Conditioned medium from hypoxic bone marrow-derived mesenchymal stem cells enhances wound healing in mice
Growing evidence indicates that bone marrow-derived mesenchymal stem cells (BM-MSCs) enhance wound repair via paracrine. Because the extent of environmental oxygenation affects the innate characteristics of BM-MSCs, including their stemness and migration capacity, the current study set out to elucid...
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| Veröffentlicht in: | PloS one 2014-04, Vol.9 (4), p.e96161-e96161 |
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| description | Growing evidence indicates that bone marrow-derived mesenchymal stem cells (BM-MSCs) enhance wound repair via paracrine. Because the extent of environmental oxygenation affects the innate characteristics of BM-MSCs, including their stemness and migration capacity, the current study set out to elucidate and compare the impact of normoxic and hypoxic cell-culture conditions on the expression and secretion of BM-MSC-derived paracrine molecules (e.g., cytokines, growth factors and chemokines) that hypothetically contribute to cutaneous wound healing in vivo. Semi-quantitative reverse transcriptase polymerase chain reaction (RT-PCR) and enzyme-linked immunosorbent assay (ELISA) analyses of normoxic and hypoxic BM-MSCs and their conditioned medium fractions showed that the stem cells expressed and secreted significantly higher amounts of basic fibroblast growth factor (bFGF),vascular endothelial growth factor A (VEGF-A) interleukin 6 (IL-6) and interleukin 8 (IL-8) under hypoxic conditions. Moreover, hypoxic BM-MSC-derived conditioned medium (hypoCM) vs. normoxic BM-MSC-derived conditioned medium (norCM) or vehicle control medium significantly enhanced the proliferation of keratinocytes, fibroblasts and endothelial cells, the migration of keratinocytes, fibroblasts, endothelial cells and monocytes, and the formation of tubular structures by endothelial cells cultured on Matrigel matrix. Consistent with these in vitro results, skin wound contraction was significantly accelerated in Balb/c nude mice treated with topical hypoCM relative to norCM or the vehicle control. Notably increased in vivo cell proliferation, neovascularization as well as recruitment of inflammatory macrophages and evidently decreased collagen I, and collagen III were also found in the hypoCM-treated group. These findings suggest that BM-MSCs promote murine skin wound healing via hypoxia-enhanced paracrine. |
| doi_str_mv | 10.1371/journal.pone.0096161 |
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Because the extent of environmental oxygenation affects the innate characteristics of BM-MSCs, including their stemness and migration capacity, the current study set out to elucidate and compare the impact of normoxic and hypoxic cell-culture conditions on the expression and secretion of BM-MSC-derived paracrine molecules (e.g., cytokines, growth factors and chemokines) that hypothetically contribute to cutaneous wound healing in vivo. Semi-quantitative reverse transcriptase polymerase chain reaction (RT-PCR) and enzyme-linked immunosorbent assay (ELISA) analyses of normoxic and hypoxic BM-MSCs and their conditioned medium fractions showed that the stem cells expressed and secreted significantly higher amounts of basic fibroblast growth factor (bFGF),vascular endothelial growth factor A (VEGF-A) interleukin 6 (IL-6) and interleukin 8 (IL-8) under hypoxic conditions. Moreover, hypoxic BM-MSC-derived conditioned medium (hypoCM) vs. normoxic BM-MSC-derived conditioned medium (norCM) or vehicle control medium significantly enhanced the proliferation of keratinocytes, fibroblasts and endothelial cells, the migration of keratinocytes, fibroblasts, endothelial cells and monocytes, and the formation of tubular structures by endothelial cells cultured on Matrigel matrix. Consistent with these in vitro results, skin wound contraction was significantly accelerated in Balb/c nude mice treated with topical hypoCM relative to norCM or the vehicle control. Notably increased in vivo cell proliferation, neovascularization as well as recruitment of inflammatory macrophages and evidently decreased collagen I, and collagen III were also found in the hypoCM-treated group. These findings suggest that BM-MSCs promote murine skin wound healing via hypoxia-enhanced paracrine.