Expansion of prostate epithelial progenitor cells after inflammation of the mouse prostate

Prostatic inflammation is a nearly ubiquitous pathological feature observed in specimens from benign prostate hyperplasia and prostate cancer patients. The microenvironment of the inflamed prostate is highly reactive, and epithelial hyperplasia is a hallmark feature of inflamed prostates. How inflam...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:American journal of physiology. Renal physiology 2015-06, Vol.308 (12), p.F1421-F1430
Hauptverfasser: Wang, Liang, Zoetemelk, Marloes, Chitteti, Brahmananda R, Ratliff, Timothy L, Myers, Jason D, Srour, Edward F, Broxmeyer, Hal, Jerde, Travis J
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page F1430
container_issue 12
container_start_page F1421
container_title American journal of physiology. Renal physiology
container_volume 308
creator Wang, Liang
Zoetemelk, Marloes
Chitteti, Brahmananda R
Ratliff, Timothy L
Myers, Jason D
Srour, Edward F
Broxmeyer, Hal
Jerde, Travis J
description Prostatic inflammation is a nearly ubiquitous pathological feature observed in specimens from benign prostate hyperplasia and prostate cancer patients. The microenvironment of the inflamed prostate is highly reactive, and epithelial hyperplasia is a hallmark feature of inflamed prostates. How inflammation orchestrates epithelial proliferation as part of its repair and recovery action is not well understood. Here, we report that a novel epithelial progenitor cell population is induced to expand during inflammation. We used sphere culture assays, immunofluorescence, and flow cytometry to show that this population is increased in bacterially induced inflamed mouse prostates relative to naïve control prostates. We confirmed from previous reports that this population exclusively possesses the ability to regrow entire prostatic structures from single cell culture using renal grafts. In addition, putative progenitor cells harvested from inflamed animals have greater aggregation capacity than those isolated from naïve control prostates. Expansion of this critical cell population requires IL-1 signaling, as IL-1 receptor 1-null mice exhibit inflammation similar to wild-type inflamed animals but exhibit significantly reduced progenitor cell proliferation and hyperplasia. These data demonstrate that inflammation promotes hyperplasia in the mouse prostatic epithelium by inducing the expansion of a selected epithelial progenitor cell population in an IL-1 receptor-dependent manner. These findings may have significant impact on our understanding of how inflammation promotes proliferative diseases such as benign prostatic hyperplasia and prostate cancer, both of which depend on expansion of cells that exhibit a progenitor-like nature.
doi_str_mv 10.1152/ajprenal.00488.2014
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4469888</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1689621869</sourcerecordid><originalsourceid>FETCH-LOGICAL-c433t-8a30b75b1a0a8dcc4bd1c10521f03e173d484e124bb061ddc19d2f4f2f8842643</originalsourceid><addsrcrecordid>eNpdkV1LBCEYhSWKvn9BEAPddDObrzqzehNE9AVBNwXRjTgzuusyM07qRv37nNqW6kbF95yDxwehI8ATgIKcqcXgda_aCcaM8wnBwDbQbpqQHFhZbqazoJDzYvq8g_ZCWGCMAQhsox1SCFKkZRe9XL0Pqg_W9Zkz2eBdiCrqTA82znVrVTvezXRvo_NZrds2ZMpE7TPbm1Z1nYora5JnnVsGvQ45QFtGtUEfrvZ99HR99Xh5m98_3NxdXtznNaM05lxRXE2LChRWvKlrVjVQAy4IGEw1TGnDONNAWFXhEpqmBtEQwwwxnDNSMrqPzr9zh2XV6abWffSqlYO3nfIf0ikr_056O5cz9yYZKwXnPAWcrgK8e13qEGVnw9hV9To1klByURLgpUjSk3_ShVv6BGFUCcJEIdioot-qOn1F8NqsHwNYjuzkDzv5xU6O7JLr-HePtecHFv0EIrGZlA</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1692495949</pqid></control><display><type>article</type><title>Expansion of prostate epithelial progenitor cells after inflammation of the mouse prostate</title><source>MEDLINE</source><source>American Physiological Society</source><source>EZB-FREE-00999 freely available EZB journals</source><source>Alma/SFX Local Collection</source><creator>Wang, Liang ; Zoetemelk, Marloes ; Chitteti, Brahmananda R ; Ratliff, Timothy L ; Myers, Jason D ; Srour, Edward F ; Broxmeyer, Hal ; Jerde, Travis