Molecular signatures of the primitive prostate stem cell niche reveal novel mesenchymal-epithelial signaling pathways
Signals between stem cells and stroma are important in establishing the stem cell niche. However, very little is known about the regulation of any mammalian stem cell niche as pure isolates of stem cells and their adjacent mesenchyme are not readily available. The prostate offers a unique model to s...
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| creator | Blum, Roy Gupta, Rashmi Burger, Patricia E Ontiveros, Christopher S Salm, Sarah N Xiong, Xiaozhong Kamb, Alexander Wesche, Holger Marshall, Lisa Cutler, Gene Wang, Xiangyun Zavadil, Jiri Moscatelli, David Wilson, E Lynette |
| description | Signals between stem cells and stroma are important in establishing the stem cell niche. However, very little is known about the regulation of any mammalian stem cell niche as pure isolates of stem cells and their adjacent mesenchyme are not readily available. The prostate offers a unique model to study signals between stem cells and their adjacent stroma as in the embryonic prostate stem cell niche, the urogenital sinus mesenchyme is easily separated from the epithelial stem cells. Here we investigate the distinctive molecular signals of these two stem cell compartments in a mammalian system.
We isolated fetal murine urogenital sinus epithelium and urogenital sinus mesenchyme and determined their differentially expressed genes. To distinguish transcripts that are shared by other developing epithelial/mesenchymal compartments from those that pertain to the prostate stem cell niche, we also determined the global gene expression of epidermis and dermis of the same embryos. Our analysis indicates that several of the key transcriptional components that are predicted to be active in the embryonic prostate stem cell niche regulate processes such as self-renewal (e.g., E2f and Ap2), lipid metabolism (e.g., Srebp1) and cell migration (e.g., Areb6 and Rreb1). Several of the enriched promoter binding motifs are shared between the prostate epithelial/mesenchymal compartments and their epidermis/dermis counterparts, indicating their likely relevance in epithelial/mesenchymal signaling in primitive cellular compartments. Based on differential gene expression we also defined ligand-receptor interactions that may be part of the molecular interplay of the embryonic prostate stem cell niche.
We provide a comprehensive description of the transcriptional program of the major regulators that are likely to control the cellular interactions in the embryonic prostatic stem cell niche, many of which may be common to mammalian niches in general. This study provides a comprehensive source for further studies of mesenchymal/epithelial interactions in the prostate stem cell niche. The elucidation of pathways in the normal primitive niche may provide greater insight into mechanisms subverted during abnormal proliferative and oncogenic processes. Understanding these events may result in the development of specific targeted therapies for prostatic diseases such as benign prostatic hypertrophy and carcinomas. |
| doi_str_mv | 10.1371/journal.pone.0013024 |
| format | Article |
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We isolated fetal murine urogenital sinus epithelium and urogenital sinus mesenchyme and determined their differentially expressed genes. To distinguish transcripts that are shared by other developing epithelial/mesenchymal compartments from those that pertain to the prostate stem cell niche, we also determined the global gene expression of epidermis and dermis of the same embryos. Our analysis indicates that several of the key transcriptional components that are predicted to be active in the embryonic prostate stem cell niche regulate processes such as self-renewal (e.g., E2f and Ap2), lipid metabolism (e.g., Srebp1) and cell migration (e.g., Areb6 and Rreb1). Several of the enriched promoter binding motifs are shared between the prostate epithelial/mesenchymal compartments and their epidermis/dermis counterparts, indicating their likely relevance in epithelial/mesenchymal signaling in primitive cellular compartments. Based on differential gene expression we also defined ligand-receptor interactions that may be part of the molecular interplay of the embryonic prostate stem cell niche.
