Planarians as a model to assess in vivo the role of matrix metalloproteinase genes during homeostasis and regeneration
Matrix metalloproteinases (MMPs) are major executors of extracellular matrix remodeling and, consequently, play key roles in the response of cells to their microenvironment. The experimentally accessible stem cell population and the robust regenerative capabilities of planarians offer an ideal model...
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| description | Matrix metalloproteinases (MMPs) are major executors of extracellular matrix remodeling and, consequently, play key roles in the response of cells to their microenvironment. The experimentally accessible stem cell population and the robust regenerative capabilities of planarians offer an ideal model to study how modulation of the proteolytic system in the extracellular environment affects cell behavior in vivo. Genome-wide identification of Schmidtea mediterranea MMPs reveals that planarians possess four mmp-like genes. Two of them (mmp1 and mmp2) are strongly expressed in a subset of secretory cells and encode putative matrilysins. The other genes (mt-mmpA and mt-mmpB) are widely expressed in postmitotic cells and appear structurally related to membrane-type MMPs. These genes are conserved in the planarian Dugesia japonica. Here we explore the role of the planarian mmp genes by RNA interference (RNAi) during tissue homeostasis and regeneration. Our analyses identify essential functions for two of them. Following inhibition of mmp1 planarians display dramatic disruption of tissues architecture and significant decrease in cell death. These results suggest that mmp1 controls tissue turnover, modulating survival of postmitotic cells. Unexpectedly, the ability to regenerate is unaffected by mmp1(RNAi). Silencing of mt-mmpA alters tissue integrity and delays blastema growth, without affecting proliferation of stem cells. Our data support the possibility that the activity of this protease modulates cell migration and regulates anoikis, with a consequent pivotal role in tissue homeostasis and regeneration. Our data provide evidence of the involvement of specific MMPs in tissue homeostasis and regeneration and demonstrate that the behavior of planarian stem cells is critically dependent on the microenvironment surrounding these cells. Studying MMPs function in the planarian model provides evidence on how individual proteases work in vivo in adult tissues. These results have high potential to generate significant information for development of regenerative and anti cancer therapies. |
| doi_str_mv | 10.1371/journal.pone.0055649 |
| format | Article |
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The experimentally accessible stem cell population and the robust regenerative capabilities of planarians offer an ideal model to study how modulation of the proteolytic system in the extracellular environment affects cell behavior in vivo. Genome-wide identification of Schmidtea mediterranea MMPs reveals that planarians possess four mmp-like genes. Two of them (mmp1 and mmp2) are strongly expressed in a subset of secretory cells and encode putative matrilysins. The other genes (mt-mmpA and mt-mmpB) are widely expressed in postmitotic cells and appear structurally related to membrane-type MMPs. These genes are conserved in the planarian Dugesia japonica. Here we explore the role of the planarian mmp genes by RNA interference (RNAi) during tissue homeostasis and regeneration. Our analyses identify essential functions for two of them. Following inhibition of mmp1 planarians display dramatic disruption of tissues architecture and significant decrease in cell death. These results suggest that mmp1 controls tissue turnover, modulating survival of postmitotic cells. Unexpectedly, the ability to regenerate is unaffected by mmp1(RNAi). Silencing of mt-mmpA alters tissue integrity and delays blastema growth, without affecting proliferation of stem cells. Our data support the possibility that the activity of this protease modulates cell migration and regulates anoikis, with a consequent pivotal role in tissue homeostasis and regeneration. Our data provide evidence of the involvement of specific MMPs in tissue homeostasis and regeneration and demonstrate that the behavior of planarian stem cells is critically dependent on the microenvironment surrounding these cells. Studying MMPs function in the planarian model provides evidence on how individual proteases work in vivo in adult tissues. These results have high potential to generate significant information for development of regenerative and anti cancer therapies.