogenesis plays an important role in the reproductive development of the male fetus. While regulators of certain aspects of steroidogenesis are known, the initial driver of steroidogenesis in the human and rodent fetal testis is unclear. Through comparative analysis of rodent fetal testis microarray datasets, 54 candidate fetal Leydig cell-specific genes were identified. Fetal mouse testis interstitial expression of a subset of these genes with unknown expression (Crhr1, Gramd1b, Itih5, Vgll3, and Vsnl1) was verified by whole-mount in situ hybridization. Among the candidate fetal Leydig cell-specific factors, three receptors (CRHR1, PRLR, and PROKR2) were tested for a steroidogenic function using ex vivo fetal testes treated with receptor agonists (CRH, PRL, and PROK2). While PRL and PROK2 had no effect, CRH, at low (approximately 1 to 10) nM concentration, increased expression of the steroidogenic genes Cyp11a1, Cyp17a1, Scarb1, and Star in GD15 mouse and GD17 rat testes, and in conjunction, testosterone production was increased. Exposure of GD15 fetal mouse testis to a specific CRHR1 antagonist blunted the CRH-induced steroidogenic gene expression and testosterone responses. Similar to ex vivo rodent fetal testes, ≥ 10 nM CRH exposure of MA-10 Leydig cells increased steroidogenic pathway mRNA and progesterone levels, showing CRH can enhance steroidogenesis by directly targeting Leydig cells. Crh mRNA expression was observed in rodent fetal hypothalamus, and CRH peptide was detected in rodent amniotic fluid. Together, these data provide a resource for discovering factors controlling fetal Leydig cell biology and suggest that CRHR1 activation by CRH stimulates rat and mouse fetal Leydig cell steroidogenesis in vivo. |
| doi_str_mv | 10.1371/journal.pone.0047359 |
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While regulators of certain aspects of steroidogenesis are known, the initial driver of steroidogenesis in the human and rodent fetal testis is unclear. Through comparative analysis of rodent fetal testis microarray datasets, 54 candidate fetal Leydig cell-specific genes were identified. Fetal mouse testis interstitial expression of a subset of these genes with unknown expression (Crhr1, Gramd1b, Itih5, Vgll3, and Vsnl1) was verified by whole-mount in situ hybridization. Among the candidate fetal Leydig cell-specific factors, three receptors (CRHR1, PRLR, and PROKR2) were tested for a steroidogenic function using ex vivo fetal testes treated with receptor agonists (CRH, PRL, and PROK2). While PRL and PROK2 had no effect, CRH, at low (approximately 1 to 10) nM concentration, increased expression of the steroidogenic genes Cyp11a1, Cyp17a1, Scarb1, and Star in GD15 mouse and GD17 rat testes, and in conjunction, testosterone production was increased. Exposure of GD15 fetal mouse testis to a specific CRHR1 antagonist blunted the CRH-induced steroidogenic gene expression and testosterone responses. Similar to ex vivo rodent fetal testes, ≥ 10 nM CRH exposure of MA-10 Leydig cells increased steroidogenic pathway mRNA and progesterone levels, showing CRH can enhance steroidogenesis by directly targeting Leydig cells. Crh mRNA expression was observed in rodent fetal hypothalamus, and CRH peptide was detected in rodent amniotic fluid. Together, these data provide a resource for discovering factors controlling fetal Leydig cell biology and suggest that CRHR1 activation by CRH stimulates rat and mouse fetal Leydig cell steroidogenesis in vivo.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0047359</identifier><identifier>PMID: 23133512</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amniotic fluid ; Amniotic Fluid - metabolism ; Animals ; Biology ; Biomedical research ; C-Reactive Protein - metabolism ; Cells (Biology) ; Comparative analysis ; Developmental biology ; DNA microarrays ; Drinking water ; Endocrinology ; Environmental health ; Exposure ; Fetuses ; Gastrointestinal Hormones - metabolism ; Gene expression ; Gene Expression Regulation, Developmental ; Genes ; Genomics ; Health sciences ; Hypothalamus ; Immunohistochemistry - methods ; Laboratory animals ; Leydig cells ; Leydig Cells - metabolism ; Male ; Medicine ; Messenger RNA ; Mice ; Neuropeptides - metabolism ; Nutrition research ; Oligonucleotide Array Sequence Analysis ; Progesterone ; Prolactin - biosynthesis ; Proteins ; Rats ; Rats, Sprague-Dawley ; Receptor mechanisms ; Receptors ; Receptors, Corticotropin-Releasing Hormone - agonists ; Receptors, Corticotropin-Releasing Hormone - physiology ; Regulators ; RNA, Messenger - metabolism ; Rodents ; Steroidogenesis ; Steroids - metabolism ; Stress response ; Testes ; Testis - embryology ; Testosterone ; Testosterone - metabolism ; Time Factors ; Toxicology ; Urocortins - metabolism ; Wide screen</subject><ispartof>PloS one, 2012-10, Vol.7 (10), p.e47359-e47359</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>2012. This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. 