We provide a comprehensive description of the transcriptional program of the major regulators that are likely to control the cellular interactions in the embryonic prostatic stem cell niche, many of which may be common to mammalian niches in general. This study provides a comprehensive source for further studies of mesenchymal/epithelial interactions in the prostate stem cell niche. The elucidation of pathways in the normal primitive niche may provide greater insight into mechanisms subverted during abnormal proliferative and oncogenic processes. Understanding these events may result in the development of specific targeted therapies for prostatic diseases such as benign prostatic hypertrophy and carcinomas.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0013024</identifier><identifier>PMID: 20941365</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Animals ; Biology ; Bone marrow ; Carcinoma ; Cell Biology/Developmental Molecular Mechanisms ; Cell Communication ; Cell migration ; Cell self-renewal ; Compartments ; Dermis ; Developmental Biology/Stem Cells ; E2F protein ; Embryos ; Epidermis ; Epithelial Cells - metabolism ; Epithelium ; Fetuses ; Gene expression ; Genes ; Growth factors ; Hypertrophy ; Immunology ; Lipid metabolism ; Male ; Mammals ; Medicine ; Mesenchyme ; Mesoderm - cytology ; Mesoderm - embryology ; Mesoderm - metabolism ; Metabolism ; Metastasis ; Mice ; Mice, Inbred C57BL ; Prostate ; Prostate - cytology ; Prostate - embryology ; Prostate - metabolism ; Prostate cancer ; Regulators ; Rodents ; Signal Transduction ; Signaling ; Sinus ; Sinuses ; Stem Cell Niche - cytology ; Stem Cell Niche - embryology ; Stem Cell Niche - metabolism ; Stem cell transplantation ; Stem cells ; Stroma ; Transcription ; Tumors ; Urology/Prostate Cancer</subject><ispartof>PloS one, 2010-09, Vol.5 (9), p.e13024</ispartof><rights>COPYRIGHT 2010 Public Library of Science</rights><rights>2010 Blum et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Blum et al. 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c691t-534935d55c681e014ac9b14b4c03bb3859ce1b3f99cff8521a718021e5890f083</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2948007/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2948007/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20941365$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Blum, Roy</creatorcontrib><creatorcontrib>Gupta, Rashmi</creatorcontrib><creatorcontrib>Burger, Patricia E</creatorcontrib><creatorcontrib>Ontiveros, Christopher S</creatorcontrib><creatorcontrib>Salm, Sarah N</creatorcontrib><creatorcontrib>Xiong, Xiaozhong</creatorcontrib><creatorcontrib>Kamb, Alexander</creatorcontrib><creatorcontrib>Wesche, Holger</creatorcontrib><creatorcontrib>Marshall, Lisa</creatorcontrib><creatorcontrib>Cutler, Gene</creatorcontrib><creatorcontrib>Wang, Xiangyun</creatorcontrib><creatorcontrib>Zavadil, Jiri</creatorcontrib><creatorcontrib>Moscatelli, David</creatorcontrib><creatorcontrib>Wilson, E Lynette</creatorcontrib><title>Molecular signatures of the primitive prostate stem cell niche reveal novel mesenchymal-epithelial signaling pathways</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Signals between stem cells and stroma are important in establishing the stem cell niche. However, very little is known about the regulation of any mammalian stem cell niche as pure isolates of stem cells and their adjacent mesenchyme are not readily available. The prostate offers a unique model to study signals between stem cells and their adjacent stroma as in the embryonic prostate stem cell niche, the urogenital sinus mesenchyme is easily separated from the epithelial stem cells. Here we investigate the distinctive molecular signals of these two stem cell compartments in a mammalian system.
We isolated fetal murine urogenital sinus epithelium and urogenital sinus mesenchyme and determined their differentially expressed genes. To distinguish transcripts that are shared by other developing epithelial/mesenchymal compartments from those that pertain to the prostate stem cell niche, we also determined the global gene expression of epidermis and dermis of the same embryos. Our analysis indicates that several of the key transcriptional components that are predicted to be active in the embryonic prostate stem cell niche regulate processes such as self-renewal (e.g., E2f and Ap2), lipid metabolism (e.g., Srebp1) and cell migration (e.g., Areb6 and Rreb1). Several of the enriched promoter binding motifs are shared between the prostate epithelial/mesenchymal compartments and their epidermis/dermis counterparts, indicating their likely relevance in epithelial/mesenchymal signaling in primitive cellular compartments. Based on differential gene expression we also defined ligand-receptor interactions that may be part of the molecular interplay of the embryonic prostate stem cell niche.
