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Mammary Branching Morphogenesis Requires Reciprocal Signaling by Heparanase and MMP-14
ABSTRACT The development of the mammary gland involves formation of a branched arboreal structure resulting from the penetration and proliferation of epithelial cells into the fat pad. The mammary cells invade by remodeling their surrounding extracellular matrix (ECM), which are rich in proteins, an...
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Published in: | Journal of cellular biochemistry 2015-08, Vol.116 (8), p.1668-1679 |
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creator | Gomes, Angélica Maciel Bhat, Ramray Correia, Ana Luísa Mott, Joni D. Ilan, Neta Vlodavsky, Israel Pavão, Mauro S.G. Bissell, Mina |
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The development of the mammary gland involves formation of a branched arboreal structure resulting from the penetration and proliferation of epithelial cells into the fat pad. The mammary cells invade by remodeling their surrounding extracellular matrix (ECM), which are rich in proteins, and glycans such as heparan sulfate proteoglycans (HSPGs). There is increasing literature on how the interaction between signaling by ECM and matrix metalloproteinases (MMPs) is relevant to morphogenetic and physiological contexts. Here we sought to understand how heparanase, the sole mammalian heparan sulfate‐degrading endoglycosidase may regulate mammary gland development. We found a robust localization of heparanase within growing end buds during branching in vivo. Using three‐dimensional (3D) organotypic cultures, we showed that heparanase expression and activity are required for mammary epithelial invasion/branching within dense collagen I gels. Morphometric analysis of glands from both heparanase‐overexpressing and knockout mice showed a direct correlation between degree of branching and the heparanase levels, confirming our 3D organotypic culture observations. Finally, we uncovered a reciprocal association between levels of heparanase and MMP14, a membrane‐bound MMP, shedding further light on how branching occurs within developing mammary glands. J. Cell. Biochem. 116: 1668–1679, 2015. © 2015 Wiley Periodicals, Inc. |
doi_str_mv | 10.1002/jcb.25127 |
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The development of the mammary gland involves formation of a branched arboreal structure resulting from the penetration and proliferation of epithelial cells into the fat pad. The mammary cells invade by remodeling their surrounding extracellular matrix (ECM), which are rich in proteins, and glycans such as heparan sulfate proteoglycans (HSPGs). There is increasing literature on how the interaction between signaling by ECM and matrix metalloproteinases (MMPs) is relevant to morphogenetic and physiological contexts. Here we sought to understand how heparanase, the sole mammalian heparan sulfate‐degrading endoglycosidase may regulate mammary gland development. We found a robust localization of heparanase within growing end buds during branching in vivo. Using three‐dimensional (3D) organotypic cultures, we showed that heparanase expression and activity are required for mammary epithelial invasion/branching within dense collagen I gels. Morphometric analysis of glands from both heparanase‐overexpressing and knockout mice showed a direct correlation between degree of branching and the heparanase levels, confirming our 3D organotypic culture observations. Finally, we uncovered a reciprocal association between levels of heparanase and MMP14, a membrane‐bound MMP, shedding further light on how branching occurs within developing mammary glands. J. Cell. Biochem. 116: 1668–1679, 2015. © 2015 Wiley Periodicals, Inc.</description><identifier>ISSN: 0730-2312</identifier><identifier>EISSN: 1097-4644</identifier><identifier>DOI: 10.1002/jcb.25127</identifier><identifier>PMID: 25735873</identifier><language>eng</language><publisher>United States: Blackwell Publishing Ltd</publisher><subject>Animals ; BRANCHING MORPHOGENESIS ; Cell culture ; Cell Movement ; Cell proliferation ; Collagen (type I) ; Epithelial cells ; Epithelial Cells - physiology ; Epithelium ; Extracellular matrix ; Female ; Gels ; Gene Expression Regulation, Developmental ; Glucuronidase - genetics ; Glucuronidase - metabolism ; Heparan sulfate ; Heparan sulfate proteoglycans ; HEPARANASE ; Localization ; MAMMARY GLAND ; Mammary glands ; Mammary Glands, Animal - enzymology ; Mammary Glands, Animal - growth & development ; Matrix metalloproteinase ; Matrix Metalloproteinase 14 - metabolism ; Matrix metalloproteinases ; Mice ; MMP-14 ; Morphogenesis ; Organ Culture Techniques ; Polysaccharides ; Proteoglycans ; Signal Transduction ; Sulfates</subject><ispartof>Journal of cellular biochemistry, 2015-08, Vol.116 (8), p.1668-1679</ispartof><rights>2015 Wiley Periodicals, Inc.