Attenuation of actinomyosinII contractile activity in growth cones accelerates filopodia-guided and microtubule-based neurite elongation
Abstract The myosinII-specific inhibitor blebbistatin was used to attenuate actinomyosinII contractility in E7-chicken retina explant, medulla and spinal cord neuronal cell cultures. Addition of 20–100 μM blebbistatin, a concentration range that reversibly disrupts actin stress fibers, led to a redu...
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| Veröffentlicht in: | Brain research 2007-10, Vol.1176, p.1-10 |
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| creator | Rösner, Harald Möller, Wolfgang Wassermann, Torsten Mihatsch, Julia Blum, Martin |
| description | Abstract The myosinII-specific inhibitor blebbistatin was used to attenuate actinomyosinII contractility in E7-chicken retina explant, medulla and spinal cord neuronal cell cultures. Addition of 20–100 μM blebbistatin, a concentration range that reversibly disrupts actin stress fibers, led to a reduction of growth cone lamellipodial areas and to an elongation of filopodia within 5 to 10 min. These morphological changes were completely reversed after removing the inhibitor. In the continued presence of blebbistatin for several hours, a dose-dependent acceleration (up to 6-fold) of neurite outgrowth was observed. The rapidly elongating neuritic processes displayed narrowed growth cones with one to three long filopodia at the leading edge. At the same time, thin neuritic branches emerged in a “push”-like fashion guided by filopodial extensions. Immunocytochemical characterization of these thin sprouts revealed that they contained actin filaments, myosinIIA, phosphorylated neurofilament/tau epitopes, MAP2, NCAM-PSA, and microtubules, demonstrating that these processes presented neurites and not filopodia. The crucial involvement of microtubules in blebbistatin-induced accelerated neurite extension was confirmed by its inhibition in the presence of nocodazole or taxol. The promotion by blebbistatin of neurite outgrowth occurred on polylysine, laminin, as well as on fibronectin as substrate. The presence of the Rho/ROCK-inhibitor Y-27632 also caused a dose-dependent promotion of neurite growth which was, however, 3-fold less pronounced as compared to blebbistatin. In contrast to blebbistatin, Y-27632 led to the enlargement of growth cone lamellipodial extensions. Our data demonstrate that neurite outgrowth and branching are inversely correlated with the degree of actinomyosinII contractility which determines the speed of retrograde flow and turnover of actin filaments and, by this, microtubule extension. |
| doi_str_mv | 10.1016/j.brainres.2007.07.081 |
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Addition of 20–100 μM blebbistatin, a concentration range that reversibly disrupts actin stress fibers, led to a reduction of growth cone lamellipodial areas and to an elongation of filopodia within 5 to 10 min. These morphological changes were completely reversed after removing the inhibitor. In the continued presence of blebbistatin for several hours, a dose-dependent acceleration (up to 6-fold) of neurite outgrowth was observed. The rapidly elongating neuritic processes displayed narrowed growth cones with one to three long filopodia at the leading edge. At the same time, thin neuritic branches emerged in a “push”-like fashion guided by filopodial extensions. Immunocytochemical characterization of these thin sprouts revealed that they contained actin filaments, myosinIIA, phosphorylated neurofilament/tau epitopes, MAP2, NCAM-PSA, and microtubules, demonstrating that these processes presented neurites and not filopodia. The crucial involvement of microtubules in blebbistatin-induced accelerated neurite extension was confirmed by its inhibition in the presence of nocodazole or taxol. The promotion by blebbistatin of neurite outgrowth occurred on polylysine, laminin, as well as on fibronectin as substrate. The presence of the Rho/ROCK-inhibitor Y-27632 also caused a dose-dependent promotion of neurite growth which was, however, 3-fold less pronounced as compared to blebbistatin. In contrast to blebbistatin, Y-27632 led to the enlargement of growth cone lamellipodial extensions. Our data demonstrate that neurite outgrowth and branching are inversely correlated with the degree of actinomyosinII contractility which determines the speed of retrograde flow and turnover of actin filaments and, by this, microtubule extension.</description><identifier>ISSN: 0006-8993</identifier><identifier>EISSN: 1872-6240</identifier><identifier>DOI: 10.1016/j.brainres.2007.07.081</identifier><identifier>PMID: 17888886</identifier><identifier>CODEN: BRREAP</identifier><language>eng</language><publisher>London: Elsevier B.V</publisher><subject>Actin ; Actomyosin - antagonists & inhibitors ; Actomyosin - metabolism ; Amides - pharmacology ; Animals ; Biological and medical sciences ; Blebbistatin ; Cell structures and functions ; Central Nervous System - cytology ; Central Nervous System - embryology ; Central Nervous System - metabolism ; Chick Embryo ; Contractile Proteins - metabolism ; Cytoskeletal Proteins - metabolism ; Cytoskeleton, cytoplasm. Intracellular movements ; Dose-Response Relationship, Drug ; Enzyme Inhibitors - pharmacology ; Fibronectins - metabolism ; Fibronectins - pharmacology ; Fundamental and applied biological sciences. Psychology ; Growth Cones - metabolism ; Growth Cones - ultrastructure ; Heterocyclic Compounds, 4 or More Rings - pharmacology ; Laminin - metabolism ; Laminin - pharmacology ; Microtubules ; Microtubules - metabolism ; Microtubules - ultrastructure ; Molecular and cellular biology ; Myosin ; Neural Pathways - cytology ; Neural Pathways - embryology ; Neural Pathways - metabolism ; Neurite outgrowth ; Neurites - metabolism ; Neurites - ultrastructure ; Neurogenesis - physiology ; Neurology ; Nocodazole - pharmacology ; Paclitaxel - pharmacology ; Pseudopodia - metabolism ; Pseudopodia - ultrastructure ; Pyridines - pharmacology ; rho GTP-Binding Proteins - antagonists & inhibitors ; rho GTP-Binding Proteins - metabolism ; Tubulin Modulators - pharmacology</subject><ispartof>Brain research, 2007-10, Vol.1176, p.1-10</ispartof><rights>Elsevier B.V.</rights><rights>2007 Elsevier B.V.</rights><rights>2008 INIST-CNRS</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c548t-c579b5939d46854d304c676e52b9056b406d2c13967ab43bc4550c7d786d19333</citedby><cites>FETCH-LOGICAL-c548t-c579b5939d46854d304c676e52b9056b406d2c13967ab43bc4550c7d786d19333</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0006899307015715$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=19190148$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/17888886$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Rösner, Harald</creatorcontrib><creatorcontrib>Möller, Wolfgang</creatorcontrib><creatorcontrib>Wassermann, Torsten</creatorcontrib><creatorcontrib>Mihatsch, Julia</creatorcontrib><creatorcontrib>Blum, Martin</creatorcontrib><title>Attenuation of actinomyosinII contractile activity in growth cones accelerates filopodia-guided and microtubule-based neurite elongation</title><title>Brain research</title><addtitle>Brain Res</addtitle><description>Abstract The myosinII-specific inhibitor blebbistatin was used to attenuate actinomyosinII contractility in E7-chicken retina explant, medulla and spinal cord neuronal cell cultures. Addition of 20–100 μM blebbistatin, a concentration range that reversibly disrupts actin stress fibers, led to a reduction of growth cone lamellipodial areas and to an elongation of filopodia within 5 to 10 min. These morphological changes were completely reversed after removing the inhibitor. In the continued presence of blebbistatin