Spatial and temporal profiles of growth factor expression during CNS demyelination reveal the dynamics of repair priming
Demyelination is the cause of disability in various neurological disorders. It is therefore crucial to understand the molecular regulation of oligodendrocytes, the myelin forming cells in the CNS. Growth factors are known to be essential for the development and maintenance of oligodendrocytes and ar...
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| Veröffentlicht in: | PloS one 2011-07, Vol.6 (7), p.e22623 |
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| creator | Gudi, Viktoria Škuljec, Jelena Yildiz, Özlem Frichert, Konstantin Skripuletz, Thomas Moharregh-Khiabani, Darius Voss, Elke Wissel, Kirsten Wolter, Sabine Stangel, Martin |
| description | Demyelination is the cause of disability in various neurological disorders. It is therefore crucial to understand the molecular regulation of oligodendrocytes, the myelin forming cells in the CNS. Growth factors are known to be essential for the development and maintenance of oligodendrocytes and are involved in the regulation of glial responses in various pathological conditions. We employed the well established murine cuprizone model of toxic demyelination to analyze the expression of 13 growth factors in the CNS during de- and remyelination. The temporal mRNA expression profile during demyelination and the subsequent remyelination were analyzed separately in the corpus callosum and cerebral cortex using laser microdissection and real-time PCR techniques. During demyelination a similar pattern of growth factor mRNA expression was observed in both areas with a strong up-regulation of NRG1 and GDNF and a slight increase of CNTF in the first week of cuprizone treatment. HGF, FGF-2, LIF, IGF-I, and TGF-ß1 were up-regulated mainly during peak demyelination. In contrast, during remyelination there were regional differences in growth factor mRNA expression levels. GDNF, CNTF, HGF, FGF-2, and BDNF were elevated in the corpus callosum but not in the cortex, suggesting tissue differences in the molecular regulation of remyelination in the white and grey matter. To clarify the cellular source we isolated microglia from the cuprizone lesions. GDNF, IGF-1, and FGF mRNA were detected in the microglial fraction with a temporal pattern corresponding to that from whole tissue PCR. In addition, immunohistochemical analysis revealed IGF-1 protein expression also in the reactive astrocytes. CNTF was located in astrocytes. This study identified seven different temporal expression patterns for growth factors in white and grey matter and demonstrated the importance of early tissue priming and exact orchestration of different steps during callosal and cortical de- and remyelination. |
| doi_str_mv | 10.1371/journal.pone.0022623 |
| format | Article |
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It is therefore crucial to understand the molecular regulation of oligodendrocytes, the myelin forming cells in the CNS. Growth factors are known to be essential for the development and maintenance of oligodendrocytes and are involved in the regulation of glial responses in various pathological conditions. We employed the well established murine cuprizone model of toxic demyelination to analyze the expression of 13 growth factors in the CNS during de- and remyelination. The temporal mRNA expression profile during demyelination and the subsequent remyelination were analyzed separately in the corpus callosum and cerebral cortex using laser microdissection and real-time PCR techniques. During demyelination a similar pattern of growth factor mRNA expression was observed in both areas with a strong up-regulation of NRG1 and GDNF and a slight increase of CNTF in the first week of cuprizone treatment. HGF, FGF-2, LIF, IGF-I, and TGF-ß1 were up-regulated mainly during peak demyelination. In contrast, during remyelination there were regional differences in growth factor mRNA expression levels. GDNF, CNTF, HGF, FGF-2, and BDNF were elevated in the corpus callosum but not in the cortex, suggesting tissue differences in the molecular regulation of remyelination in the white and grey matter. To clarify the cellular source we isolated microglia from the cuprizone lesions. GDNF, IGF-1, and FGF mRNA were detected in the microglial fraction with a temporal pattern corresponding to that from whole tissue PCR. In addition, immunohistochemical analysis revealed IGF-1 protein expression also in the reactive astrocytes. CNTF was located in astrocytes. This study identified seven different temporal expression patterns for growth factors in white and grey matter and demonstrated the importance of early tissue priming and exact orchestration of different steps during callosal and cortical de- and remyelination.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0022623</identifier><identifier>PMID: 21818353</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Animals ; