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Migration Inhibitory Factor Mediates Angiogenesis via Mitogen-Activated Protein Kinase and Phosphatidylinositol Kinase
ABSTRACT—In this study, we investigated the effects of migration inhibitory factor (rhMIF) on angiogenesis-related signaling cascades and apoptosis in human endothelial cells (ECs). We show that in vitro rhMIF induces migration and tube formation in Matrigel of human dermal microvascular endothelial...
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| Published in: | Circulation research 2003-08, Vol.93 (4), p.321-329 |
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| container_title | Circulation research |
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| creator | Amin, M Asif Volpert, Olga V Woods, James M Kumar, Pawan Harlow, Lisa A Koch, Alisa E |
| description | ABSTRACT—In this study, we investigated the effects of migration inhibitory factor (rhMIF) on angiogenesis-related signaling cascades and apoptosis in human endothelial cells (ECs). We show that in vitro rhMIF induces migration and tube formation in Matrigel of human dermal microvascular endothelial cells (HMVECs), with potency comparable to that of basic fibroblast growth factor. In vivo, rhMIF induces angiogenesis in Matrigel plugs and in the corneal bioassay. Using panels of relatively specific kinase inhibitors, antisense oligonucleotides, and dominant-negative mutants, we show that mitogen-activated protein kinase (MAPK) and phosphatidylinositol 3-kinase (PI3K) are critical for MIF-dependent HMVEC migration, whereas Src and p38 kinases are nonessential. Moreover, we demonstrate that rhMIF induces time-dependent increases in phosphorylation levels of MEK1/2, Erk1/2, and Elk-1, as well as PI3K, and its effector kinase, Akt, in HMVECs. Studies with dominant-negative mutants and antisense oligonucleotides corroborate these effects in HMVECs. Furthermore, we demonstrate that rhMIF-induced angiogenesis in the rat cornea in vivo and in the ex vivo endothelial cell morphogenesis assay is also MAPK- and PI3K-dependent. Our findings support a role for MIF as an angiogenic factor and provide a rationale for the use of MIF as a therapeutic inducer of neovascularization in the development of collateral circulation in coronary artery disease. |
| doi_str_mv | 10.1161/01.RES.0000087641.56024.DA |
| format | article |
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We show that in vitro rhMIF induces migration and tube formation in Matrigel of human dermal microvascular endothelial cells (HMVECs), with potency comparable to that of basic fibroblast growth factor. In vivo, rhMIF induces angiogenesis in Matrigel plugs and in the corneal bioassay. Using panels of relatively specific kinase inhibitors, antisense oligonucleotides, and dominant-negative mutants, we show that mitogen-activated protein kinase (MAPK) and phosphatidylinositol 3-kinase (PI3K) are critical for MIF-dependent HMVEC migration, whereas Src and p38 kinases are nonessential. Moreover, we demonstrate that rhMIF induces time-dependent increases in phosphorylation levels of MEK1/2, Erk1/2, and Elk-1, as well as PI3K, and its effector kinase, Akt, in HMVECs. Studies with dominant-negative mutants and antisense oligonucleotides corroborate these effects in HMVECs. Furthermore, we demonstrate that rhMIF-induced angiogenesis in the rat cornea in vivo and in the ex vivo endothelial cell morphogenesis assay is also MAPK- and PI3K-dependent. Our findings support a role for MIF as an angiogenic factor and provide a rationale for the use of MIF as a therapeutic inducer of neovascularization in the development of collateral circulation in coronary artery disease.