We provide a comprehensive description of the transcriptional program of the major regulators that are likely to control the cellular interactions in the embryonic prostatic stem cell niche, many of which may be common to mammalian niches in general. This study provides a comprehensive source for further studies of mesenchymal/epithelial interactions in the prostate stem cell niche. The elucidation of pathways in the normal primitive niche may provide greater insight into mechanisms subverted during abnormal proliferative and oncogenic processes. Understanding these events may result in the development of specific targeted therapies for prostatic diseases such as benign prostatic hypertrophy and carcinomas.</description><subject>Analysis</subject><subject>Animals</subject><subject>Biology</subject><subject>Bone marrow</subject><subject>Carcinoma</subject><subject>Cell Biology/Developmental Molecular Mechanisms</subject><subject>Cell Communication</subject><subject>Cell migration</subject><subject>Cell self-renewal</subject><subject>Compartments</subject><subject>Dermis</subject><subject>Developmental Biology/Stem Cells</subject><subject>E2F protein</subject><subject>Embryos</subject><subject>Epidermis</subject><subject>Epithelial Cells - metabolism</subject><subject>Epithelium</subject><subject>Fetuses</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Growth factors</subject><subject>Hypertrophy</subject><subject>Immunology</subject><subject>Lipid metabolism</subject><subject>Male</subject><subject>Mammals</subject><subject>Medicine</subject><subject>Mesenchyme</subject><subject>Mesoderm - cytology</subject><subject>Mesoderm - embryology</subject><subject>Mesoderm - metabolism</subject><subject>Metabolism</subject><subject>Metastasis</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Prostate</subject><subject>Prostate - cytology</subject><subject>Prostate - embryology</subject><subject>Prostate - metabolism</subject><subject>Prostate cancer</subject><subject>Regulators</subject><subject>Rodents</subject><subject>Signal Transduction</subject><subject>Signaling</subject><subject>Sinus</subject><subject>Sinuses</subject><subject>Stem Cell Niche - cytology</subject><subject>Stem Cell Niche - embryology</subject><subject>Stem Cell Niche - metabolism</subject><subject>Stem cell transplantation</subject><subject>Stem cells</subject><subject>Stroma</subject><subject>Transcription</subject><subject>Tumors</subject><subject>Urology/Prostate 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signatures of the primitive prostate stem cell niche reveal novel mesenchymal-epithelial signaling pathways</title><author>Blum, Roy ; Gupta, Rashmi ; Burger, Patricia E ; Ontiveros, Christopher S ; Salm, Sarah N ; Xiong, Xiaozhong ; Kamb, Alexander ; Wesche, Holger ; Marshall, Lisa ; Cutler, Gene ; Wang, Xiangyun ; Zavadil, Jiri ; Moscatelli, David ; Wilson, E Lynette</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c691t-534935d55c681e014ac9b14b4c03bb3859ce1b3f99cff8521a718021e5890f083</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Analysis</topic><topic>Animals</topic><topic>Biology</topic><topic>Bone marrow</topic><topic>Carcinoma</topic><topic>Cell Biology/Developmental Molecular Mechanisms</topic><topic>Cell Communication</topic><topic>Cell migration</topic><topic>Cell self-renewal</topic><topic>Compartments</topic><topic>Dermis</topic><topic>Developmental 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Alexander</au><au>Wesche, Holger</au><au>Marshall, Lisa</au><au>Cutler, Gene</au><au>Wang, Xiangyun</au><au>Zavadil, Jiri</au><au>Moscatelli, David</au><au>Wilson, E Lynette</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Molecular signatures of the primitive prostate stem cell niche reveal novel mesenchymal-epithelial signaling pathways</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2010-09-30</date><risdate>2010</risdate><volume>5</volume><issue>9</issue><spage>e13024</spage><pages>e13024-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Signals between stem cells and stroma are important in establishing the stem cell niche. However, very little is known about the regulation of any mammalian stem cell niche as pure isolates of stem cells and their adjacent mesenchyme are not readily available. The prostate offers a unique model to study signals between stem cells and their adjacent stroma as in the embryonic prostate stem cell niche, the urogenital sinus mesenchyme is easily separated from the epithelial stem cells. Here we investigate the distinctive molecular signals of these two stem cell compartments in a mammalian system.