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0096161</identifier><identifier>PMID: 24781370</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Arthritis ; Base Sequence ; Biology and Life Sciences ; Bone healing ; Bone marrow ; Bone Marrow Cells - metabolism ; Cell culture ; Cell growth ; Cell Hypoxia ; Cell migration ; Cell Proliferation ; Cells, Cultured ; Chemokines ; Collagen ; Collagen (type I) ; Collagen (type III) ; Conditioning ; Contraction ; Culture Media, Conditioned ; Cytokines ; Deoxyribonucleic acid ; Diabetes ; DNA ; DNA polymerases ; DNA Primers ; Endothelial cells ; Enzyme-linked immunosorbent assay ; Fibroblast growth factors ; Fibroblasts ; Growth factors ; Health aspects ; Humans ; Hypotheses ; Hypoxia ; Inflammation ; Interleukin 6 ; Interleukin 8 ; Macrophages ; Medicine and Health Sciences ; Mesenchymal stem cells ; Mesenchymal Stromal Cells - metabolism ; Mesenchyme ; Mice ; Oxygenation ; Physiological aspects ; Polymerase chain reaction ; Research and Analysis Methods ; Reverse Transcriptase Polymerase Chain Reaction ; Signal transduction ; Skin ; Stem cell research ; Stem cells ; Surgery ; Vascular endothelial growth factor ; Wound Healing</subject><ispartof>PloS one, 2014-04, Vol.9 (4), p.e96161-e96161</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Chen et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://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>2014 Chen et al 2014 Chen et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c758t-2b9218295324727f3166598c61710d3e80b2ce7845f333b2e30e75837182f3ed3</citedby><cites>FETCH-LOGICAL-c758t-2b9218295324727f3166598c61710d3e80b2ce7845f333b2e30e75837182f3ed3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4004560/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4004560/$$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/24781370$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Lei</creatorcontrib><creatorcontrib>Xu, Yingbin</creatorcontrib><creatorcontrib>Zhao, Jingling</creatorcontrib><creatorcontrib>Zhang, Zhaoqiang</creatorcontrib><creatorcontrib>Yang, Ronghua</creatorcontrib><creatorcontrib>Xie, Julin</creatorcontrib><creatorcontrib>Liu, Xusheng</creatorcontrib><creatorcontrib>Qi, Shaohai</creatorcontrib><title>Conditioned medium from hypoxic bone marrow-derived mesenchymal stem cells enhances wound healing in mice</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Growing evidence indicates that bone marrow-derived mesenchymal stem cells (BM-MSCs) enhance wound repair via paracrine. Because the extent of environmental oxygenation affects the innate characteristics of BM-MSCs, including their stemness and migration capacity, the current study set out to elucidate and compare the impact of normoxic and hypoxic cell-culture conditions on the expression and secretion of BM-MSC-derived paracrine molecules (e.g., cytokines, growth factors and chemokines) that hypothetically contribute to cutaneous wound healing in vivo. Semi-quantitative reverse transcriptase polymerase chain reaction (RT-PCR) and enzyme-linked immunosorbent assay (ELISA) analyses of normoxic and hypoxic BM-MSCs and their conditioned medium fractions showed that the stem cells expressed and secreted significantly higher amounts of basic fibroblast growth factor (bFGF),vascular endothelial growth factor A (VEGF-A) interleukin 6 (IL-6) and interleukin 8 (IL-8) under hypoxic conditions. 