</description><identifier>ISSN: 0009-7330</identifier><identifier>EISSN: 1524-4571</identifier><identifier>DOI: 10.1161/01.RES.0000087641.56024.DA</identifier><identifier>PMID: 12881477</identifier><identifier>CODEN: CIRUAL</identifier><language>eng</language><publisher>Hagerstown, MD: American Heart Association, Inc</publisher><subject>Angiogenesis Inducing Agents - pharmacology ; Animals ; Biological and medical sciences ; Blood vessels and receptors ; Cell Line ; Cell Movement - drug effects ; Chromones - pharmacology ; Cornea - blood supply ; DNA-Binding Proteins ; Dose-Response Relationship, Drug ; Endothelium, Vascular - cytology ; Endothelium, Vascular - drug effects ; Endothelium, Vascular - metabolism ; Enzyme Inhibitors - pharmacology ; ets-Domain Protein Elk-1 ; Flavonoids - pharmacology ; Fundamental and applied biological sciences. Psychology ; Humans ; Macrophage Migration-Inhibitory Factors - pharmacology ; Mice ; Mice, Inbred C57BL ; Mitogen-Activated Protein Kinase 1 - antagonists & inhibitors ; Mitogen-Activated Protein Kinase 1 - metabolism ; Mitogen-Activated Protein Kinase 3 ; Mitogen-Activated Protein Kinases - antagonists & inhibitors ; Mitogen-Activated Protein Kinases - genetics ; Mitogen-Activated Protein Kinases - metabolism ; Morpholines - pharmacology ; Mutation ; Neovascularization, Physiologic - drug effects ; Oligonucleotides, Antisense - pharmacology ; Phosphatidylinositol 3-Kinases - antagonists & inhibitors ; Phosphatidylinositol 3-Kinases - metabolism ; Phosphorylation ; Protein-Serine-Threonine Kinases ; Proto-Oncogene Proteins - metabolism ; Proto-Oncogene Proteins c-akt ; Rats ; Recombinant Proteins - pharmacology ; Signal Transduction - drug effects ; Transcription Factors ; Vertebrates: cardiovascular system</subject><ispartof>Circulation research, 2003-08, Vol.93 (4), p.321-329</ispartof><rights>2003 American Heart Association, Inc.</rights><rights>2004 INIST-CNRS</rights><rights>Copyright American Heart Association, Inc. Aug 22 2003</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5718-1e126dfdd082cb929650f2d60de33b6721d2e6f23deadb782051354a7c05a6e03</citedby><cites>FETCH-LOGICAL-c5718-1e126dfdd082cb929650f2d60de33b6721d2e6f23deadb782051354a7c05a6e03</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>315,786,790,27957,27958</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=15090334$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/12881477$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Amin, M Asif</creatorcontrib><creatorcontrib>Volpert, Olga V</creatorcontrib><creatorcontrib>Woods, James M</creatorcontrib><creatorcontrib>Kumar, Pawan</creatorcontrib><creatorcontrib>Harlow, Lisa A</creatorcontrib><creatorcontrib>Koch, Alisa E</creatorcontrib><title>Migration Inhibitory Factor Mediates Angiogenesis via Mitogen-Activated Protein Kinase and Phosphatidylinositol Kinase</title><title>Circulation research</title><addtitle>Circ Res</addtitle><description>ABSTRACT—In this study, we investigated the effects of migration inhibitory factor (rhMIF) on angiogenesis-related signaling cascades and apoptosis in human endothelial cells (ECs). We show that in vitro rhMIF induces migration and tube formation in Matrigel of human dermal microvascular endothelial cells (HMVECs), with potency comparable to that of basic fibroblast growth factor. In vivo, rhMIF induces angiogenesis in Matrigel plugs and in the corneal bioassay. Using panels of relatively specific kinase inhibitors, antisense oligonucleotides, and dominant-negative mutants, we show that mitogen-activated protein kinase (MAPK) and phosphatidylinositol 3-kinase (PI3K) are critical for MIF-dependent HMVEC migration, whereas Src and p38 kinases are nonessential. Moreover, we demonstrate that rhMIF induces time-dependent increases in phosphorylation levels of MEK1/2, Erk1/2, and Elk-1, as well as PI3K, and its effector kinase, Akt, in HMVECs. Studies with dominant-negative mutants and antisense oligonucleotides corroborate these effects in HMVECs. Furthermore, we demonstrate that rhMIF-induced angiogenesis in the rat cornea in vivo and in the ex vivo endothelial cell morphogenesis assay is also MAPK- and PI3K-dependent. Our findings support a role for MIF as an angiogenic factor and provide a rationale for the use of MIF as a therapeutic inducer of neovascularization in the development of collateral circulation in coronary artery disease.</description><subject>Angiogenesis Inducing Agents - pharmacology</subject><subject>Animals</subject><subject>Biological and medical sciences</subject><subject>Blood vessels and receptors</subject><subject>Cell Line</subject><subject>Cell Movement - drug effects</subject><subject>Chromones - pharmacology</subject><subject>Cornea - blood supply</subject><subject>DNA-Binding Proteins</subject><subject>Dose-Response Relationship, Drug</subject><subject>Endothelium, Vascular - cytology</subject><subject>Endothelium, Vascular - drug effects</subject><subject>Endothelium, Vascular - metabolism</subject><subject>Enzyme Inhibitors - pharmacology</subject><subject>ets-Domain Protein Elk-1</subject><subject>Flavonoids - pharmacology</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Humans</subject><subject>Macrophage Migration-Inhibitory Factors - pharmacology</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mitogen-Activated Protein Kinase 1 - antagonists & inhibitors</subject><subject>Mitogen-Activated Protein Kinase 1 - metabolism</subject><subject>Mitogen-Activated Protein Kinase 3</subject><subject>Mitogen-Activated Protein Kinases - antagonists & inhibitors</subject><subject>Mitogen-Activated Protein Kinases - genetics</subject><subject>Mitogen-Activated Protein Kinases - metabolism</subject><subject>Morpholines - pharmacology</subject><subject>Mutation</subject><subject>Neovascularization, Physiologic - drug effects</subject><subject>Oligonucleotides, Antisense - pharmacology</subject><subject>Phosphatidylinositol 3-Kinases - antagonists & inhibitors</subject><subject>Phosphatidylinositol 3-Kinases - metabolism</subject><subject>Phosphorylation</subject><subject>Protein-Serine-Threonine Kinases</subject><subject>Proto-Oncogene Proteins - metabolism</subject><subject>Proto-Oncogene Proteins c-akt</subject><subject>Rats</subject><subject>Recombinant Proteins - pharmacology</subject><subject>Signal Transduction - drug effects</subject><subject>Transcription Factors</subject><subject>Vertebrates: cardiovascular system</subject><issn>0009-7330</issn><issn>1524-4571</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2003</creationdate><recordtype>article</recordtype><recordid>eNpdkVuP0zAQhS0EYsvCX0DRSvCWML7kxlu1F1ixFYjLs-XEk8ZLanftpKv-e9w2UiX8cmTPNzPHOoRcUcgoLegnoNnP218ZHE5VFoJmeQFMZDfLF2RBcyZSkZf0JVnEep2WnMMFeRPCIwAVnNWvyQVlVUVFWS7IbmXWXo3G2eTe9qYxo_P75E61UZMVaqNGDMnSro1bo8VgQrIzKllFLt7TZTuaXUR08sO7EY1NvhmrAibKxqfehW0fh-v9YKwLsWeY62_Jq04NAd_Nekn-3N3-vv6aPnz_cn-9fEjb-IMqpUhZoTutoWJtU7O6yKFjugCNnDdFyahmWHSMa1S6KSsGOeW5UGULuSoQ-CX5eJq79e5pwjDKjQktDoOy6KYgS14A5BWL4NV_4KObvI3eJKNMCA6UR-jzCWq9C8FjJ7febJTfSwryEI0EKmM08hyNPEYjb5ax-f28YWo2qM-tcxYR-DADKrRq6LyyrQlnLocaOBeREyfu2Q0j-vB3mJ7Ryx7VMPbH1dEsS9lBK8YgPZrh_wDk3Kfq</recordid><startdate>20030822</startdate><enddate>20030822</enddate><creator>Amin, M Asif</creator><creator>Volpert, Olga V</creator><creator>Woods, James M</creator><creator>Kumar, Pawan</creator><creator>Harlow, Lisa A</creator><creator>Koch, Alisa E</creator><general>American Heart Association, Inc</general><general>Lippincott</general><general>Lippincott Williams & Wilkins Ovid Technologies</general><scope>IQODW</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>7QP</scope><scope>7T5</scope><scope>7TK</scope><scope>H94</scope><scope>K9.