Axonal regeneration after sciatic nerve lesion is delayed but complete in GFAP- and vimentin-deficient mice
Peripheral axotomy of motoneurons triggers Wallerian degeneration of injured axons distal to the lesion, followed by axon regeneration. Centrally, axotomy induces loss of synapses (synaptic stripping) from the surface of lesioned motoneurons in the spinal cord. At the lesion site, reactive Schwann c...
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| description | Peripheral axotomy of motoneurons triggers Wallerian degeneration of injured axons distal to the lesion, followed by axon regeneration. Centrally, axotomy induces loss of synapses (synaptic stripping) from the surface of lesioned motoneurons in the spinal cord. At the lesion site, reactive Schwann cells provide trophic support and guidance for outgrowing axons. The mechanisms of synaptic stripping remain elusive, but reactive astrocytes and microglia appear to be important in this process. We studied axonal regeneration and synaptic stripping of motoneurons after a sciatic nerve lesion in mice lacking the intermediate filament (nanofilament) proteins glial fibrillary acidic protein (GFAP) and vimentin, which are upregulated in reactive astrocytes and Schwann cells. Seven days after sciatic nerve transection, ultrastructural analysis of synaptic density on the somata of injured motoneurons revealed more remaining boutons covering injured somata in GFAP(-/-)Vim(-/-) mice. After sciatic nerve crush in GFAP(-/-)Vim(-/-) mice, the fraction of reinnervated motor endplates on muscle fibers of the gastrocnemius muscle was reduced 13 days after the injury, and axonal regeneration and functional recovery were delayed but complete. Thus, the absence of GFAP and vimentin in glial cells does not seem to affect the outcome after peripheral motoneuron injury but may have an important effect on the response dynamics. |
| doi_str_mv | 10.1371/journal.pone.0079395 |
| format | Article |
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Centrally, axotomy induces loss of synapses (synaptic stripping) from the surface of lesioned motoneurons in the spinal cord. At the lesion site, reactive Schwann cells provide trophic support and guidance for outgrowing axons. The mechanisms of synaptic stripping remain elusive, but reactive astrocytes and microglia appear to be important in this process. We studied axonal regeneration and synaptic stripping of motoneurons after a sciatic nerve lesion in mice lacking the intermediate filament (nanofilament) proteins glial fibrillary acidic protein (GFAP) and vimentin, which are upregulated in reactive astrocytes and Schwann cells. Seven days after sciatic nerve transection, ultrastructural analysis of synaptic density on the somata of injured motoneurons revealed more remaining boutons covering injured somata in GFAP(-/-)Vim(-/-) mice. After sciatic nerve crush in GFAP(-/-)Vim(-/-) mice, the fraction of reinnervated motor endplates on muscle fibers of the gastrocnemius muscle was reduced 13 days after the injury, and axonal regeneration and functional recovery were delayed but complete. Thus, the absence of GFAP and vimentin in glial cells does not seem to affect the outcome after peripheral motoneuron injury but may have an important effect on the response dynamics.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0079395</identifier><identifier>PMID: 24223940</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Animals ; Astrocytes ; Axon guidance ; Axons ; Axons - pathology ; Axotomy ; Degeneration ; Experiments ; Female ; Gastrocnemius muscle ; Genetic aspects ; Glial cells ; Glial fibrillary acidic protein ; Glial Fibrillary Acidic Protein - deficiency ; Glial Fibrillary Acidic Protein - metabolism ; Immunoglobulins ; Injury analysis ; Injury prevention ; Intermediate filament proteins ; Lesions ; Medicin och hälsovetenskap ; Mental health ; Mice ; Microglia ; Motor endplates ; Motor neurons ; Motor Neurons - pathology ; Muscles ; Muscles - innervation ; Myelin Sheath - physiology ; Nerve Regeneration ; Nervous system ; Neurodegeneration ; Neurogenesis ; Neurosciences ; Neurovetenskaper ; Physiological aspects ; Physiology ; Presynapse ; Proteins ; Recovery of Function ; Regeneration ; Regeneration (Biology) ; Rehabilitation ; Schwann cells ; Sciatic nerve ; Sciatic Nerve - pathology ; Sciatic Nerve - physiopathology ; Sciatic Neuropathy - metabolism ; Sciatic Neuropathy - pathology ; Sciatic Neuropathy - physiopathology ; Spinal cord ; Statistical analysis ; Stem cells ; Stripping ; Synapses ; Synapses - pathology ; Synaptic density ; Up-Regulation ; Vimentin ; Vimentin - deficiency ; Vimentin - metabolism</subject><ispartof>PloS one, 2013-11, Vol.8 (11), p.e79395-e79395</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Berg 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>2013 Berg et al 2013 Berg et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c921t-a292f48f5eceb014be99003075cd4e87002ed3dec041927289b3646de245f5903</citedby><cites>FETCH-LOGICAL-c921t-a292f48f5eceb014be99003075cd4e87002ed3dec041927289b3646de245f5903</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/PMC3815133/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3815133/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,552,727,780,784,864,885,2101,2927,23865,27923,27924,53790,53792,79471,79472</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24223940$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-212333$$DView record from Swedish Publication Index$$Hfree_for_read</backlink><backlink>$$Uhttps://gup.ub.gu.se/publication/188926$$DView record from Swedish Publication Index$$Hfree_for_read</backlink><backlink>$$Uhttp://kipublications.ki.se/Default.aspx?queryparsed=id:127729618$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><contributor>Phillips, William</contributor><creatorcontrib>Berg, Alexander</creatorcontrib><creatorcontrib>Zelano, Johan</creatorcontrib><creatorcontrib>Pekna, Marcela</creatorcontrib><creatorcontrib>Wilhelmsson, Ulrika</creatorcontrib><creatorcontrib>Pekny, Milos</creatorcontrib><creatorcontrib>Cullheim, Staffan</creatorcontrib><title>Axonal regeneration after sciatic nerve lesion is delayed but complete in GFAP- and vimentin-deficient mice</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Peripheral axotomy of motoneurons triggers Wallerian degeneration of injured axons distal to the lesion, followed by axon regeneration. Centrally, axotomy induces loss of synapses (synaptic stripping) from the surface of lesioned motoneurons in the spinal cord. At the lesion site, reactive Schwann cells provide trophic support and guidance for outgrowing axons. The mechanisms of synaptic stripping remain elusive, but reactive astrocytes and microglia appear to be important in this process. We studied axonal regeneration and synaptic stripping of motoneurons after a sciatic nerve lesion in mice lacking the intermediate filament (nanofilament) proteins glial fibrillary acidic protein (GFAP) and vimentin, which are upregulated in reactive astrocytes and Schwann cells. Seven days after sciatic nerve transection, ultrastructural analysis of synaptic density on the somata of injured motoneurons revealed more remaining boutons covering injured somata in GFAP(-/-)Vim(-/-) mice. After sciatic nerve crush in GFAP(-/-)Vim(-/-) mice, the fraction of reinnervated motor endplates on muscle fibers of the gastrocnemius muscle was reduced 13 days after the injury, and axonal regeneration and functional recovery were delayed but complete. Thus, the absence of GFAP and vimentin in glial cells does not seem to affect the outcome after peripheral motoneuron injury but may have an important effect on the response dynamics.</description><subject>Analysis</subject><subject>Animals</subject><subject>Astrocytes</subject><subject>Axon guidance</subject><subject>Axons</subject><subject>Axons - pathology</subject><subject>Axotomy</subject><subject>Degeneration</subject><subject>Experiments</subject><subject>Female</subject><subject>Gastrocnemius muscle</subject><subject>Genetic aspects</subject><subject>Glial cells</subject><subject>Glial fibrillary acidic protein</subject><subject>Glial Fibrillary Acidic Protein - deficiency</subject><subject>Glial Fibrillary Acidic Protein - metabolism</subject><subject>Immunoglobulins</subject><subject>Injury