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These findings suggest that BM-MSCs promote murine skin wound healing via hypoxia-enhanced paracrine.</description><subject>Animals</subject><subject>Arthritis</subject><subject>Base Sequence</subject><subject>Biology and Life Sciences</subject><subject>Bone healing</subject><subject>Bone marrow</subject><subject>Bone Marrow Cells - metabolism</subject><subject>Cell culture</subject><subject>Cell growth</subject><subject>Cell Hypoxia</subject><subject>Cell migration</subject><subject>Cell Proliferation</subject><subject>Cells, Cultured</subject><subject>Chemokines</subject><subject>Collagen</subject><subject>Collagen (type I)</subject><subject>Collagen (type III)</subject><subject>Conditioning</subject><subject>Contraction</subject><subject>Culture Media, Conditioned</subject><subject>Cytokines</subject><subject>Deoxyribonucleic acid</subject><subject>Diabetes</subject><subject>DNA</subject><subject>DNA polymerases</subject><subject>DNA Primers</subject><subject>Endothelial cells</subject><subject>Enzyme-linked immunosorbent assay</subject><subject>Fibroblast growth factors</subject><subject>Fibroblasts</subject><subject>Growth factors</subject><subject>Health aspects</subject><subject>Humans</subject><subject>Hypotheses</subject><subject>Hypoxia</subject><subject>Inflammation</subject><subject>Interleukin 6</subject><subject>Interleukin 8</subject><subject>Macrophages</subject><subject>Medicine and Health Sciences</subject><subject>Mesenchymal stem cells</subject><subject>Mesenchymal Stromal Cells - metabolism</subject><subject>Mesenchyme</subject><subject>Mice</subject><subject>Oxygenation</subject><subject>Physiological aspects</subject><subject>Polymerase chain reaction</subject><subject>Research and Analysis Methods</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>Signal transduction</subject><subject>Skin</subject><subject>Stem cell research</subject><subject>Stem cells</subject><subject>Surgery</subject><subject>Vascular endothelial growth factor</subject><subject>Wound Healing</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk9tq3DAQhk1padK0b1BaQaG0F7vVwbLlm0JYelgIBHq6FbI8XmuxpY1kJ9m3r5x1wrrkovhCRvrmH80_miR5TfCSsJx82rrBW9Uud87CEuMiIxl5kpySgtFFRjF7evR_krwIYYsxZyLLnicnNM1FFMGniVk5W5neRJEKdVCZoUO1dx1q9jt3azQq4wnqlPfuZlGBN9d3XACrm32nWhR66JCGtg0IbKOshoBu3GAr1IBqjd0gY1FnNLxMntWqDfBqWs-S31-__Fp9X1xcfluvzi8WOueiX9CyoETQgrN4SZrXjGQZL4TOSE5wxUDgkmrIRcprxlhJgWGIgdERQWsGFTtL3h50d60LcnIpSMJJIYpC5DQS6wNRObWVO29ieXvplJF3G85vpPK90S1IrmKE5rouM5KWuhZKgM5piaEoC5WO2T5P2YYy2qfB9l61M9H5iTWN3LhrmWKc8gxHgQ-TgHdXA4RediaMfioLbhjvHfuXspxmEX33D_p4dRO1UbEAY2sX8-pRVJ6znHPBqRi1lo9Q8asgNiv2vDZxfxbwcRYQmR5u-40aQpDrnz_-n738M2ffH7Hjm-mb4NphfJJhDqYHUHsXgof6wWSC5TgR927IcSLkNBEx7M1xgx6C7keA_QXdUwYx</recordid><startdate>20140401</startdate><enddate>20140401</enddate><creator>Chen, Lei</creator><creator>Xu, Yingbin</creator><creator>Zhao, Jingling</creator><creator>Zhang, Zhaoqiang</creator><creator>Yang, Ronghua</creator><creator>Xie, Julin</creator><creator>Liu, Xusheng</creator><creator>Qi, Shaohai</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20140401</creationdate><title>Conditioned medium from hypoxic bone marrow-derived mesenchymal stem cells enhances wound healing in mice</title><author>Chen, Lei ; Xu, Yingbin ; Zhao, Jingling ; Zhang, Zhaoqiang ; Yang, Ronghua ; Xie, Julin ; Liu, Xusheng ; Qi, Shaohai</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c758t-2b9218295324727f3166598c61710d3e80b2ce7845f333b2e30e75837182f3ed3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animals</topic><topic>Arthritis</topic><topic>Base Sequence</topic><topic>Biology and Life Sciences</topic><topic>Bone healing</topic><topic>Bone marrow</topic><topic>Bone Marrow Cells - 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Because the extent of environmental oxygenation affects the innate characteristics of