Cell Surface Heparan Sulfate Chains Regulate Local Reception of FGF Signaling in the Mouse Embryo
Heparan sulfate (HS) proteoglycans modulate the activity of multiple growth factors on the cell surface and extracellular matrix. However, it remains unclear how the HS chains control the movement and reception of growth factors into targeted receiving cells during mammalian morphogenetic processes....
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| Veröffentlicht in: | Developmental cell 2011-08, Vol.21 (2), p.257-272 |
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| container_title | Developmental cell |
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| creator | Shimokawa, Kayo Kimura-Yoshida, Chiharu Nagai, Naoko Mukai, Kazuhiro Matsubara, Kazumi Watanabe, Hideto Matsuda, Yoichi Mochida, Kyoko Matsuo, Isao |
| description | Heparan sulfate (HS) proteoglycans modulate the activity of multiple growth factors on the cell surface and extracellular matrix. However, it remains unclear how the HS chains control the movement and reception of growth factors into targeted receiving cells during mammalian morphogenetic processes. Here, we found that HS-deficient Ext2 null mutant mouse embryos fail to respond to fibroblast growth factor (FGF) signaling. Marker expression analyses revealed that cell surface-tethered HS chains are crucial for local retention of FGF4 and FGF8 ligands in the extraembryonic ectoderm. Fine chimeric studies with single-cell resolution and expression studies with specific inhibitors for HS movement demonstrated that proteolytic cleavage of HS chains can spread FGF signaling to adjacent cells within a short distance. Together, the results show that spatiotemporal expression of cell surface-tethered HS chains regulate the local reception of FGF-signaling activity during mammalian embryogenesis.
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► Local heparan sulfate expression can determine which cells bind and respond to FGF ► Heparan sulfate can move to immediately adjacent cells and activate FGF signaling ► Proteolytic cleavage of heparan sulfate proteoglycans can control FGF signaling |
| doi_str_mv | 10.1016/j.devcel.2011.06.027 |
| format | Article |
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[Display omitted]
► Local heparan sulfate expression can determine which cells bind and respond to FGF ► Heparan sulfate can move to immediately adjacent cells and activate FGF signaling ► Proteolytic cleavage of heparan sulfate proteoglycans can control FGF signaling</description><identifier>ISSN: 1534-5807</identifier><identifier>EISSN: 1878-1551</identifier><identifier>DOI: 10.1016/j.devcel.2011.06.027</identifier><identifier>PMID: 21839920</identifier><language>eng</language><publisher>Cambridge, MA: Elsevier Inc</publisher><subject>Animals ; Biological and medical sciences ; Cell differentiation, maturation, development, hematopoiesis ; Cell physiology ; Disaccharides - metabolism ; Embryo, Mammalian - cytology ; Embryo, Mammalian - drug effects ; Embryo, Mammalian - metabolism ; Enzyme Inhibitors - pharmacology ; Enzyme-Linked Immunosorbent Assay ; Fibroblast Growth Factor 4 - metabolism ; Fibroblast Growth Factor 8 - metabolism ; Fibroblast Growth Factors - genetics ; Fibroblast Growth Factors - metabolism ; Fundamental and applied biological sciences. Psychology ; Gene Expression Regulation, Developmental - drug effects ; Gene Expression Regulation, Developmental - physiology ; Green Fluorescent Proteins - genetics ; Heparitin Sulfate - metabolism ; Mice ; Mice, Knockout ; Models, Biological ; Molecular and cellular biology ; Mutation - genetics ; N-Acetylglucosaminyltransferases - genetics ; Organ Culture Techniques ; Protein Binding ; Signal Transduction - genetics ; Signal Transduction - physiology</subject><ispartof>Developmental cell, 2011-08, Vol.21 (2), p.257-272</ispartof><rights>2011 Elsevier Inc.</rights><rights>2015 INIST-CNRS</rights><rights>Copyright © 2011 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c437t-8b49471f27b78429bfeb7818dc72d559843562d963fe99732007abdd750a1da93</citedby><cites>FETCH-LOGICAL-c437t-8b49471f27b78429bfeb7818dc72d559843562d963fe99732007abdd750a1da93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.devcel.2011.06.027$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=24440525$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21839920$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Shimokawa, Kayo</creatorcontrib><creatorcontrib>Kimura-Yoshida, Chiharu</creatorcontrib><creatorcontrib>Nagai, Naoko</creatorcontrib><creatorcontrib>Mukai, Kazuhiro</creatorcontrib><creatorcontrib>Matsubara, Kazumi</creatorcontrib><creatorcontrib>Watanabe, Hideto</creatorcontrib><creatorcontrib>Matsuda, Yoichi</creatorcontrib><creatorcontrib>Mochida, Kyoko</creatorcontrib><creatorcontrib>Matsuo, Isao</creatorcontrib><title>Cell Surface Heparan Sulfate Chains Regulate Local Reception of FGF Signaling in the Mouse Embryo</title><title>Developmental cell</title><addtitle>Dev Cell</addtitle><description>Heparan sulfate (HS) proteoglycans modulate the activity of multiple growth factors on the cell surface and extracellular matrix. However, it remains unclear how the HS chains control the movement and reception of growth factors into targeted receiving cells during mammalian morphogenetic processes. Here, we found that HS-deficient Ext2 null mutant mouse embryos fail to respond to fibroblast growth factor (FGF) signaling. Marker expression analyses revealed that cell surface-tethered HS chains are crucial for local retention of FGF4 and FGF8 ligands in the extraembryonic ectoderm. Fine chimeric studies with single-cell resolution and expression studies with specific inhibitors for HS movement demonstrated that proteolytic cleavage of HS chains can spread FGF signaling to adjacent cells within a short distance. Together, the results show that spatiotemporal expression of cell surface-tethered HS chains regulate the local reception of FGF-signaling activity during mammalian embryogenesis.