</scope><scope>7X8</scope></search><sort><creationdate>20030822</creationdate><title>Migration Inhibitory Factor Mediates Angiogenesis via Mitogen-Activated Protein Kinase and Phosphatidylinositol Kinase</title><author>Amin, M Asif ; Volpert, Olga V ; Woods, James M ; Kumar, Pawan ; Harlow, Lisa A ; Koch, Alisa E</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5718-1e126dfdd082cb929650f2d60de33b6721d2e6f23deadb782051354a7c05a6e03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2003</creationdate><topic>Angiogenesis Inducing Agents - pharmacology</topic><topic>Animals</topic><topic>Biological and medical sciences</topic><topic>Blood vessels and receptors</topic><topic>Cell Line</topic><topic>Cell Movement - drug effects</topic><topic>Chromones - pharmacology</topic><topic>Cornea - blood supply</topic><topic>DNA-Binding Proteins</topic><topic>Dose-Response Relationship, Drug</topic><topic>Endothelium, Vascular - cytology</topic><topic>Endothelium, Vascular - drug effects</topic><topic>Endothelium, Vascular - metabolism</topic><topic>Enzyme Inhibitors - pharmacology</topic><topic>ets-Domain Protein Elk-1</topic><topic>Flavonoids - pharmacology</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Humans</topic><topic>Macrophage Migration-Inhibitory Factors - pharmacology</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mitogen-Activated Protein Kinase 1 - antagonists & inhibitors</topic><topic>Mitogen-Activated Protein Kinase 1 - metabolism</topic><topic>Mitogen-Activated Protein Kinase 3</topic><topic>Mitogen-Activated Protein Kinases - antagonists & inhibitors</topic><topic>Mitogen-Activated Protein Kinases - genetics</topic><topic>Mitogen-Activated Protein Kinases - metabolism</topic><topic>Morpholines - pharmacology</topic><topic>Mutation</topic><topic>Neovascularization, Physiologic - drug effects</topic><topic>Oligonucleotides, Antisense - pharmacology</topic><topic>Phosphatidylinositol 3-Kinases - antagonists & inhibitors</topic><topic>Phosphatidylinositol 3-Kinases - metabolism</topic><topic>Phosphorylation</topic><topic>Protein-Serine-Threonine Kinases</topic><topic>Proto-Oncogene Proteins - metabolism</topic><topic>Proto-Oncogene Proteins c-akt</topic><topic>Rats</topic><topic>Recombinant Proteins - pharmacology</topic><topic>Signal Transduction - drug effects</topic><topic>Transcription Factors</topic><topic>Vertebrates: cardiovascular system</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Amin, M Asif</creatorcontrib><creatorcontrib>Volpert, Olga V</creatorcontrib><creatorcontrib>Woods, James M</creatorcontrib><creatorcontrib>Kumar, Pawan</creatorcontrib><creatorcontrib>Harlow, Lisa A</creatorcontrib><creatorcontrib>Koch, Alisa E</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>Circulation research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Amin, M Asif</au><au>Volpert, Olga V</au><au>Woods, James M</au><au>Kumar, Pawan</au><au>Harlow, Lisa A</au><au>Koch, Alisa E</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Migration Inhibitory Factor Mediates Angiogenesis via Mitogen-Activated Protein Kinase and Phosphatidylinositol