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4857-486b1a52c3d7081f781229da1a471043be64b959cbdfeefe5ec439a46ae4659d3</citedby><cites>FETCH-LOGICAL-c4857-486b1a52c3d7081f781229da1a471043be64b959cbdfeefe5ec439a46ae4659d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25735873$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gomes, Angélica Maciel</creatorcontrib><creatorcontrib>Bhat, Ramray</creatorcontrib><creatorcontrib>Correia, Ana Luísa</creatorcontrib><creatorcontrib>Mott, Joni D.</creatorcontrib><creatorcontrib>Ilan, Neta</creatorcontrib><creatorcontrib>Vlodavsky, Israel</creatorcontrib><creatorcontrib>Pavão, Mauro S.G.</creatorcontrib><creatorcontrib>Bissell, Mina</creatorcontrib><title>Mammary Branching Morphogenesis Requires Reciprocal Signaling by Heparanase and MMP-14</title><title>Journal of cellular biochemistry</title><addtitle>J. Cell. Biochem</addtitle><description>ABSTRACT
The development of the mammary gland involves formation of a branched arboreal structure resulting from the penetration and proliferation of epithelial cells into the fat pad. The mammary cells invade by remodeling their surrounding extracellular matrix (ECM), which are rich in proteins, and glycans such as heparan sulfate proteoglycans (HSPGs). There is increasing literature on how the interaction between signaling by ECM and matrix metalloproteinases (MMPs) is relevant to morphogenetic and physiological contexts. Here we sought to understand how heparanase, the sole mammalian heparan sulfate‐degrading endoglycosidase may regulate mammary gland development. We found a robust localization of heparanase within growing end buds during branching in vivo. Using three‐dimensional (3D) organotypic cultures, we showed that heparanase expression and activity are required for mammary epithelial invasion/branching within dense collagen I gels. Morphometric analysis of glands from both heparanase‐overexpressing and knockout mice showed a direct correlation between degree of branching and the heparanase levels, confirming our 3D organotypic culture observations. Finally, we uncovered a reciprocal association between levels of heparanase and MMP14, a membrane‐bound MMP, shedding further light on how branching occurs within developing mammary glands. J. Cell. Biochem. 116: 1668–1679, 2015. © 2015 Wiley Periodicals, Inc.</description><subject>Animals</subject><subject>BRANCHING MORPHOGENESIS</subject><subject>Cell culture</subject><subject>Cell Movement</subject><subject>Cell proliferation</subject><subject>Collagen (type I)</subject><subject>Epithelial cells</subject><subject>Epithelial Cells - physiology</subject><subject>Epithelium</subject><subject>Extracellular matrix</subject><subject>Female</subject><subject>Gels</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Glucuronidase - genetics</subject><subject>Glucuronidase - metabolism</subject><subject>Heparan sulfate</subject><subject>Heparan sulfate proteoglycans</subject><subject>HEPARANASE</subject><subject>Localization</subject><subject>MAMMARY GLAND</subject><subject>Mammary glands</subject><subject>Mammary Glands, Animal - enzymology</subject><subject>Mammary Glands, Animal - growth & development</subject><subject>Matrix metalloproteinase</subject><subject>Matrix Metalloproteinase 14 - metabolism</subject><subject>Matrix metalloproteinases</subject><subject>Mice</subject><subject>MMP-14</subject><subject>Morphogenesis</subject><subject>Organ Culture Techniques</subject><subject>Polysaccharides</subject><subject>Proteoglycans</subject><subject>Signal Transduction</subject><subject>Sulfates</subject><issn>0730-2312</issn><issn>1097-4644</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><recordid>eNp9kc1OGzEUhS3UClLKoi-ARuqmXQz43-MliQopylDEX5eWx3MnOExmgs2ozdvXaYAFUrvyXXzn0_U9CH0i-IhgTI8XrjqiglC1g0YEa5Vzyfk7NMKK4ZwyQvfQhxgXGGOtGd1Fe1QoJgrFRuiutMulDetsHGzn7n03z8o-rO77OXQQfcyu4HHwATaD86vQO9tm137e2XbDVutsCiubsjZCZrs6K8vLnPCP6H1j2wgHz-8-uj39djOZ5rMfZ98nJ7Pc8UKkPQtZESuoY7XCBWlUQSjVtSWWK4I5q0DySgvtqroBaECA40xbLi1wKXTN9tGXrTdt9jhAfDJLHx20re2gH6IhUmPJk6FI6Oc36KIfQvpHNCzdjGmu2H8pIgtdcEyJStTXLeVCH2OAxqyC35zREGw2lZhUiflbSWIPn41DtYT6lXzpIAHHW-CXb2H9b5M5n4xflPk24eMT_H5N2PBgpGJKmJ8XZ-b0fHZzUY6ZmbI_YC2h5A</recordid><startdate>201508</startdate><enddate>201508</enddate><creator>Gomes, Angélica Maciel</creator><creator>Bhat, Ramray</creator><creator>Correia, Ana Luísa</creator><creator>Mott, Joni D.</creator><creator>Ilan, Neta</creator><creator>Vlodavsky, Israel</creator><creator>Pavão, Mauro S.G.</creator><creator>Bissell, Mina</creator><general>Blackwell Publishing Ltd</general><general>Wiley Subscription Services, Inc</general><scope>BSCLL</scope><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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7T7</scope><scope>7TK</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>7X8</scope></search><sort><creationdate>201508</creationdate><title>Mammary Branching Morphogenesis Requires Reciprocal Signaling by Heparanase and MMP-14</title><author>Gomes, Angélica Maciel ; Bhat, Ramray ; Correia, Ana Luísa ; Mott, Joni D. ; Ilan, Neta ; Vlodavsky, Israel ; Pavão, Mauro S.G. ; Bissell, Mina</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4857-486b1a52c3d7081f781229da1a471043be64b959cbdfeefe5ec439a46ae4659d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>BRANCHING MORPHOGENESIS</topic><topic>Cell culture</topic><topic>Cell Movement</topic><topic>Cell proliferation</topic><topic>Collagen (type I)</topic><topic>Epithelial cells</topic><topic>Epithelial Cells - physiology</topic><topic>Epithelium</topic><topic>Extracellular matrix</topic><topic>Female</topic><topic>Gels</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Glucuronidase - genetics</topic><topic>Glucuronidase - metabolism</topic><topic>Heparan sulfate</topic><topic>Heparan sulfate proteoglycans</topic><topic>HEPARANASE</topic><topic>Localization</topic><topic>MAMMARY GLAND</topic><topic>Mammary glands</topic><topic>Mammary Glands, Animal - enzymology</topic><topic>Mammary Glands, Animal - growth & development</topic><topic>Matrix metalloproteinase</topic><topic>Matrix Metalloproteinase 14 - metabolism</topic><topic>Matrix metalloproteinases</topic><topic>Mice</topic><topic>MMP-14</topic><topic>Morphogenesis</topic><topic>Organ Culture Techniques</topic><topic>Polysaccharides</topic><topic>Proteoglycans</topic><topic>Signal Transduction</topic><topic>Sulfates</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gomes, Angélica Maciel</creatorcontrib><creatorcontrib>Bhat, Ramray</creatorcontrib><creatorcontrib>Correia, Ana Luísa</creatorcontrib><creatorcontrib>Mott, Joni D.</creatorcontrib><creatorcontrib>Ilan, Neta</creatorcontrib><creatorcontrib>Vlodavsky, Israel</creatorcontrib><creatorcontrib>Pavão, Mauro S.G.</creatorcontrib><creatorcontrib>Bissell, Mina</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Neurosciences Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of cellular biochemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gomes, Angélica Maciel</au><au>Bhat, Ramray</au><au>Correia, Ana Luísa</au><au>Mott, Joni D.</au><au>Ilan, Neta</au><au>Vlodavsky, Israel</au><au>Pavão, Mauro S.G.</au><au>Bissell, Mina</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mammary Branching Morphogenesis Requires Reciprocal Signaling by Heparanase and MMP-14</atitle><jtitle>Journal of cellular biochemistry</jtitle><addtitle>J. Cell. Biochem</addtitle><date>2015-08</date><risdate>2015</risdate><volume>116</volume><issue>8</issue><spage>1668</spage><epage>1679</epage><pages>1668-1679</pages><issn>0730-2312</issn><eissn>1097-4644</eissn><abstract>ABSTRACT
The development of the mammary gland involves formation of a branched arboreal structure resulting from the penetration and proliferation of epithelial cells into the fat pad. The mammary cells invade by remodeling their surrounding extracellular matrix (ECM), which are rich in proteins, and glycans such as heparan sulfate proteoglycans (HSPGs). There is increasing literature on how the interaction between signaling by ECM and matrix metalloproteinases (MMPs) is relevant to morphogenetic and physiological contexts. Here we sought to understand how heparanase, the sole mammalian heparan sulfate‐degrading endoglycosidase may regulate mammary gland development. We found a robust localization of heparanase within growing end buds during branching in vivo. Using three‐dimensional (3D) organotypic cultures, we showed that heparanase expression and activity are required for mammary epithelial invasion/branching within dense collagen I gels. Morphometric analysis of glands from both heparanase‐overexpressing and knockout mice showed a direct correlation between degree of branching and the heparanase levels, confirming our 3D organotypic culture observations. Finally, we uncovered a reciprocal association between levels of heparanase and MMP14, a membrane‐bound MMP, shedding further light on how branching occurs within developing mammary glands. J. Cell. Biochem. 116: 1668–1679, 2015. © 2015 Wiley Periodicals, Inc.</abstract><cop>United States</cop><pub>Blackwell Publishing Ltd</pub><pmid>25735873</pmid><doi>10.1002/jcb.25127</doi><tpages>12</tpages></addata></record> |
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subjects | Animals BRANCHING MORPHOGENESIS Cell culture Cell Movement Cell proliferation Collagen (type I) Epithelial cells Epithelial Cells - physiology Epithelium Extracellular matrix Female Gels Gene Expression Regulation, Developmental Glucuronidase - genetics Glucuronidase - metabolism Heparan sulfate Heparan sulfate proteoglycans HEPARANASE Localization MAMMARY GLAND Mammary glands Mammary Glands, Animal - enzymology Mammary Glands, Animal - growth & development Matrix metalloproteinase Matrix Metalloproteinase 14 - metabolism Matrix metalloproteinases Mice MMP-14 Morphogenesis Organ Culture Techniques Polysaccharides Proteoglycans Signal Transduction Sulfates |
title | Mammary Branching Morphogenesis Requires Reciprocal Signaling by Heparanase and MMP-14 |
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