Angiogenin enhances cell migration by regulating stress fiber assembly and focal adhesion dynamics
Angiogenin (ANG) acts on both vascular endothelial cells and cancer cells, but the underlying mechanism remains elusive. In this study, we carried out a co-immunoprecipitation assay in HeLa cells and identified 14 potential ANG-interacting proteins. Among these proteins, β-actin, α-actinin 4, and no...
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| creator | Wei, Saisai Gao, Xiangwei Du, Juan Su, Jinfeng Xu, Zhengping |
| description | Angiogenin (ANG) acts on both vascular endothelial cells and cancer cells, but the underlying mechanism remains elusive. In this study, we carried out a co-immunoprecipitation assay in HeLa cells and identified 14 potential ANG-interacting proteins. Among these proteins, β-actin, α-actinin 4, and non-muscle myosin heavy chain 9 are stress fiber components and involved in cytoskeleton organization and movement, which prompted us to investigate the mechanism of action of ANG in cell migration. Upon confirmation of the interactions between ANG and the three proteins, further studies revealed that ANG co-localized with β-actin and α-actinin 4 at the leading edge of migrating cells. Down-regulation of ANG resulted in fewer but thicker stress fibers with less dynamics, which was associated with the enlargements of focal adhesions. The focal adhesion kinase activity and cell migration capacity were significantly decreased in ANG-deficient cells. Taken together, our data demonstrated that the existence of ANG in the cytoplasm optimizes stress fiber assembly and focal adhesion formation to accommodate cell migration. The finding that ANG promoted cancer cell migration might provide new clues for tumor metastasis research. |
| doi_str_mv | 10.1371/journal.pone.0028797 |
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In this study, we carried out a co-immunoprecipitation assay in HeLa cells and identified 14 potential ANG-interacting proteins. Among these proteins, β-actin, α-actinin 4, and non-muscle myosin heavy chain 9 are stress fiber components and involved in cytoskeleton organization and movement, which prompted us to investigate the mechanism of action of ANG in cell migration. Upon confirmation of the interactions between ANG and the three proteins, further studies revealed that ANG co-localized with β-actin and α-actinin 4 at the leading edge of migrating cells. Down-regulation of ANG resulted in fewer but thicker stress fibers with less dynamics, which was associated with the enlargements of focal adhesions. The focal adhesion kinase activity and cell migration capacity were significantly decreased in ANG-deficient cells. Taken together, our data demonstrated that the existence of ANG in the cytoplasm optimizes stress fiber assembly and focal adhesion formation to accommodate cell migration. The finding that ANG promoted cancer cell migration might provide new clues for tumor metastasis research.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0028797</identifier><identifier>PMID: 22194915</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Actin ; Adhesion ; Angiogenin ; Assembly ; Biology ; Cancer ; Cancer metastasis ; Cell adhesion & migration ; Cell migration ; Cell Movement ; Cytoplasm ; Cytoskeleton ; Cytoskeleton - metabolism ; Down-Regulation ; Endothelial cells ; Environmental health ; Enzyme Activation ; Fibers ; Focal adhesion kinase ; Focal Adhesion Protein-Tyrosine Kinases - metabolism ; Focal Adhesions - metabolism ; Gene expression ; HeLa Cells ; Human Umbilical Vein Endothelial Cells - cytology ; Humans ; Identification ; Immunoprecipitation ; Kinases ; Mammals ; Mass Spectrometry ; Medicine ; Metastases ; Molecular Sequence Annotation ; Motility ; Muscle proteins ; Muscles ; Myosin ; Peptides ; Phosphorylation ; Protein Binding ; Proteins ; Pseudopodia - metabolism ; Ribonuclease, Pancreatic - deficiency ; Ribonuclease, Pancreatic - metabolism ; Smooth muscle ; Stress ; Stress Fibers - metabolism ; Stresses ; α-Actinin</subject><ispartof>PloS one, 2011-12, Vol.6 (12), p.e28797-e28797</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>2011 Wei 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>Wei et al. 