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0055649</identifier><identifier>PMID: 23405188</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Animals ; Anoikis ; Apoptosis ; Biology ; Blotting, Western ; Cancer ; Cell adhesion & migration ; Cell death ; Cell Differentiation ; Cell migration ; Cell Movement ; Cell Proliferation ; Cell survival ; Cellular Microenvironment - physiology ; Cèl·lules mare ; Drosophila ; Enzymes ; Extracellular matrix ; Gelatinase A ; Gene expression ; Genes ; Genome ; Genomes ; Genomics ; Genètica molecular ; Homeostasis ; Homeostasis - physiology ; In Situ Hybridization ; In Situ Nick-End Labeling ; Insects ; Mammals ; Matrix metalloproteinase ; Matrix metalloproteinases ; Matrix Metalloproteinases - genetics ; Matrix Metalloproteinases - metabolism ; Metalloproteinase ; Mitosis ; Models, Animal ; Molecular genetics ; Planaria (Genus) ; Planarians - cytology ; Planarians - enzymology ; Planària (Gènere) ; Proteases ; Proteolysis ; Real-Time Polymerase Chain Reaction ; Regeneració (Biologia) ; Regeneration ; Regeneration (Biology) ; Regeneration - physiology ; Reverse Transcriptase Polymerase Chain Reaction ; Ribonucleic acid ; RNA ; RNA Interference ; RNA, Messenger - genetics ; RNA-mediated interference ; Stem cells ; Stem Cells - cytology ; Stem Cells - enzymology ; Studies ; Tissues ; Turbellaria</subject><ispartof>PloS one, 2013-02, Vol.8 (2), p.e55649</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Isolani 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>cc-by (c) M.E. Isolani et al., 2013 info:eu-repo/semantics/openAccess <a href="http://creativecommons.org/licenses/by/3.0/es">http://creativecommons.org/licenses/by/3.0/es</a></rights><rights>2013 Isolani et al 2013 Isolani et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c734t-cbb3e641410fff912529258bff95c645843437b9daeaae5b4da6be5c71ce480f3</citedby><cites>FETCH-LOGICAL-c734t-cbb3e641410fff912529258bff95c645843437b9daeaae5b4da6be5c71ce480f3</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/PMC3566077/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3566077/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2095,2914,23846,26953,27903,27904,53769,53771,79346,79347</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23405188$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Singh, Shree Ram</contributor><creatorcontrib>Isolani, Maria Emilia</creatorcontrib><creatorcontrib>Abril, Josep F</creatorcontrib><creatorcontrib>Saló, Emili</creatorcontrib><creatorcontrib>Deri, Paolo</creatorcontrib><creatorcontrib>Bianucci, Anna Maria</creatorcontrib><creatorcontrib>Batistoni, Renata</creatorcontrib><title>Planarians as a model to assess in vivo the role of matrix metalloproteinase genes during homeostasis and regeneration</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Matrix metalloproteinases (MMPs) are major executors of extracellular matrix remodeling and, consequently, play key roles in the response of cells to their microenvironment. The experimentally accessible stem cell population and the robust regenerative capabilities of planarians offer an ideal model to study how modulation of the proteolytic system in the extracellular environment affects cell behavior in vivo. Genome-wide identification of Schmidtea mediterranea MMPs reveals that planarians possess four mmp-like genes. Two of them (mmp1 and mmp2) are strongly expressed in a subset of secretory cells and encode putative matrilysins. The other genes (mt-mmpA and mt-mmpB) are widely expressed in postmitotic cells and appear structurally related to membrane-type MMPs. These genes are conserved in the planarian Dugesia japonica. Here we explore the role of the planarian mmp genes by RNA interference (RNAi) during tissue homeostasis and regeneration. Our analyses identify essential functions for two of them. Following inhibition of mmp1 planarians display dramatic disruption of tissues architecture and significant decrease in cell death. These results suggest that mmp1 controls tissue turnover, modulating survival