Vascular endothelial growth factor and substrate mechanics regulate in vitro tubulogenesis of endothelial progenitor cells
Endothelial progenitor cells (EPCs) in the circulatory system have been suggested to maintain vascular homeostasis and contribute to adult vascular regeneration and repair. These processes require that EPCs break down the extracellular matrix (ECM), migrate, differentiate and undergo tube morphogene...
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description | Endothelial progenitor cells (EPCs) in the circulatory system have been suggested to maintain vascular homeostasis and contribute to adult vascular regeneration and repair. These processes require that EPCs break down the extracellular matrix (ECM), migrate, differentiate and undergo tube morphogenesis. Evidently, the ECM plays a critical role by providing biochemical and biophysical cues that regulate cellular behaviour. Using a chemically and mechanically tunable hydrogel to study tube morphogenesis in vitro, we show that vascular endothelial growth factor (VEGF) and substrate mechanics co‐regulate tubulogenesis of EPCs. High levels of VEGF are required to initiate tube morphogenesis and activate matrix metalloproteinases (MMPs), which enable EPC migration. Under these conditions, the elasticity of the substrate affects the progression of tube morphogenesis. With decreases in substrate stiffness, we observe decreased MMP expression while increased cellular elongation, with intracellular vacuole extension and coalescence to open lumen compartments. RNAi studies demonstrate that membrane type 1‐MMP (MT1‐MMP) is required to enable the movement of EPCs on the matrix and that EPCs sense matrix stiffness through signalling cascades leading to the activation of the RhoGTPase Cdc42. Collectively, these results suggest that coupled responses for VEGF stimulation and modulation of substrate stiffness are required to regulate tube morphogenesis of EPCs. |
doi_str_mv | 10.1111/j.1582-4934.2009.00981.x |
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These processes require that EPCs break down the extracellular matrix (ECM), migrate, differentiate and undergo tube morphogenesis. Evidently, the ECM plays a critical role by providing biochemical and biophysical cues that regulate cellular behaviour. Using a chemically and mechanically tunable hydrogel to study tube morphogenesis in vitro, we show that vascular endothelial growth factor (VEGF) and substrate mechanics co‐regulate tubulogenesis of EPCs. High levels of VEGF are required to initiate tube morphogenesis and activate matrix metalloproteinases (MMPs), which enable EPC migration. Under these conditions, the elasticity of the substrate affects the progression of tube morphogenesis. With decreases in substrate stiffness, we observe decreased MMP expression while increased cellular elongation, with intracellular vacuole extension and coalescence to open lumen compartments. RNAi studies demonstrate that membrane type 1‐MMP (MT1‐MMP) is required to enable the movement of EPCs on the matrix and that EPCs sense matrix stiffness through signalling cascades leading to the activation of the RhoGTPase Cdc42. Collectively, these results suggest that coupled responses for VEGF stimulation and modulation of substrate stiffness are required to regulate tube morphogenesis of EPCs.</description><identifier>ISSN: 1582-1838</identifier><identifier>EISSN: 1582-4934</identifier><identifier>DOI: 10.1111/j.1582-4934.2009.00981.x</identifier><identifier>PMID: 19968735</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Angiogenesis ; Antigens ; Biochemistry ; Cdc42 protein ; Cell Differentiation ; Cell Division ; Cell growth ; Cell migration ; Cell Movement ; Cells ; Cells, Cultured ; Circulatory system ; Electron microscopes ; Endothelial Cells - metabolism ; endothelial progenitor cells ; Endothelium, Vascular - growth & development ; Extracellular matrix ; Extracellular Matrix - metabolism ; Female ; Homeostasis ; Humans ; Hydrogels ; Hydrogels - chemistry ; Infant, Newborn ; Intracellular