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c691t-7b674d788afd47d42d21d56c3311747bc424b55f7855458fb02ed90993d3ba4a3</citedby><cites>FETCH-LOGICAL-c691t-7b674d788afd47d42d21d56c3311747bc424b55f7855458fb02ed90993d3ba4a3</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/PMC3237552/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3237552/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22194915$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Addison, Christina Lynn</contributor><creatorcontrib>Wei, Saisai</creatorcontrib><creatorcontrib>Gao, Xiangwei</creatorcontrib><creatorcontrib>Du, Juan</creatorcontrib><creatorcontrib>Su, Jinfeng</creatorcontrib><creatorcontrib>Xu, Zhengping</creatorcontrib><title>Angiogenin enhances cell migration by regulating stress fiber assembly and focal adhesion dynamics</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Angiogenin (ANG) acts on both vascular endothelial cells and cancer cells, but the underlying mechanism remains elusive. In this study, we carried out a co-immunoprecipitation assay in HeLa cells and identified 14 potential ANG-interacting proteins. Among these proteins, β-actin, α-actinin 4, and non-muscle myosin heavy chain 9 are stress fiber components and involved in cytoskeleton organization and movement, which prompted us to investigate the mechanism of action of ANG in cell migration. Upon confirmation of the interactions between ANG and the three proteins, further studies revealed that ANG co-localized with β-actin and α-actinin 4 at the leading edge of migrating cells. Down-regulation of ANG resulted in fewer but thicker stress fibers with less dynamics, which was associated with the enlargements of focal adhesions. The focal adhesion kinase activity and cell migration capacity were significantly decreased in ANG-deficient cells. Taken together, our data demonstrated that the existence of ANG in the cytoplasm optimizes stress fiber assembly and focal adhesion formation to accommodate cell migration. The finding that ANG promoted cancer cell migration might provide new clues for tumor metastasis research.</description><subject>Actin</subject><subject>Adhesion</subject><subject>Angiogenin</subject><subject>Assembly</subject><subject>Biology</subject><subject>Cancer</subject><subject>Cancer metastasis</subject><subject>Cell adhesion & migration</subject><subject>Cell migration</subject><subject>Cell Movement</subject><subject>Cytoplasm</subject><subject>Cytoskeleton</subject><subject>Cytoskeleton - metabolism</subject><subject>Down-Regulation</subject><subject>Endothelial cells</subject><subject>Environmental health</subject><subject>Enzyme Activation</subject><subject>Fibers</subject><subject>Focal adhesion kinase</subject><subject>Focal Adhesion Protein-Tyrosine Kinases - metabolism</subject><subject>Focal Adhesions - metabolism</subject><subject>Gene expression</subject><subject>HeLa Cells</subject><subject>Human Umbilical Vein Endothelial Cells - cytology</subject><subject>Humans</subject><subject>Identification</subject><subject>Immunoprecipitation</subject><subject>Kinases</subject><subject>Mammals</subject><subject>Mass Spectrometry</subject><subject>Medicine</subject><subject>Metastases</subject><subject>Molecular Sequence Annotation</subject><subject>Motility</subject><subject>Muscle proteins</subject><subject>Muscles</subject><subject>Myosin</subject><subject>Peptides</subject><subject>Phosphorylation</subject><subject>Protein Binding</subject><subject>Proteins</subject><subject>Pseudopodia - metabolism</subject><subject>Ribonuclease, Pancreatic - deficiency</subject><subject>Ribonuclease, Pancreatic - metabolism</subject><subject>Smooth muscle</subject><subject>Stress</subject><subject>Stress Fibers - metabolism</subject><subject>Stresses</subject><subject>α-Actinin</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</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><sourceid>DOA</sourceid><recordid>eNqNk1uL1DAYhoso7jr6D0QLguLFjM2hSXsjDIuHgYUFT7chTb52MmSSMWnF-femTneZyl5IL9okz_t-zXfIsueoWCHC0budH4KTdnXwDlZFgSte8wfZJaoJXjJckIdn3xfZkxh3RVGSirHH2QXGqKY1Ki-zZu064ztwxuXgttIpiLkCa_O96YLsjXd5c8wDdINNK9flsQ8QY96aBkIuY4R9Y4-5dDpvvZI2l3oLcZTpo5N7o-LT7FErbYRn03uRff_44dvV5-X1zafN1fp6qViN-iVvGKeaV5VsNeWaYo2RLpkiBCFOeaMopk1ZtrwqS1pWbVNg0HVR10STRlJJFtnLk-_B-iim9ESBCMIoiSqWiM2J0F7uxCGYvQxH4aURfzd86IQMvVEWRDJnRBUKGGa0hKpGFKEKa6ZRjQmD5PV-ijY0e9AKXB-knZnOT5zZis7_EgQTXpY4GbyZDIL_OUDsxd7EMfPSgR-iqFGKTOpUw0X26h_y_stNVCfT_xvX-hRWjZ5iTTmrWEFYlajVPVR6NKRapVZqTdqfCd7OBInp4XffySFGsfn65f_Zmx9z9vUZuwVp-230dhg7Ls5BegJV8DEGaO9yjAoxTsJtNsQ4CWKahCR7cV6fO9Ft65M_g-0C-A</recordid><startdate>20111214</startdate><enddate>20111214</enddate><creator>Wei, Saisai</creator><creator>Gao, Xiangwei</creator><creator>Du, Juan</creator><creator>Su, Jinfeng</creator><creator>Xu, Zhengping</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20111214</creationdate><title>Angiogenin enhances cell migration by regulating stress fiber assembly and focal adhesion dynamics</title><author>Wei, Saisai ; Gao, Xiangwei ; Du, Juan ; Su, Jinfeng ; Xu, Zhengping</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c691t-7b674d788afd47d42d21d56c3311747bc424b55f7855458fb02ed90993d3ba4a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Actin</topic><topic>Adhesion</topic><topic>Angiogenin</topic><topic>Assembly</topic><topic>Biology</topic><topic>Cancer</topic><topic>Cancer metastasis</topic><topic>Cell adhesion & migration</topic><topic>Cell migration</topic><topic>Cell Movement</topic><topic>Cytoplasm</topic><topic>Cytoskeleton</topic><topic>Cytoskeleton - 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Academic</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>Wei, Saisai</au><au>Gao, Xiangwei</au><au>Du, Juan</au><au>Su, Jinfeng</au><au>Xu, Zhengping</au><au>Addison, Christina Lynn</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Angiogenin enhances cell migration by regulating stress fiber assembly and focal adhesion dynamics</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2011-12-14</date><risdate>2011</risdate><volume>6</volume><issue>12</issue><spage>e28797</spage><epage>e28797</epage><pages>e28797-e28797</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Angiogenin (ANG) acts on both vascular endothelial cells and cancer cells, but the underlying mechanism remains elusive. In this study, we carried out a co-immunoprecipitation assay in HeLa cells and identified 14 potential ANG-interacting proteins. Among these proteins, β-actin, α-actinin 4, and non-muscle myosin heavy chain 9 are stress fiber components and involved in cytoskeleton organization and movement, which prompted us to investigate the mechanism of action of ANG in cell migration. Upon confirmation of the interactions between ANG and the three proteins, further studies revealed that ANG co-localized with β-actin and α-actinin 4 at the leading edge of migrating cells. Down-regulation of ANG resulted in fewer but thicker stress fibers with less dynamics, which was associated with the enlargements of focal adhesions. The focal adhesion kinase activity and cell migration capacity were significantly decreased in ANG-deficient cells. Taken together, our data demonstrated that the existence of ANG in the cytoplasm optimizes stress fiber assembly and focal adhesion formation to accommodate cell migration. The finding that ANG promoted cancer cell migration might provide new clues for tumor metastasis research.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22194915</pmid><doi>10.1371/journal.pone.0028797</doi><tpages>e28797</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Actin Adhesion Angiogenin Assembly Biology Cancer Cancer metastasis Cell adhesion & migration Cell migration Cell Movement Cytoplasm Cytoskeleton Cytoskeleton - metabolism Down-Regulation Endothelial cells Environmental health Enzyme Activation Fibers Focal adhesion kinase Focal Adhesion Protein-Tyrosine Kinases - metabolism Focal Adhesions - metabolism Gene expression HeLa Cells Human Umbilical Vein Endothelial Cells - cytology Humans Identification Immunoprecipitation Kinases Mammals Mass Spectrometry Medicine Metastases Molecular Sequence Annotation Motility Muscle proteins Muscles Myosin Peptides Phosphorylation Protein Binding Proteins Pseudopodia - metabolism Ribonuclease, Pancreatic - deficiency Ribonuclease, Pancreatic - metabolism Smooth muscle Stress Stress Fibers - metabolism Stresses α-Actinin |
| title | Angiogenin enhances cell migration by regulating stress fiber assembly and focal adhesion dynamics |
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