J</creator><creatorcontrib>Wang, Liang ; Zoetemelk, Marloes ; Chitteti, Brahmananda R ; Ratliff, Timothy L ; Myers, Jason D ; Srour, Edward F ; Broxmeyer, Hal ; Jerde, Travis J</creatorcontrib><description>Prostatic inflammation is a nearly ubiquitous pathological feature observed in specimens from benign prostate hyperplasia and prostate cancer patients. The microenvironment of the inflamed prostate is highly reactive, and epithelial hyperplasia is a hallmark feature of inflamed prostates. How inflammation orchestrates epithelial proliferation as part of its repair and recovery action is not well understood. Here, we report that a novel epithelial progenitor cell population is induced to expand during inflammation. We used sphere culture assays, immunofluorescence, and flow cytometry to show that this population is increased in bacterially induced inflamed mouse prostates relative to naïve control prostates. We confirmed from previous reports that this population exclusively possesses the ability to regrow entire prostatic structures from single cell culture using renal grafts. In addition, putative progenitor cells harvested from inflamed animals have greater aggregation capacity than those isolated from naïve control prostates. Expansion of this critical cell population requires IL-1 signaling, as IL-1 receptor 1-null mice exhibit inflammation similar to wild-type inflamed animals but exhibit significantly reduced progenitor cell proliferation and hyperplasia. These data demonstrate that inflammation promotes hyperplasia in the mouse prostatic epithelium by inducing the expansion of a selected epithelial progenitor cell population in an IL-1 receptor-dependent manner. These findings may have significant impact on our understanding of how inflammation promotes proliferative diseases such as benign prostatic hyperplasia and prostate cancer, both of which depend on expansion of cells that exhibit a progenitor-like nature.</description><identifier>ISSN: 1931-857X</identifier><identifier>EISSN: 1522-1466</identifier><identifier>DOI: 10.1152/ajprenal.00488.2014</identifier><identifier>PMID: 25925259</identifier><language>eng</language><publisher>United States: American Physiological Society</publisher><subject>Animals ; Cell culture ; Cell Proliferation - physiology ; Cells ; Cytokines ; Disease Models, Animal ; Inflammation - pathology ; Interleukin-1 - metabolism ; Male ; Mice ; Mice, Knockout ; Prostate ; Prostatic Hyperplasia - pathology ; Rodents ; Stem Cells - cytology</subject><ispartof>American journal of physiology. Renal physiology, 2015-06, Vol.308 (12), p.F1421-F1430</ispartof><rights>Copyright © 2015 the American Physiological Society.</rights><rights>Copyright American Physiological Society Jun 15, 2015</rights><rights>Copyright © 2015 the American Physiological Society 2015 American Physiological Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c433t-8a30b75b1a0a8dcc4bd1c10521f03e173d484e124bb061ddc19d2f4f2f8842643</citedby><cites>FETCH-LOGICAL-c433t-8a30b75b1a0a8dcc4bd1c10521f03e173d484e124bb061ddc19d2f4f2f8842643</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,3039,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25925259$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Liang</creatorcontrib><creatorcontrib>Zoetemelk, Marloes</creatorcontrib><creatorcontrib>Chitteti, Brahmananda R</creatorcontrib><creatorcontrib>Ratliff, Timothy L</creatorcontrib><creatorcontrib>Myers, Jason D</creatorcontrib><creatorcontrib>Srour, Edward F</creatorcontrib><creatorcontrib>Broxmeyer, Hal</creatorcontrib><creatorcontrib>Jerde, Travis J</creatorcontrib><title>Expansion of prostate epithelial progenitor cells after inflammation of the mouse prostate</title><title>American journal of physiology. Renal physiology</title><addtitle>Am J Physiol Renal Physiol</addtitle><description>Prostatic inflammation is a nearly ubiquitous pathological feature observed in specimens from benign prostate hyperplasia and prostate cancer patients. The microenvironment of the inflamed prostate is highly reactive, and epithelial hyperplasia is a hallmark feature of inflamed prostates. How inflammation