of postmitotic cells. Unexpectedly, the ability to regenerate is unaffected by mmp1(RNAi). Silencing of mt-mmpA alters tissue integrity and delays blastema growth, without affecting proliferation of stem cells. Our data support the possibility that the activity of this protease modulates cell migration and regulates anoikis, with a consequent pivotal role in tissue homeostasis and regeneration. Our data provide evidence of the involvement of specific MMPs in tissue homeostasis and regeneration and demonstrate that the behavior of planarian stem cells is critically dependent on the microenvironment surrounding these cells. Studying MMPs function in the planarian model provides evidence on how individual proteases work in vivo in adult tissues. These results have high potential to generate significant information for development of regenerative and anti cancer therapies.</description><subject>Analysis</subject><subject>Animals</subject><subject>Anoikis</subject><subject>Apoptosis</subject><subject>Biology</subject><subject>Blotting, Western</subject><subject>Cancer</subject><subject>Cell adhesion & migration</subject><subject>Cell death</subject><subject>Cell Differentiation</subject><subject>Cell migration</subject><subject>Cell Movement</subject><subject>Cell Proliferation</subject><subject>Cell survival</subject><subject>Cellular Microenvironment - physiology</subject><subject>Cèl·lules mare</subject><subject>Drosophila</subject><subject>Enzymes</subject><subject>Extracellular matrix</subject><subject>Gelatinase A</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genome</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Genètica molecular</subject><subject>Homeostasis</subject><subject>Homeostasis - 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physiology</topic><topic>Cèl·lules mare</topic><topic>Drosophila</topic><topic>Enzymes</topic><topic>Extracellular matrix</topic><topic>Gelatinase A</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Genome</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Genètica molecular</topic><topic>Homeostasis</topic><topic>Homeostasis - physiology</topic><topic>In Situ Hybridization</topic><topic>In Situ Nick-End Labeling</topic><topic>Insects</topic><topic>Mammals</topic><topic>Matrix metalloproteinase</topic><topic>Matrix metalloproteinases</topic><topic>Matrix Metalloproteinases - genetics</topic><topic>Matrix Metalloproteinases - metabolism</topic><topic>Metalloproteinase</topic><topic>Mitosis</topic><topic>Models, Animal</topic><topic>Molecular genetics</topic><topic>Planaria (Genus)</topic><topic>Planarians - cytology</topic><topic>Planarians - enzymology</topic><topic>Planària (Gènere)</topic><topic>Proteases</topic><topic>Proteolysis</topic><topic>Real-Time Polymerase Chain Reaction</topic><topic>Regeneració (Biologia)</topic><topic>Regeneration</topic><topic>Regeneration (Biology)</topic><topic>Regeneration - physiology</topic><topic>Reverse Transcriptase Polymerase Chain Reaction</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA Interference</topic><topic>RNA, Messenger - genetics</topic><topic>RNA-mediated interference</topic><topic>Stem cells</topic><topic>Stem Cells - cytology</topic><topic>Stem Cells - enzymology</topic><topic>Studies</topic><topic>Tissues</topic><topic>Turbellaria</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Isolani, Maria Emilia</creatorcontrib><creatorcontrib>Abril, Josep F</creatorcontrib><creatorcontrib>Saló, Emili</creatorcontrib><creatorcontrib>Deri, Paolo</creatorcontrib><creatorcontrib>Bianucci, Anna Maria</creatorcontrib><creatorcontrib>Batistoni, Renata</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>Recercat</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Isolani, Maria Emilia</au><au>Abril, Josep F</au><au>Saló, Emili</au><au>Deri, Paolo</au><au>Bianucci, Anna Maria</au><au>Batistoni, Renata</au><au>Singh, Shree Ram</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Planarians as a model to assess in vivo the role of matrix metalloproteinase genes during homeostasis and regeneration</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-02-06</date><risdate>2013</risdate><volume>8</volume><issue>2</issue><spage>e55649</spage><pages>e55649-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Matrix metalloproteinases (MMPs) are major executors of extracellular