Kinase</atitle><jtitle>Circulation research</jtitle><addtitle>Circ Res</addtitle><date>2003-08-22</date><risdate>2003</risdate><volume>93</volume><issue>4</issue><spage>321</spage><epage>329</epage><pages>321-329</pages><issn>0009-7330</issn><eissn>1524-4571</eissn><coden>CIRUAL</coden><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>ABSTRACT—In this study, we investigated the effects of migration inhibitory factor (rhMIF) on angiogenesis-related signaling cascades and apoptosis in human endothelial cells (ECs). We show that in vitro rhMIF induces migration and tube formation in Matrigel of human dermal microvascular endothelial cells (HMVECs), with potency comparable to that of basic fibroblast growth factor. In vivo, rhMIF induces angiogenesis in Matrigel plugs and in the corneal bioassay. Using panels of relatively specific kinase inhibitors, antisense oligonucleotides, and dominant-negative mutants, we show that mitogen-activated protein kinase (MAPK) and phosphatidylinositol 3-kinase (PI3K) are critical for MIF-dependent HMVEC migration, whereas Src and p38 kinases are nonessential. Moreover, we demonstrate that rhMIF induces time-dependent increases in phosphorylation levels of MEK1/2, Erk1/2, and Elk-1, as well as PI3K, and its effector kinase, Akt, in HMVECs. Studies with dominant-negative mutants and antisense oligonucleotides corroborate these effects in HMVECs. Furthermore, we demonstrate that rhMIF-induced angiogenesis in the rat cornea in vivo and in the ex vivo endothelial cell morphogenesis assay is also MAPK- and PI3K-dependent. Our findings support a role for MIF as an angiogenic factor and provide a rationale for the use of MIF as a therapeutic inducer of neovascularization in the development of collateral circulation in coronary artery disease.</abstract><cop>Hagerstown, MD</cop><pub>American Heart Association, Inc</pub><pmid>12881477</pmid><doi>10.1161/01.RES.0000087641.56024.DA</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Circulation research, 2003-08, Vol.93 (4), p.321-329 |
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| subjects | Angiogenesis Inducing Agents - pharmacology Animals Biological and medical sciences Blood vessels and receptors Cell Line Cell Movement - drug effects Chromones - pharmacology Cornea - blood supply DNA-Binding Proteins Dose-Response Relationship, Drug Endothelium, Vascular - cytology Endothelium, Vascular - drug effects Endothelium, Vascular - metabolism Enzyme Inhibitors - pharmacology ets-Domain Protein Elk-1 Flavonoids - pharmacology Fundamental and applied biological sciences. Psychology Humans Macrophage Migration-Inhibitory Factors - pharmacology Mice Mice, Inbred C57BL Mitogen-Activated Protein Kinase 1 - antagonists & inhibitors Mitogen-Activated Protein Kinase 1 - metabolism Mitogen-Activated Protein Kinase 3 Mitogen-Activated Protein Kinases - antagonists & inhibitors Mitogen-Activated Protein Kinases - genetics Mitogen-Activated Protein Kinases - metabolism Morpholines - pharmacology Mutation Neovascularization, Physiologic - drug effects Oligonucleotides, Antisense - pharmacology Phosphatidylinositol 3-Kinases - antagonists & inhibitors Phosphatidylinositol 3-Kinases - metabolism Phosphorylation Protein-Serine-Threonine Kinases Proto-Oncogene Proteins - metabolism Proto-Oncogene Proteins c-akt Rats Recombinant Proteins - pharmacology Signal Transduction - drug effects Transcription Factors Vertebrates: cardiovascular system |
| title | Migration Inhibitory Factor Mediates Angiogenesis via Mitogen-Activated Protein Kinase and Phosphatidylinositol Kinase |
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