for several hours, a dose-dependent acceleration (up to 6-fold) of neurite outgrowth was observed. The rapidly elongating neuritic processes displayed narrowed growth cones with one to three long filopodia at the leading edge. At the same time, thin neuritic branches emerged in a “push”-like fashion guided by filopodial extensions. Immunocytochemical characterization of these thin sprouts revealed that they contained actin filaments, myosinIIA, phosphorylated neurofilament/tau epitopes, MAP2, NCAM-PSA, and microtubules, demonstrating that these processes presented neurites and not filopodia. The crucial involvement of microtubules in blebbistatin-induced accelerated neurite extension was confirmed by its inhibition in the presence of nocodazole or taxol. The promotion by blebbistatin of neurite outgrowth occurred on polylysine, laminin, as well as on fibronectin as substrate. The presence of the Rho/ROCK-inhibitor Y-27632 also caused a dose-dependent promotion of neurite growth which was, however, 3-fold less pronounced as compared to blebbistatin. In contrast to blebbistatin, Y-27632 led to the enlargement of growth cone lamellipodial extensions. Our data demonstrate that neurite outgrowth and branching are inversely correlated with the degree of actinomyosinII contractility which determines the speed of retrograde flow and turnover of actin filaments and, by this, microtubule extension.</description><subject>Actin</subject><subject>Actomyosin - antagonists & inhibitors</subject><subject>Actomyosin - metabolism</subject><subject>Amides - pharmacology</subject><subject>Animals</subject><subject>Biological and medical sciences</subject><subject>Blebbistatin</subject><subject>Cell structures and functions</subject><subject>Central Nervous System - cytology</subject><subject>Central Nervous System - embryology</subject><subject>Central Nervous System - metabolism</subject><subject>Chick Embryo</subject><subject>Contractile Proteins - metabolism</subject><subject>Cytoskeletal Proteins - metabolism</subject><subject>Cytoskeleton, cytoplasm. Intracellular movements</subject><subject>Dose-Response Relationship, Drug</subject><subject>Enzyme Inhibitors - pharmacology</subject><subject>Fibronectins - metabolism</subject><subject>Fibronectins - pharmacology</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Growth Cones - metabolism</subject><subject>Growth Cones - ultrastructure</subject><subject>Heterocyclic Compounds, 4 or More Rings - pharmacology</subject><subject>Laminin - metabolism</subject><subject>Laminin - pharmacology</subject><subject>Microtubules</subject><subject>Microtubules - metabolism</subject><subject>Microtubules - ultrastructure</subject><subject>Molecular and cellular biology</subject><subject>Myosin</subject><subject>Neural Pathways - cytology</subject><subject>Neural Pathways - embryology</subject><subject>Neural Pathways - metabolism</subject><subject>Neurite outgrowth</subject><subject>Neurites - metabolism</subject><subject>Neurites - ultrastructure</subject><subject>Neurogenesis - physiology</subject><subject>Neurology</subject><subject>Nocodazole - pharmacology</subject><subject>Paclitaxel - pharmacology</subject><subject>Pseudopodia - metabolism</subject><subject>Pseudopodia - ultrastructure</subject><subject>Pyridines - pharmacology</subject><subject>rho GTP-Binding Proteins - antagonists & inhibitors</subject><subject>rho GTP-Binding Proteins - metabolism</subject><subject>Tubulin Modulators - pharmacology</subject><issn>0006-8993</issn><issn>1872-6240</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2007</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFUk2PFCEQ7RiNO67-hU1f9NZj0dBAX4ybjR-TbOJBPRMaqkfGHhiBXjP_wJ8tvTNmEy9LKnxUPeoVvKqqKwJrAoS_3a2HqJ2PmNYtgFgvJsmTakWkaBveMnharQCAN7Lv6UX1IqVdOVLaw_Pqggi5DL6q_lznjH7W2QVfh7HWJjsf9seQnN9sahN8jotvwvvQncvH2vl6G8Pv_GMJYyoBgxNGnct-dFM4BOt0s52dRVtrb-u9MzHkeZgnbAaditfjHF3GGqfgt_fkL6tno54Svjqvl9X3jx--3Xxubr982txc3zamYzKXWfRD19PeMi47ZikwwwXHrh166PjAgNvWENpzoQdGB8O6DoywQnJLekrpZfXmlPcQw68ZU1Z7l0r9k_YY5qS4ZCBaRh4FtkAlEOgKkJ-A5ZEpRRzVIbq9jkdFQC1iqZ36J5ZaxFKLyYXh6swwD3u0D9fO6hTA6zNAJ6OnMWpvXHrA9aQHwmTBvT_hsHzcncOoknHoDVoX0WRlg3u8lnf_pTCT866w_sQjpl2Yoy-yKKJSq0B9XVpr6SwQQDpBOvoX3QjNgQ</recordid><startdate>20071024</startdate><enddate>20071024</enddate><creator>Rösner, Harald</creator><creator>Möller, Wolfgang</creator><creator>Wassermann, Torsten</creator><creator>Mihatsch, Julia</creator><creator>Blum, Martin</creator><general>Elsevier B.V</general><general>Elsevier</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>7TK</scope><scope>7X8</scope></search><sort><creationdate>20071024</creationdate><title>Attenuation of actinomyosinII contractile activity in growth cones accelerates filopodia-guided and microtubule-based neurite elongation</title><author>Rösner, Harald ; Möller, Wolfgang ; Wassermann, Torsten ; Mihatsch, Julia ; Blum, Martin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c548t-c579b5939d46854d304c676e52b9056b406d2c13967ab43bc4550c7d786d19333</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2007</creationdate><topic>Actin</topic><topic>Actomyosin - antagonists & inhibitors</topic><topic>Actomyosin - metabolism</topic><topic>Amides - pharmacology</topic><topic>Animals</topic><topic>Biological and medical sciences</topic><topic>Blebbistatin</topic><topic>Cell structures and functions</topic><topic>Central Nervous System - cytology</topic><topic>Central Nervous System - embryology</topic><topic>Central Nervous System - metabolism</topic><topic>Chick Embryo</topic><topic>Contractile Proteins - metabolism</topic><topic>Cytoskeletal Proteins - metabolism</topic><topic>Cytoskeleton, cytoplasm. Intracellular movements</topic><topic>Dose-Response Relationship, Drug</topic><topic>Enzyme Inhibitors - pharmacology</topic><topic>Fibronectins - metabolism</topic><topic>Fibronectins - pharmacology</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Growth Cones - metabolism</topic><topic>Growth Cones - ultrastructure</topic><topic>Heterocyclic Compounds, 4 or More Rings - pharmacology</topic><topic>Laminin - metabolism</topic><topic>Laminin - pharmacology</topic><topic>Microtubules</topic><topic>Microtubules - metabolism</topic><topic>Microtubules - ultrastructure</topic><topic>Molecular and cellular biology</topic><topic>Myosin</topic><topic>Neural Pathways - cytology</topic><topic>Neural Pathways - embryology</topic><topic>Neural Pathways - metabolism</topic><topic>Neurite outgrowth</topic><topic>Neurites - metabolism</topic><topic>Neurites - ultrastructure</topic><topic>Neurogenesis - physiology</topic><topic>Neurology</topic><topic>Nocodazole - pharmacology</topic><topic>Paclitaxel - pharmacology</topic><topic>Pseudopodia - metabolism</topic><topic>Pseudopodia - ultrastructure</topic><topic>Pyridines - pharmacology</topic><topic>rho GTP-Binding Proteins - antagonists & inhibitors</topic><topic>rho GTP-Binding Proteins - metabolism</topic><topic>Tubulin Modulators - pharmacology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Rösner, Harald</creatorcontrib><creatorcontrib>Möller, Wolfgang</creatorcontrib><creatorcontrib>Wassermann, Torsten</creatorcontrib><creatorcontrib>Mihatsch, Julia</creatorcontrib><creatorcontrib>Blum, Martin</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>Neurosciences Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Brain research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Rösner, Harald</au><au>Möller, Wolfgang</au><au>Wassermann, Torsten</au><au>Mihatsch, Julia</au><au>Blum, Martin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Attenuation of actinomyosinII contractile activity in growth cones accelerates filopodia-guided and microtubule-based neurite elongation</atitle><jtitle>Brain research</jtitle><addtitle>Brain