signalling ; Ischemia ; Male ; Matrix metalloproteinase ; Matrix Metalloproteinases - metabolism ; Microscopy, Electron, Transmission ; Morphogenesis ; Phenols ; Progenitor cells ; RNA-mediated interference ; Stem Cells - metabolism ; Transmission electron microscopy ; tubulogenesis ; Vascular endothelial growth factor ; Vascular Endothelial Growth Factors - pharmacology ; Viscoelasticity</subject><ispartof>Journal of cellular and molecular medicine, 2010-10, Vol.14 (10), p.2436-2447</ispartof><rights>2009 The Authors Journal compilation © 2010 Foundation for Cellular and Molecular Medicine/Blackwell Publishing Ltd</rights><rights>2009 The Authors Journal compilation © 2010 Foundation for Cellular and Molecular Medicine/Blackwell Publishing Ltd.</rights><rights>2010. This work is published under https://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Copyright Blackwell Publishing Ltd. Oct 2010</rights><rights>2009 The Authors Journal compilation © 2010 Foundation for Cellular and Molecular Medicine/Blackwell Publishing Ltd 2009</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5281-1b09f4c151bd89edba06a0706be50aa714c0140220babbb2dff5b928e19c39903</citedby><cites>FETCH-LOGICAL-c5281-1b09f4c151bd89edba06a0706be50aa714c0140220babbb2dff5b928e19c39903</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/PMC3823161/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3823161/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,1417,11562,27924,27925,45574,45575,46052,46476,53791,53793</link.rule.ids><linktorsrc>$$Uhttps://onlinelibrary.wiley.com/doi/abs/10.1111%2Fj.1582-4934.2009.00981.x$$EView_record_in_Wiley-Blackwell$$FView_record_in_$$GWiley-Blackwell</linktorsrc><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19968735$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hanjaya‐Putra, Donny</creatorcontrib><creatorcontrib>Yee, Jane</creatorcontrib><creatorcontrib>Ceci, Doug</creatorcontrib><creatorcontrib>Truitt, Rachel</creatorcontrib><creatorcontrib>Yee, Derek</creatorcontrib><creatorcontrib>Gerecht, Sharon</creatorcontrib><title>Vascular endothelial growth factor and substrate mechanics regulate in vitro tubulogenesis of endothelial progenitor cells</title><title>Journal of cellular and molecular medicine</title><addtitle>J Cell Mol Med</addtitle><description>Endothelial progenitor cells (EPCs) in the circulatory system have been suggested to maintain vascular homeostasis and contribute to adult vascular regeneration and repair. These processes require that EPCs break down the extracellular matrix (ECM), migrate, differentiate and undergo tube morphogenesis. Evidently, the ECM plays a critical role by providing biochemical and biophysical cues that regulate cellular behaviour. Using a chemically and mechanically tunable hydrogel to study tube morphogenesis in vitro, we show that vascular endothelial growth factor (VEGF) and substrate mechanics co‐regulate tubulogenesis of EPCs. High levels of VEGF are required to initiate tube morphogenesis and activate matrix metalloproteinases (MMPs), which enable EPC migration. Under these conditions, the elasticity of the substrate affects the progression of tube morphogenesis. With decreases in substrate stiffness, we observe decreased MMP expression while increased cellular elongation, with intracellular vacuole extension and coalescence to open lumen compartments. RNAi studies demonstrate that membrane type 1‐MMP (MT1‐MMP) is required to enable the movement of EPCs on the matrix and that EPCs sense matrix stiffness through signalling cascades leading to the activation of the RhoGTPase Cdc42. Collectively, these results suggest that coupled responses for VEGF stimulation and modulation of substrate stiffness are required to regulate tube morphogenesis of EPCs.