orchestrates epithelial proliferation as part of its repair and recovery action is not well understood. Here, we report that a novel epithelial progenitor cell population is induced to expand during inflammation. We used sphere culture assays, immunofluorescence, and flow cytometry to show that this population is increased in bacterially induced inflamed mouse prostates relative to naïve control prostates. We confirmed from previous reports that this population exclusively possesses the ability to regrow entire prostatic structures from single cell culture using renal grafts. In addition, putative progenitor cells harvested from inflamed animals have greater aggregation capacity than those isolated from naïve control prostates. Expansion of this critical cell population requires IL-1 signaling, as IL-1 receptor 1-null mice exhibit inflammation similar to wild-type inflamed animals but exhibit significantly reduced progenitor cell proliferation and hyperplasia. These data demonstrate that inflammation promotes hyperplasia in the mouse prostatic epithelium by inducing the expansion of a selected epithelial progenitor cell population in an IL-1 receptor-dependent manner. These findings may have significant impact on our understanding of how inflammation promotes proliferative diseases such as benign prostatic hyperplasia and prostate cancer, both of which depend on expansion of cells that exhibit a progenitor-like nature.</description><subject>Animals</subject><subject>Cell culture</subject><subject>Cell Proliferation - physiology</subject><subject>Cells</subject><subject>Cytokines</subject><subject>Disease Models, Animal</subject><subject>Inflammation - pathology</subject><subject>Interleukin-1 - metabolism</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Knockout</subject><subject>Prostate</subject><subject>Prostatic Hyperplasia - pathology</subject><subject>Rodents</subject><subject>Stem Cells - cytology</subject><issn>1931-857X</issn><issn>1522-1466</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkV1LBCEYhSWKvn9BEAPddDObrzqzehNE9AVBNwXRjTgzuusyM07qRv37nNqW6kbF95yDxwehI8ATgIKcqcXgda_aCcaM8wnBwDbQbpqQHFhZbqazoJDzYvq8g_ZCWGCMAQhsox1SCFKkZRe9XL0Pqg_W9Zkz2eBdiCrqTA82znVrVTvezXRvo_NZrds2ZMpE7TPbm1Z1nYora5JnnVsGvQ45QFtGtUEfrvZ99HR99Xh5m98_3NxdXtznNaM05lxRXE2LChRWvKlrVjVQAy4IGEw1TGnDONNAWFXhEpqmBtEQwwwxnDNSMrqPzr9zh2XV6abWffSqlYO3nfIf0ikr_056O5cz9yYZKwXnPAWcrgK8e13qEGVnw9hV9To1klByURLgpUjSk3_ShVv6BGFUCcJEIdioot-qOn1F8NqsHwNYjuzkDzv5xU6O7JLr-HePtecHFv0EIrGZlA</recordid><startdate>20150615</startdate><enddate>20150615</enddate><creator>Wang, Liang</creator><creator>Zoetemelk, Marloes</creator><creator>Chitteti, Brahmananda R</creator><creator>Ratliff, Timothy L</creator><creator>Myers, Jason D</creator><creator>Srour, Edward F</creator><creator>Broxmeyer, Hal</creator><creator>Jerde, Travis J</creator><general>American Physiological Society</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20150615</creationdate><title>Expansion of prostate epithelial progenitor cells after inflammation of the mouse prostate</title><author>Wang, Liang ; Zoetemelk, Marloes ; Chitteti, Brahmananda R ; Ratliff, Timothy L ; Myers, Jason D ; Srour, Edward F ; Broxmeyer, Hal ; Jerde, Travis J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c433t-8a30b75b1a0a8dcc4bd1c10521f03e173d484e124bb061ddc19d2f4f2f8842643</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Cell culture</topic><topic>Cell Proliferation - physiology</topic><topic>Cells</topic><topic>Cytokines</topic><topic>Disease Models, Animal</topic><topic>Inflammation - pathology</topic><topic>Interleukin-1 - metabolism</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Knockout</topic><topic>Prostate</topic><topic>Prostatic Hyperplasia - pathology</topic><topic>Rodents</topic><topic>Stem Cells - cytology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Liang</creatorcontrib><creatorcontrib>Zoetemelk, Marloes</creatorcontrib><creatorcontrib>Chitteti, Brahmananda R</creatorcontrib><creatorcontrib>Ratliff, Timothy L</creatorcontrib><creatorcontrib>Myers, Jason D</creatorcontrib><creatorcontrib>Srour, Edward