matrix remodeling and, consequently, play key roles in the response of cells to their microenvironment. The experimentally accessible stem cell population and the robust regenerative capabilities of planarians offer an ideal model to study how modulation of the proteolytic system in the extracellular environment affects cell behavior in vivo. Genome-wide identification of Schmidtea mediterranea MMPs reveals that planarians possess four mmp-like genes. Two of them (mmp1 and mmp2) are strongly expressed in a subset of secretory cells and encode putative matrilysins. The other genes (mt-mmpA and mt-mmpB) are widely expressed in postmitotic cells and appear structurally related to membrane-type MMPs. These genes are conserved in the planarian Dugesia japonica. Here we explore the role of the planarian mmp genes by RNA interference (RNAi) during tissue homeostasis and regeneration. Our analyses identify essential functions for two of them. Following inhibition of mmp1 planarians display dramatic disruption of tissues architecture and significant decrease in cell death. These results suggest that mmp1 controls tissue turnover, modulating survival of postmitotic cells. Unexpectedly, the ability to regenerate is unaffected by mmp1(RNAi). Silencing of mt-mmpA alters tissue integrity and delays blastema growth, without affecting proliferation of stem cells. Our data support the possibility that the activity of this protease modulates cell migration and regulates anoikis, with a consequent pivotal role in tissue homeostasis and regeneration. Our data provide evidence of the involvement of specific MMPs in tissue homeostasis and regeneration and demonstrate that the behavior of planarian stem cells is critically dependent on the microenvironment surrounding these cells. Studying MMPs function in the planarian model provides evidence on how individual proteases work in vivo in adult tissues. These results have high potential to generate significant information for development of regenerative and anti cancer therapies.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23405188</pmid><doi>10.1371/journal.pone.0055649</doi><tpages>e55649</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2013-02, Vol.8 (2), p.e55649 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1330877491 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS); Recercat; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Analysis Animals Anoikis Apoptosis Biology Blotting, Western Cancer Cell adhesion & migration Cell death Cell Differentiation Cell migration Cell Movement Cell Proliferation Cell survival Cellular Microenvironment - physiology Cèl·lules mare Drosophila Enzymes Extracellular matrix Gelatinase A Gene expression Genes Genome Genomes Genomics Genètica molecular Homeostasis Homeostasis - physiology In Situ Hybridization In Situ Nick-End Labeling Insects Mammals Matrix metalloproteinase Matrix metalloproteinases Matrix Metalloproteinases - genetics Matrix Metalloproteinases - metabolism Metalloproteinase Mitosis Models, Animal Molecular genetics Planaria (Genus) Planarians - cytology Planarians - enzymology Planària (Gènere) Proteases Proteolysis Real-Time Polymerase Chain Reaction Regeneració (Biologia) Regeneration Regeneration (Biology) Regeneration - physiology Reverse Transcriptase Polymerase Chain Reaction Ribonucleic acid RNA RNA Interference RNA, Messenger - genetics RNA-mediated interference Stem cells Stem Cells - cytology Stem Cells - enzymology Studies Tissues Turbellaria |
| title | Planarians as a model to assess in vivo the role of matrix metalloproteinase genes during homeostasis and regeneration |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-25T09%3A11%3A08IST&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=Planarians%20as%20a%20model%20to%20assess%20in%20vivo%20the%20role%20of%20matrix%20metalloproteinase%20genes%20during%20homeostasis%20and%20regeneration&rft.jtitle=PloS%20one&rft.au=Isolani,%20Maria%20Emilia&rft.date=2013-02-06&rft.volume=8&rft.issue=2&rft.spage=e55649&rft.pages=e55649-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0055649&rft_dat=%3Cgale_plos_%3EA478414000%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=1330877491&rft_id=info:pmid/23405188&rft_galeid=A478414000&rft_doaj_id=oai_doaj_org_article_56965b70dcb6459388d8429672b5b512&rfr_iscdi=true |