We isolated fetal murine urogenital sinus epithelium and urogenital sinus mesenchyme and determined their differentially expressed genes. To distinguish transcripts that are shared by other developing epithelial/mesenchymal compartments from those that pertain to the prostate stem cell niche, we also determined the global gene expression of epidermis and dermis of the same embryos. Our analysis indicates that several of the key transcriptional components that are predicted to be active in the embryonic prostate stem cell niche regulate processes such as self-renewal (e.g., E2f and Ap2), lipid metabolism (e.g., Srebp1) and cell migration (e.g., Areb6 and Rreb1). Several of the enriched promoter binding motifs are shared between the prostate epithelial/mesenchymal compartments and their epidermis/dermis counterparts, indicating their likely relevance in epithelial/mesenchymal signaling in primitive cellular compartments. Based on differential gene expression we also defined ligand-receptor interactions that may be part of the molecular interplay of the embryonic prostate stem cell niche.
We provide a comprehensive description of the transcriptional program of the major regulators that are likely to control the cellular interactions in the embryonic prostatic stem cell niche, many of which may be common to mammalian niches in general. This study provides a comprehensive source for further studies of mesenchymal/epithelial interactions in the prostate stem cell niche. The elucidation of pathways in the normal primitive niche may provide greater insight into mechanisms subverted during abnormal proliferative and oncogenic processes. Understanding these events may result in the development of specific targeted therapies for prostatic diseases such as benign prostatic hypertrophy and carcinomas.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>20941365</pmid><doi>10.1371/journal.pone.0013024</doi><tpages>e13024</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2010-09, Vol.5 (9), p.e13024 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1292581547 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Analysis Animals Biology Bone marrow Carcinoma Cell Biology/Developmental Molecular Mechanisms Cell Communication Cell migration Cell self-renewal Compartments Dermis Developmental Biology/Stem Cells E2F protein Embryos Epidermis Epithelial Cells - metabolism Epithelium Fetuses Gene expression Genes Growth factors Hypertrophy Immunology Lipid metabolism Male Mammals Medicine Mesenchyme Mesoderm - cytology Mesoderm - embryology Mesoderm - metabolism Metabolism Metastasis Mice Mice, Inbred C57BL Prostate Prostate - cytology Prostate - embryology Prostate - metabolism Prostate cancer Regulators Rodents Signal Transduction Signaling Sinus Sinuses Stem Cell Niche - cytology Stem Cell Niche - embryology Stem Cell Niche - metabolism Stem cell transplantation Stem cells Stroma Transcription Tumors Urology/Prostate Cancer |
| title | Molecular signatures of the primitive prostate stem cell niche reveal novel mesenchymal-epithelial signaling pathways |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-08T11%3A52%3A57IST&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=Molecular%20signatures%20of%20the%20primitive%20prostate%20stem%20cell%20niche%20reveal%20novel%20mesenchymal-epithelial%20signaling%20pathways&rft.jtitle=PloS%20one&rft.au=Blum,%20Roy&rft.date=2010-09-30&rft.volume=5&rft.issue=9&rft.spage=e13024&rft.pages=e13024-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0013024&rft_dat=%3Cgale_plos_%3EA473856353%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=1292581547&rft_id=info:pmid/20941365&rft_galeid=A473856353&rft_doaj_id=oai_doaj_org_article_edc2e4d8f0b5421992293e7bdc8e072e&rfr_iscdi=true |