</description><subject>Angiogenesis</subject><subject>Antigens</subject><subject>Biochemistry</subject><subject>Cdc42 protein</subject><subject>Cell Differentiation</subject><subject>Cell Division</subject><subject>Cell growth</subject><subject>Cell migration</subject><subject>Cell Movement</subject><subject>Cells</subject><subject>Cells, Cultured</subject><subject>Circulatory system</subject><subject>Electron microscopes</subject><subject>Endothelial Cells - metabolism</subject><subject>endothelial progenitor cells</subject><subject>Endothelium, Vascular - growth & development</subject><subject>Extracellular matrix</subject><subject>Extracellular Matrix - metabolism</subject><subject>Female</subject><subject>Homeostasis</subject><subject>Humans</subject><subject>Hydrogels</subject><subject>Hydrogels - chemistry</subject><subject>Infant, Newborn</subject><subject>Intracellular signalling</subject><subject>Ischemia</subject><subject>Male</subject><subject>Matrix metalloproteinase</subject><subject>Matrix Metalloproteinases - metabolism</subject><subject>Microscopy, Electron, Transmission</subject><subject>Morphogenesis</subject><subject>Phenols</subject><subject>Progenitor cells</subject><subject>RNA-mediated interference</subject><subject>Stem Cells - metabolism</subject><subject>Transmission electron microscopy</subject><subject>tubulogenesis</subject><subject>Vascular endothelial growth factor</subject><subject>Vascular Endothelial Growth Factors - pharmacology</subject><subject>Viscoelasticity</subject><issn>1582-1838</issn><issn>1582-4934</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqNkk2PFCEQhonRuOvoXzBED56mLaA_4KCJmair2Y0X9UqApmeYMDBC937466V3JqtrYiIJoUI99YaXKoQwgYqU9XpbkYbTZS1YXVEAUZXNSXX9AJ3eJR4eY8IZP0FPct4CsJYw8RidECFa3rHmFP38rrKZvErYhj6OG-ud8nid4tW4wYMyY0xYhR7nSecxqdHinTUbFZzJONl1qSxXLuBLN6aIx0lPPq5tsNllHId7ovs0Z9ysaKz3-Sl6NCif7bPjuUDfPrz_ujpbnn_5-Gn17nxpGsrJkmgQQ21IQ3TPhe21glZBB622DSjVkdoAqYFS0EprTfthaLSg3BJhmBDAFujtQXc_6Z3tjQ3FiJf75HYq3cionLyfCW4j1_FSMk4ZKT-2QK-OAin-mGwe5c7l2YIKNk5Zdi0BRjnUhXzxF7mNUwrFneTAa867hhbo5b8gBl0jGs7a-dX8QJkUc052uHswATkPgdzKub9y7rWch0DeDoG8LqXP_zT8u_DY9QK8OQBXztub_xaWn1cXFyVivwCJlsOv</recordid><startdate>201010</startdate><enddate>201010</enddate><creator>Hanjaya‐Putra, Donny</creator><creator>Yee, Jane</creator><creator>Ceci, Doug</creator><creator>Truitt, Rachel</creator><creator>Yee, Derek</creator><creator>Gerecht, Sharon</creator><general>Blackwell Publishing Ltd</general><general>John Wiley & Sons, Inc</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>3V.</scope><scope>7QP</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>201010</creationdate><title>Vascular endothelial growth factor and substrate mechanics regulate in vitro tubulogenesis of endothelial progenitor cells</title><author>Hanjaya‐Putra, Donny ; Yee, Jane ; Ceci, Doug ; Truitt, Rachel ; Yee, Derek ; Gerecht, Sharon</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5281-1b09f4c151bd89edba06a0706be50aa714c0140220babbb2dff5b928e19c39903</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Angiogenesis</topic><topic>Antigens</topic><topic>Biochemistry</topic><topic>Cdc42 protein</topic><topic>Cell Differentiation</topic><topic>Cell Division</topic><topic>Cell growth</topic><topic>Cell migration</topic><topic>Cell Movement</topic><topic>Cells</topic><topic>Cells, Cultured</topic><topic>Circulatory system</topic><topic>Electron microscopes</topic><topic>Endothelial Cells - metabolism</topic><topic>endothelial progenitor cells</topic><topic>Endothelium, Vascular - growth & development</topic><topic>Extracellular matrix</topic><topic>Extracellular Matrix - metabolism</topic><topic>Female</topic><topic>Homeostasis</topic><topic>Humans</topic><topic>Hydrogels</topic><topic>Hydrogels - chemistry</topic><topic>Infant, Newborn</topic><topic>Intracellular signalling</topic><topic>Ischemia</topic><topic>Male</topic><topic>Matrix metalloproteinase</topic><topic>Matrix Metalloproteinases - metabolism</topic><topic>Microscopy, Electron, Transmission</topic><topic>Morphogenesis</topic><topic>Phenols</topic><topic>Progenitor cells</topic><topic>RNA-mediated interference</topic><topic>Stem Cells - metabolism</topic><topic>Transmission electron microscopy</topic><topic>tubulogenesis</topic><topic>Vascular endothelial growth factor</topic><topic>Vascular Endothelial Growth Factors - pharmacology</topic><topic>Viscoelasticity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hanjaya‐Putra, Donny</creatorcontrib><creatorcontrib>Yee, Jane</creatorcontrib><creatorcontrib>Ceci, Doug</creatorcontrib><creatorcontrib>Truitt, Rachel</creatorcontrib><creatorcontrib>Yee, Derek</creatorcontrib><creatorcontrib>Gerecht, Sharon</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>ProQuest_Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech 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>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</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>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>ProQuest Science Journals</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of cellular and molecular medicine</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext_linktorsrc</fulltext></delivery><addata><au>Hanjaya‐Putra, Donny</au><au>Yee, Jane</au><au>Ceci, Doug</au><au>Truitt, Rachel</au><au>Yee, Derek</au><au>Gerecht, Sharon</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Vascular endothelial growth factor and substrate mechanics regulate in vitro tubulogenesis of endothelial progenitor cells</atitle><jtitle>Journal of cellular and molecular medicine</jtitle><addtitle>J Cell Mol Med</addtitle><date>2010-10</date><risdate>2010</risdate><volume>14</volume><issue>10</issue><spage>2436</spage><epage>2447</epage><pages>2436-2447</pages><issn>1582-1838</issn><eissn>1582-4934</eissn><abstract>Endothelial progenitor cells (EPCs) in the circulatory system have been suggested to maintain vascular homeostasis and contribute to adult vascular regeneration and repair. These processes require that EPCs break down the extracellular matrix (ECM), migrate, differentiate and undergo tube morphogenesis. Evidently, the ECM plays a critical role by providing biochemical and biophysical cues that regulate cellular behaviour. Using a chemically and mechanically tunable hydrogel to study tube morphogenesis in vitro, we show that vascular endothelial growth factor (VEGF) and substrate mechanics co‐regulate tubulogenesis of EPCs. High levels of VEGF are required to initiate tube morphogenesis and activate matrix metalloproteinases (MMPs), which enable EPC migration. Under these conditions, the elasticity of the substrate affects the progression of tube morphogenesis. With decreases in substrate stiffness, we observe decreased MMP expression while increased cellular elongation, with intracellular vacuole extension and coalescence to open lumen compartments. RNAi studies demonstrate that membrane type 1‐MMP (MT1‐MMP) is required to enable the movement of EPCs on the matrix and that EPCs sense matrix stiffness through signalling cascades leading to the activation of the RhoGTPase Cdc42. Collectively, these results suggest that coupled responses for VEGF stimulation and modulation of substrate stiffness are required to regulate tube morphogenesis of EPCs.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>19968735</pmid><doi>10.1111/j.1582-4934.2009.00981.x</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Angiogenesis Antigens Biochemistry Cdc42 protein Cell Differentiation Cell Division Cell growth Cell migration Cell Movement Cells Cells, Cultured Circulatory system Electron microscopes Endothelial Cells - metabolism endothelial progenitor cells Endothelium, Vascular - growth & development Extracellular matrix Extracellular Matrix - metabolism Female Homeostasis Humans Hydrogels Hydrogels - chemistry Infant, Newborn Intracellular signalling Ischemia Male Matrix metalloproteinase Matrix Metalloproteinases - metabolism Microscopy, Electron, Transmission Morphogenesis Phenols Progenitor cells RNA-mediated interference Stem Cells - metabolism Transmission electron microscopy tubulogenesis Vascular endothelial growth factor Vascular Endothelial Growth Factors - pharmacology Viscoelasticity |
title | Vascular endothelial growth factor and substrate mechanics regulate in vitro tubulogenesis of endothelial progenitor cells |
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