BM-MSCs, including their stemness and migration capacity, the current study set out to elucidate and compare the impact of normoxic and hypoxic cell-culture conditions on the expression and secretion of BM-MSC-derived paracrine molecules (e.g., cytokines, growth factors and chemokines) that hypothetically contribute to cutaneous wound healing in vivo. Semi-quantitative reverse transcriptase polymerase chain reaction (RT-PCR) and enzyme-linked immunosorbent assay (ELISA) analyses of normoxic and hypoxic BM-MSCs and their conditioned medium fractions showed that the stem cells expressed and secreted significantly higher amounts of basic fibroblast growth factor (bFGF),vascular endothelial growth factor A (VEGF-A) interleukin 6 (IL-6) and interleukin 8 (IL-8) under hypoxic conditions. Moreover, hypoxic BM-MSC-derived conditioned medium (hypoCM) vs. normoxic BM-MSC-derived conditioned medium (norCM) or vehicle control medium significantly enhanced the proliferation of keratinocytes, fibroblasts and endothelial cells, the migration of keratinocytes, fibroblasts, endothelial cells and monocytes, and the formation of tubular structures by endothelial cells cultured on Matrigel matrix. Consistent with these in vitro results, skin wound contraction was significantly accelerated in Balb/c nude mice treated with topical hypoCM relative to norCM or the vehicle control. Notably increased in vivo cell proliferation, neovascularization as well as recruitment of inflammatory macrophages and evidently decreased collagen I, and collagen III were also found in the hypoCM-treated group. These findings suggest that BM-MSCs promote murine skin wound healing via hypoxia-enhanced paracrine.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24781370</pmid><doi>10.1371/journal.pone.0096161</doi><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2014-04, Vol.9 (4), p.e96161-e96161 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1519899872 |
| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; Full-Text Journals in Chemistry (Open access); DOAJ Directory of Open Access Journals; PubMed Central; EZB Electronic Journals Library |
| subjects | Animals Arthritis Base Sequence Biology and Life Sciences Bone healing Bone marrow Bone Marrow Cells - metabolism Cell culture Cell growth Cell Hypoxia Cell migration Cell Proliferation Cells, Cultured Chemokines Collagen Collagen (type I) Collagen (type III) Conditioning Contraction Culture Media, Conditioned Cytokines Deoxyribonucleic acid Diabetes DNA DNA polymerases DNA Primers Endothelial cells Enzyme-linked immunosorbent assay Fibroblast growth factors Fibroblasts Growth factors Health aspects Humans Hypotheses Hypoxia Inflammation Interleukin 6 Interleukin 8 Macrophages Medicine and Health Sciences Mesenchymal stem cells Mesenchymal Stromal Cells - metabolism Mesenchyme Mice Oxygenation Physiological aspects Polymerase chain reaction Research and Analysis Methods Reverse Transcriptase Polymerase Chain Reaction Signal transduction Skin Stem cell research Stem cells Surgery Vascular endothelial growth factor Wound Healing |
| title | Conditioned medium from hypoxic bone marrow-derived mesenchymal stem cells enhances wound healing in mice |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-07T18%3A43%3A10IST&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=Conditioned%20medium%20from%20hypoxic%20bone%20marrow-derived%20mesenchymal%20stem%20cells%20enhances%20wound%20healing%20in%20mice&rft.jtitle=PloS%20one&rft.au=Chen,%20Lei&rft.date=2014-04-01&rft.volume=9&rft.issue=4&rft.spage=e96161&rft.epage=e96161&rft.pages=e96161-e96161&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0096161&rft_dat=%3Cgale_plos_%3EA375585286%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=1519899872&rft_id=info:pmid/24781370&rft_galeid=A375585286&rft_doaj_id=oai_doaj_org_article_5a987c5cfb614bcf8a8ec72b0e9b9a4d&rfr_iscdi=true |