Res</addtitle><date>2007-10-24</date><risdate>2007</risdate><volume>1176</volume><spage>1</spage><epage>10</epage><pages>1-10</pages><issn>0006-8993</issn><eissn>1872-6240</eissn><coden>BRREAP</coden><abstract>Abstract The myosinII-specific inhibitor blebbistatin was used to attenuate actinomyosinII contractility in E7-chicken retina explant, medulla and spinal cord neuronal cell cultures. Addition of 20–100 μM blebbistatin, a concentration range that reversibly disrupts actin stress fibers, led to a reduction of growth cone lamellipodial areas and to an elongation of filopodia within 5 to 10 min. These morphological changes were completely reversed after removing the inhibitor. In the continued presence of blebbistatin for several hours, a dose-dependent acceleration (up to 6-fold) of neurite outgrowth was observed. The rapidly elongating neuritic processes displayed narrowed growth cones with one to three long filopodia at the leading edge. At the same time, thin neuritic branches emerged in a “push”-like fashion guided by filopodial extensions. Immunocytochemical characterization of these thin sprouts revealed that they contained actin filaments, myosinIIA, phosphorylated neurofilament/tau epitopes, MAP2, NCAM-PSA, and microtubules, demonstrating that these processes presented neurites and not filopodia. The crucial involvement of microtubules in blebbistatin-induced accelerated neurite extension was confirmed by its inhibition in the presence of nocodazole or taxol. The promotion by blebbistatin of neurite outgrowth occurred on polylysine, laminin, as well as on fibronectin as substrate. The presence of the Rho/ROCK-inhibitor Y-27632 also caused a dose-dependent promotion of neurite growth which was, however, 3-fold less pronounced as compared to blebbistatin. In contrast to blebbistatin, Y-27632 led to the enlargement of growth cone lamellipodial extensions. Our data demonstrate that neurite outgrowth and branching are inversely correlated with the degree of actinomyosinII contractility which determines the speed of retrograde flow and turnover of actin filaments and, by this, microtubule extension.</abstract><cop>London</cop><cop>Amsterdam</cop><cop>New York, NY</cop><pub>Elsevier B.V</pub><pmid>17888886</pmid><doi>10.1016/j.brainres.2007.07.081</doi><tpages>10</tpages></addata></record> |
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| subjects | Actin Actomyosin - antagonists & inhibitors Actomyosin - metabolism Amides - pharmacology Animals Biological and medical sciences Blebbistatin Cell structures and functions Central Nervous System - cytology Central Nervous System - embryology Central Nervous System - metabolism Chick Embryo Contractile Proteins - metabolism Cytoskeletal Proteins - metabolism Cytoskeleton, cytoplasm. Intracellular movements Dose-Response Relationship, Drug Enzyme Inhibitors - pharmacology Fibronectins - metabolism Fibronectins - pharmacology Fundamental and applied biological sciences. Psychology Growth Cones - metabolism Growth Cones - ultrastructure Heterocyclic Compounds, 4 or More Rings - pharmacology Laminin - metabolism Laminin - pharmacology Microtubules Microtubules - metabolism Microtubules - ultrastructure Molecular and cellular biology Myosin Neural Pathways - cytology Neural Pathways - embryology Neural Pathways - metabolism Neurite outgrowth Neurites - metabolism Neurites - ultrastructure Neurogenesis - physiology Neurology Nocodazole - pharmacology Paclitaxel - pharmacology Pseudopodia - metabolism Pseudopodia - ultrastructure Pyridines - pharmacology rho GTP-Binding Proteins - antagonists & inhibitors rho GTP-Binding Proteins - metabolism Tubulin Modulators - pharmacology |
| title | Attenuation of actinomyosinII contractile activity in growth cones accelerates filopodia-guided and microtubule-based neurite elongation |
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