[Display omitted]
► Local heparan sulfate expression can determine which cells bind and respond to FGF ► Heparan sulfate can move to immediately adjacent cells and activate FGF signaling ► Proteolytic cleavage of heparan sulfate proteoglycans can control FGF signaling</description><subject>Animals</subject><subject>Biological and medical sciences</subject><subject>Cell differentiation, maturation, development, hematopoiesis</subject><subject>Cell physiology</subject><subject>Disaccharides - metabolism</subject><subject>Embryo, Mammalian - cytology</subject><subject>Embryo, Mammalian - drug effects</subject><subject>Embryo, Mammalian - metabolism</subject><subject>Enzyme Inhibitors - pharmacology</subject><subject>Enzyme-Linked Immunosorbent Assay</subject><subject>Fibroblast Growth Factor 4 - metabolism</subject><subject>Fibroblast Growth Factor 8 - metabolism</subject><subject>Fibroblast Growth Factors - genetics</subject><subject>Fibroblast Growth Factors - metabolism</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Expression Regulation, Developmental - drug effects</subject><subject>Gene Expression Regulation, Developmental - physiology</subject><subject>Green Fluorescent Proteins - genetics</subject><subject>Heparitin Sulfate - metabolism</subject><subject>Mice</subject><subject>Mice, Knockout</subject><subject>Models, Biological</subject><subject>Molecular and cellular biology</subject><subject>Mutation - genetics</subject><subject>N-Acetylglucosaminyltransferases - genetics</subject><subject>Organ Culture Techniques</subject><subject>Protein Binding</subject><subject>Signal Transduction - genetics</subject><subject>Signal Transduction - physiology</subject><issn>1534-5807</issn><issn>1878-1551</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kNFqFDEUhoMotlbfQCQ34tWMSSaZJDeCLN22sCJYvQ6Z5GSbJTuzJjOFvr1ZdrV3XuX88P0nhw-h95S0lND-86718OggtYxQ2pK-JUy-QJdUSdVQIejLOouON0IReYHelLIjtUYVeY0uGFWd1oxcIruClPD9koN1gG_hYLMda07BzoBXDzaOBf-A7ZKOeTM5m2p0cJjjNOIp4PXNGt_H7WhTHLc4jnh-APxtWgrg6_2Qn6a36FWwqcC783uFfq2vf65um833m7vV103jeCfnRg1cc0kDk4NUnOkhQB2o8k4yL4RWvBM987rvAmgtO0aItIP3UhBLvdXdFfp02nvI0-8Fymz2sVQ_yY5QzzFKdYor2ZNK8hPp8lRKhmAOOe5tfjKUmKNbszMnt-bo1pDeVLe19uH8wTLswf8r_ZVZgY9nwJbqKVSTLpZnjnNOBBOV-3LioOp4jJBNcRFGBz5mcLPxU_z_JX8AKciXqA</recordid><startdate>20110816</startdate><enddate>20110816</enddate><creator>Shimokawa, Kayo</creator><creator>Kimura-Yoshida, Chiharu</creator><creator>Nagai, Naoko</creator><creator>Mukai, Kazuhiro</creator><creator>Matsubara, Kazumi</creator><creator>Watanabe, Hideto</creator><creator>Matsuda, Yoichi</creator><creator>Mochida, Kyoko</creator><creator>Matsuo, Isao</creator><general>Elsevier Inc</general><general>Cell Press</general><scope>6I.</scope><scope>AAFTH</scope><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>7X8</scope></search><sort><creationdate>20110816</creationdate><title>Cell Surface Heparan Sulfate Chains Regulate Local Reception of FGF Signaling in the Mouse Embryo</title><author>Shimokawa, Kayo ; Kimura-Yoshida, Chiharu ; Nagai, Naoko ; Mukai, Kazuhiro ; Matsubara, Kazumi ; Watanabe, Hideto ; Matsuda, Yoichi ; Mochida, Kyoko ; Matsuo, Isao</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c437t-8b49471f27b78429bfeb7818dc72d559843562d963fe99732007abdd750a1da93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Animals</topic><topic>Biological and medical sciences</topic><topic>Cell differentiation, maturation, development, hematopoiesis</topic><topic>Cell physiology</topic><topic>Disaccharides - metabolism</topic><topic>Embryo, Mammalian - cytology</topic><topic>Embryo, Mammalian - drug effects</topic><topic>Embryo, Mammalian - metabolism</topic><topic>Enzyme Inhibitors - pharmacology</topic><topic>Enzyme-Linked Immunosorbent Assay</topic><topic>Fibroblast Growth Factor 4 - metabolism</topic><topic>Fibroblast Growth Factor 8 - metabolism</topic><topic>Fibroblast Growth Factors - genetics</topic><topic>Fibroblast Growth Factors - metabolism</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Expression Regulation, Developmental - drug effects</topic><topic>Gene Expression Regulation, Developmental - physiology</topic><topic>Green Fluorescent Proteins - genetics</topic><topic>Heparitin Sulfate - metabolism</topic><topic>Mice</topic><topic>Mice, Knockout</topic><topic>Models, Biological</topic><topic>Molecular and cellular biology</topic><topic>Mutation - genetics</topic><topic>N-Acetylglucosaminyltransferases - genetics</topic><topic>Organ Culture Techniques</topic><topic>Protein Binding</topic><topic>Signal Transduction - genetics</topic><topic>Signal Transduction - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Shimokawa, Kayo</creatorcontrib><creatorcontrib>Kimura-Yoshida, Chiharu</creatorcontrib><creatorcontrib>Nagai, Naoko</creatorcontrib><creatorcontrib>Mukai, Kazuhiro</creatorcontrib><creatorcontrib>Matsubara, Kazumi</creatorcontrib><creatorcontrib>Watanabe, Hideto</creatorcontrib><creatorcontrib>Matsuda, Yoichi</creatorcontrib><creatorcontrib>Mochida, Kyoko</creatorcontrib><creatorcontrib>Matsuo, Isao</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><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>MEDLINE - Academic</collection><jtitle>Developmental cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Shimokawa, Kayo</au><au>Kimura-Yoshida, Chiharu</au><au>Nagai, Naoko</au><au>Mukai, Kazuhiro</au><au>Matsubara, Kazumi</au><au>Watanabe, Hideto</au><au>Matsuda, Yoichi</au><au>Mochida, Kyoko</au><au>Matsuo, Isao</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cell Surface Heparan Sulfate Chains Regulate Local Reception of FGF Signaling in the Mouse Embryo</atitle><jtitle>Developmental cell</jtitle><addtitle>Dev Cell</addtitle><date>2011-08-16</date><risdate>2011</risdate><volume>21</volume><issue>2</issue><spage>257</spage><epage>272</epage><pages>257-272</pages><issn>1534-5807</issn><eissn>1878-1551</eissn><abstract>Heparan sulfate (HS) proteoglycans modulate the activity of multiple growth factors on the cell surface and extracellular matrix. However, it remains unclear how the HS chains control the movement and reception of growth factors into targeted receiving cells during mammalian morphogenetic processes. Here, we found that HS-deficient Ext2 null mutant mouse embryos fail to respond to fibroblast growth factor (FGF) signaling. Marker expression analyses revealed that cell surface-tethered HS chains are crucial for local retention of FGF4 and FGF8 ligands in the extraembryonic ectoderm. Fine chimeric studies with single-cell resolution and expression studies with specific inhibitors for HS movement demonstrated that proteolytic cleavage of HS chains can spread FGF signaling to adjacent cells within a short distance. Together, the results show that spatiotemporal expression of cell surface-tethered HS chains regulate the local reception of FGF-signaling activity during mammalian embryogenesis.
[Display omitted]
► Local heparan sulfate expression can determine which cells bind and respond to FGF ► Heparan sulfate can move to immediately adjacent cells and activate FGF signaling ► Proteolytic cleavage of heparan sulfate proteoglycans can control FGF signaling</abstract><cop>Cambridge, MA</cop><pub>Elsevier Inc</pub><pmid>21839920</pmid><doi>10.1016/j.devcel.2011.06.027</doi><tpages>16</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Biological and medical sciences Cell differentiation, maturation, development, hematopoiesis Cell physiology Disaccharides - metabolism Embryo, Mammalian - cytology Embryo, Mammalian - drug effects Embryo, Mammalian - metabolism Enzyme Inhibitors - pharmacology Enzyme-Linked Immunosorbent Assay Fibroblast Growth Factor 4 - metabolism Fibroblast Growth Factor 8 - metabolism Fibroblast Growth Factors - genetics Fibroblast Growth Factors - metabolism Fundamental and applied biological sciences. Psychology Gene Expression Regulation, Developmental - drug effects Gene Expression Regulation, Developmental - physiology Green Fluorescent Proteins - genetics Heparitin Sulfate - metabolism Mice Mice, Knockout Models, Biological Molecular and cellular biology Mutation - genetics N-Acetylglucosaminyltransferases - genetics Organ Culture Techniques Protein Binding Signal Transduction - genetics Signal Transduction - physiology |
| title | Cell Surface Heparan Sulfate Chains Regulate Local Reception of FGF Signaling in the Mouse Embryo |
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