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While regulators of certain aspects of steroidogenesis are known, the initial driver of steroidogenesis in the human and rodent fetal testis is unclear. Through comparative analysis of rodent fetal testis microarray datasets, 54 candidate fetal Leydig cell-specific genes were identified. Fetal mouse testis interstitial expression of a subset of these genes with unknown expression (Crhr1, Gramd1b, Itih5, Vgll3, and Vsnl1) was verified by whole-mount in situ hybridization. Among the candidate fetal Leydig cell-specific factors, three receptors (CRHR1, PRLR, and PROKR2) were tested for a steroidogenic function using ex vivo fetal testes treated with receptor agonists (CRH, PRL, and PROK2). While PRL and PROK2 had no effect, CRH, at low (approximately 1 to 10) nM concentration, increased expression of the steroidogenic genes Cyp11a1, Cyp17a1, Scarb1, and Star in GD15 mouse and GD17 rat testes, and in conjunction, testosterone production was increased. Exposure of GD15 fetal mouse testis to a specific CRHR1 antagonist blunted the CRH-induced steroidogenic gene expression and testosterone responses. Similar to ex vivo rodent fetal testes, ≥ 10 nM CRH exposure of MA-10 Leydig cells increased steroidogenic pathway mRNA and progesterone levels, showing CRH can enhance steroidogenesis by directly targeting Leydig cells. Crh mRNA expression was observed in rodent fetal hypothalamus, and CRH peptide was detected in rodent amniotic fluid. Together, these data provide a resource for discovering factors controlling fetal Leydig cell biology and suggest that CRHR1 activation by CRH stimulates rat and mouse fetal Leydig cell steroidogenesis in vivo.</description><subject>Amniotic fluid</subject><subject>Amniotic Fluid - metabolism</subject><subject>Animals</subject><subject>Biology</subject><subject>Biomedical research</subject><subject>C-Reactive Protein - metabolism</subject><subject>Cells (Biology)</subject><subject>Comparative analysis</subject><subject>Developmental biology</subject><subject>DNA microarrays</subject><subject>Drinking water</subject><subject>Endocrinology</subject><subject>Environmental health</subject><subject>Exposure</subject><subject>Fetuses</subject><subject>Gastrointestinal Hormones - metabolism</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Genes</subject><subject>Genomics</subject><subject>Health sciences</subject><subject>Hypothalamus</subject><subject>Immunohistochemistry - 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While regulators of certain aspects of steroidogenesis are known, the initial driver of steroidogenesis in the human and rodent fetal testis is unclear. Through comparative analysis of rodent fetal testis microarray datasets, 54 candidate fetal Leydig cell-specific genes were identified. Fetal mouse testis interstitial expression of a subset of these genes with unknown expression (Crhr1, Gramd1b, Itih5, Vgll3, and Vsnl1) was verified by whole-mount in situ hybridization. Among the candidate fetal Leydig cell-specific factors, three receptors (CRHR1, PRLR, and PROKR2) were tested for a steroidogenic function using ex vivo fetal testes treated with receptor agonists (CRH, PRL, and PROK2). While PRL and PROK2 had no effect, CRH, at low (approximately 1 to 10) nM concentration, increased expression of the steroidogenic genes Cyp11a1, Cyp17a1, Scarb1, and Star in GD15 mouse and GD17 rat testes, and in conjunction, testosterone production was increased. Exposure of GD15 fetal mouse testis to a specific CRHR1 antagonist blunted the CRH-induced steroidogenic gene expression and testosterone responses. Similar to ex vivo rodent fetal testes, ≥ 10 nM CRH exposure of MA-10 Leydig cells increased steroidogenic pathway mRNA and progesterone levels, showing CRH can enhance steroidogenesis by directly targeting Leydig cells. Crh mRNA expression was observed in rodent fetal hypothalamus, and CRH peptide was detected in rodent amniotic fluid. Together, these data provide a resource for discovering factors controlling fetal Leydig cell biology and suggest that CRHR1 activation by CRH stimulates rat and mouse fetal Leydig cell steroidogenesis in vivo.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23133512</pmid><doi>10.1371/journal.pone.0047359</doi><tpages>e47359</tpages><oa>free_for_read</oa></addata></record> |
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| recordid | cdi_plos_journals_1327131294 |
| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Amniotic fluid Amniotic Fluid - metabolism Animals Biology Biomedical research C-Reactive Protein - metabolism Cells (Biology) Comparative analysis Developmental biology DNA microarrays Drinking water Endocrinology Environmental health Exposure Fetuses Gastrointestinal Hormones - metabolism Gene expression Gene Expression Regulation, Developmental Genes Genomics Health sciences Hypothalamus Immunohistochemistry - methods Laboratory animals Leydig cells Leydig Cells - metabolism Male Medicine Messenger RNA Mice Neuropeptides - metabolism Nutrition research Oligonucleotide Array Sequence Analysis Progesterone Prolactin - biosynthesis Proteins Rats Rats, Sprague-Dawley Receptor mechanisms Receptors Receptors, Corticotropin-Releasing Hormone - agonists Receptors, Corticotropin-Releasing Hormone - physiology Regulators RNA, Messenger - metabolism Rodents Steroidogenesis Steroids - metabolism Stress response Testes Testis - embryology Testosterone Testosterone - metabolism Time Factors Toxicology Urocortins - metabolism Wide screen |
| title | A transcriptome-wide screen for mRNAs enriched in fetal Leydig cells: CRHR1 agonism stimulates rat and mouse fetal testis steroidogenesis |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-21T18%3A45%3A24IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=A%20transcriptome-wide%20screen%20for%20mRNAs%20enriched%20in%20fetal%20Leydig%20cells:%20CRHR1%20agonism%20stimulates%20rat%20and%20mouse%20fetal%20testis%20steroidogenesis&rft.jtitle=PloS%20one&rft.au=McDowell,%20Erin%20N&rft.date=2012-10-25&rft.volume=7&rft.issue=10&rft.spage=e47359&rft.epage=e47359&rft.pages=e47359-e47359&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0047359&rft_dat=%3Cgale_plos_%3EA477041538%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1327131294&rft_id=info:pmid/23133512&rft_galeid=A477041538&rft_doaj_id=oai_doaj_org_article_6ec08728219946f590bf12b9702ba6d5&rfr_iscdi=true |