F</creatorcontrib><creatorcontrib>Broxmeyer, Hal</creatorcontrib><creatorcontrib>Jerde, Travis J</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>American journal of physiology. Renal physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Liang</au><au>Zoetemelk, Marloes</au><au>Chitteti, Brahmananda R</au><au>Ratliff, Timothy L</au><au>Myers, Jason D</au><au>Srour, Edward F</au><au>Broxmeyer, Hal</au><au>Jerde, Travis J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Expansion of prostate epithelial progenitor cells after inflammation of the mouse prostate</atitle><jtitle>American journal of physiology. Renal physiology</jtitle><addtitle>Am J Physiol Renal Physiol</addtitle><date>2015-06-15</date><risdate>2015</risdate><volume>308</volume><issue>12</issue><spage>F1421</spage><epage>F1430</epage><pages>F1421-F1430</pages><issn>1931-857X</issn><eissn>1522-1466</eissn><abstract>Prostatic inflammation is a nearly ubiquitous pathological feature observed in specimens from benign prostate hyperplasia and prostate cancer patients. The microenvironment of the inflamed prostate is highly reactive, and epithelial hyperplasia is a hallmark feature of inflamed prostates. How inflammation orchestrates epithelial proliferation as part of its repair and recovery action is not well understood. Here, we report that a novel epithelial progenitor cell population is induced to expand during inflammation. We used sphere culture assays, immunofluorescence, and flow cytometry to show that this population is increased in bacterially induced inflamed mouse prostates relative to naïve control prostates. We confirmed from previous reports that this population exclusively possesses the ability to regrow entire prostatic structures from single cell culture using renal grafts. In addition, putative progenitor cells harvested from inflamed animals have greater aggregation capacity than those isolated from naïve control prostates. Expansion of this critical cell population requires IL-1 signaling, as IL-1 receptor 1-null mice exhibit inflammation similar to wild-type inflamed animals but exhibit significantly reduced progenitor cell proliferation and hyperplasia. These data demonstrate that inflammation promotes hyperplasia in the mouse prostatic epithelium by inducing the expansion of a selected epithelial progenitor cell population in an IL-1 receptor-dependent manner. These findings may have significant impact on our understanding of how inflammation promotes proliferative diseases such as benign prostatic hyperplasia and prostate cancer, both of which depend on expansion of cells that exhibit a progenitor-like nature.</abstract><cop>United States</cop><pub>American Physiological Society</pub><pmid>25925259</pmid><doi>10.1152/ajprenal.00488.2014</doi><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1931-857X
ispartof American journal of physiology. Renal physiology, 2015-06, Vol.308 (12), p.F1421-F1430
issn 1931-857X
1522-1466
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4469888
source MEDLINE; American Physiological Society; EZB-FREE-00999 freely available EZB journals; Alma/SFX Local Collection
subjects Animals
Cell culture
Cell Proliferation - physiology
Cells
Cytokines
Disease Models, Animal
Inflammation - pathology
Interleukin-1 - metabolism
Male
Mice
Mice, Knockout
Prostate
Prostatic Hyperplasia - pathology
Rodents
Stem Cells - cytology
title Expansion of prostate epithelial progenitor cells after inflammation of the mouse prostate
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-06T17%3A06%3A58IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Expansion%20of%20prostate%20epithelial%20progenitor%20cells%20after%20inflammation%20of%20the%20mouse%20prostate&rft.jtitle=American%20journal%20of%20physiology.%20Renal%20physiology&rft.au=Wang,%20Liang&rft.date=2015-06-15&rft.volume=308&rft.issue=12&rft.spage=F1421&rft.epage=F1430&rft.pages=F1421-F1430&rft.issn=1931-857X&rft.eissn=1522-1466&rft_id=info:doi/10.1152/ajprenal.00488.2014&rft_dat=%3Cproquest_pubme%3E1689621869%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1692495949&rft_id=info:pmid/25925259&rfr_iscdi=true