analysis</subject><subject>Injury prevention</subject><subject>Intermediate filament proteins</subject><subject>Lesions</subject><subject>Medicin och hälsovetenskap</subject><subject>Mental health</subject><subject>Mice</subject><subject>Microglia</subject><subject>Motor endplates</subject><subject>Motor neurons</subject><subject>Motor Neurons - pathology</subject><subject>Muscles</subject><subject>Muscles - innervation</subject><subject>Myelin Sheath - physiology</subject><subject>Nerve Regeneration</subject><subject>Nervous system</subject><subject>Neurodegeneration</subject><subject>Neurogenesis</subject><subject>Neurosciences</subject><subject>Neurovetenskaper</subject><subject>Physiological aspects</subject><subject>Physiology</subject><subject>Presynapse</subject><subject>Proteins</subject><subject>Recovery of Function</subject><subject>Regeneration</subject><subject>Regeneration (Biology)</subject><subject>Rehabilitation</subject><subject>Schwann cells</subject><subject>Sciatic nerve</subject><subject>Sciatic Nerve - pathology</subject><subject>Sciatic Nerve - physiopathology</subject><subject>Sciatic Neuropathy - metabolism</subject><subject>Sciatic Neuropathy - pathology</subject><subject>Sciatic Neuropathy - physiopathology</subject><subject>Spinal cord</subject><subject>Statistical analysis</subject><subject>Stem cells</subject><subject>Stripping</subject><subject>Synapses</subject><subject>Synapses - pathology</subject><subject>Synaptic density</subject><subject>Up-Regulation</subject><subject>Vimentin</subject><subject>Vimentin - deficiency</subject><subject>Vimentin - metabolism</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</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>D8T</sourceid><sourceid>DOA</sourceid><recordid>eNqNk21vlTAUx4nRuDn9BkabmBhN5NonoH1jcjPdvMmSGR_2tinlwLpxKVKY27e33MvmMJsRXlBOf_9_23N6oug5wQvCMvL-zA1do-tF6xpYYJxJJpMH0S6RjMYpxezhrfFO9MT7M4wTJtL0cbRDOaVMcrwbnS8vXXBBHVTQQKd76xqkyx465I0NvwaF8AWgGvw4ZT0qoNZXUKB86JFx67aGHpBt0OHB8kuMdFOgC7uGprdNXEBpjQ1jtLYGnkaPSl17eDZ996IfB5--73-Oj44PV_vLo9hISvpYU0lLLsoEDOSY8BykxJjhLDEFB5FhTKFgBRjMiaQZFTJnKU8LoDwpE4nZXvRy69vWzqspT14RzjNBiRRJIFZbonD6TLWdXevuSjlt1SbgukrpLpy9BiWBs1RAqak2POEgWUazUpdhByIvMh284q2X_wXtkM_cptB5GIFKaJIm4-7kvXzbueKP6FpIaJZRmRLxz7WqoVUhVA0biRCSpoF_dy__0Z4sNycdBkUJZeHZiz5MiRvyNRQmFK7T9XyHs5nGnqrKXSgmSEI2Bm8mg879HMD3am29gbrWDbhhLEEiQgpoRgL66i_07kJNVKVDLWxTurCuGU3VMkCci5TJQC3uoMJbQLh3oT9KG-IzwduZIDA9XPaVHrxXq29f_589Ppmzr2-xp6Dr_tS7ehi7ys9BvgVN57zvoLxJMsFqbO_rbKixvdXU3kH24naBbkTX_cx-A5srTF8</recordid><startdate>20131101</startdate><enddate>20131101</enddate><creator>Berg, Alexander</creator><creator>Zelano, Johan</creator><creator>Pekna, Marcela</creator><creator>Wilhelmsson, Ulrika</creator><creator>Pekny, Milos</creator><creator>Cullheim, Staffan</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>AEUYN</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>ACNBI</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D8T</scope><scope>DF2</scope><scope>ZZAVC</scope><scope>F1U</scope><scope>DOA</scope></search><sort><creationdate>20131101</creationdate><title>Axonal regeneration after sciatic nerve lesion is delayed but complete in GFAP- and vimentin-deficient mice</title><author>Berg, Alexander ; Zelano, Johan ; Pekna, Marcela ; Wilhelmsson, Ulrika ; Pekny, Milos ; Cullheim, Staffan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c921t-a292f48f5eceb014be99003075cd4e87002ed3dec041927289b3646de245f5903</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Analysis</topic><topic>Animals</topic><topic>Astrocytes</topic><topic>Axon guidance</topic><topic>Axons</topic><topic>Axons - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>SWEPUB Uppsala universitet full text</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Freely available online</collection><collection>SWEPUB Uppsala universitet</collection><collection>SwePub Articles full text</collection><collection>SWEPUB Göteborgs universitet</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>Berg, Alexander</au><au>Zelano, Johan</au><au>Pekna, Marcela</au><au>Wilhelmsson, Ulrika</au><au>Pekny, Milos</au><au>Cullheim, Staffan</au><au>Phillips, William</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Axonal regeneration after sciatic nerve lesion is delayed but complete in GFAP- and vimentin-deficient mice</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-11-01</date><risdate>2013</risdate><volume>8</volume><issue>11</issue><spage>e79395</spage><epage>e79395</epage><pages>e79395-e79395</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Peripheral axotomy of motoneurons triggers Wallerian degeneration of injured axons distal to the lesion, followed by axon regeneration. Centrally, axotomy induces loss of synapses (synaptic stripping) from the surface of lesioned motoneurons in the spinal cord. At the lesion site, reactive Schwann cells provide trophic support and guidance for outgrowing axons. The mechanisms of synaptic stripping remain elusive, but reactive astrocytes and microglia appear to be important in this process. We studied axonal regeneration and synaptic stripping of motoneurons after a sciatic nerve lesion in mice lacking the intermediate filament (nanofilament) proteins glial fibrillary acidic protein (GFAP) and vimentin, which are upregulated in reactive astrocytes and Schwann cells. Seven days after sciatic nerve transection, ultrastructural analysis of synaptic density on the somata of injured motoneurons revealed more remaining boutons covering injured somata in GFAP(-/-)Vim(-/-) mice. After sciatic nerve crush in GFAP(-/-)Vim(-/-) mice, the fraction of reinnervated motor endplates on muscle fibers of the gastrocnemius muscle was reduced 13 days after the injury, and axonal regeneration and functional recovery were delayed but complete. Thus, the absence of GFAP and vimentin in glial cells does not seem to affect the outcome after peripheral motoneuron injury but may have an important effect on the response dynamics.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24223940</pmid><doi>10.1371/journal.pone.0079395</doi><tpages>e79395</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | PloS one, 2013-11, Vol.8 (11), p.e79395-e79395 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1447821985 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; SWEPUB Freely available online; Public Library of Science (PLoS); EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Analysis Animals Astrocytes Axon guidance Axons Axons - pathology Axotomy Degeneration Experiments Female Gastrocnemius muscle Genetic aspects Glial cells Glial fibrillary acidic protein Glial Fibrillary Acidic Protein - deficiency Glial Fibrillary Acidic Protein - metabolism Immunoglobulins Injury analysis Injury prevention Intermediate filament proteins Lesions Medicin och hälsovetenskap Mental health Mice Microglia Motor endplates Motor neurons Motor Neurons - pathology Muscles Muscles - innervation Myelin Sheath - physiology Nerve Regeneration Nervous system Neurodegeneration Neurogenesis Neurosciences Neurovetenskaper Physiological aspects Physiology Presynapse Proteins Recovery of Function Regeneration Regeneration (Biology) Rehabilitation Schwann cells Sciatic nerve Sciatic Nerve - pathology Sciatic Nerve - physiopathology Sciatic Neuropathy - metabolism Sciatic Neuropathy - pathology Sciatic Neuropathy - physiopathology Spinal cord Statistical analysis Stem cells Stripping Synapses Synapses - pathology Synaptic density Up-Regulation Vimentin Vimentin - deficiency Vimentin - metabolism |
| title | Axonal regeneration after sciatic nerve lesion is delayed but complete in GFAP- and vimentin-deficient mice |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-09T01%3A05%3A20IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Axonal%20regeneration%20after%20sciatic%20nerve%20lesion%20is%20delayed%20but%20complete%20in%20GFAP-%20and%20vimentin-deficient%20mice&rft.jtitle=PloS%20one&rft.au=Berg,%20Alexander&rft.date=2013-11-01&rft.volume=8&rft.issue=11&rft.spage=e79395&rft.epage=e79395&rft.pages=e79395-e79395&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0079395&rft_dat=%3Cgale_plos_%3EA478448639%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1447821985&rft_id=info:pmid/24223940&rft_galeid=A478448639&rft_doaj_id=oai_doaj_org_article_9e4368efa2ac454e93727fafd3d8bd7a&rfr_iscdi=true |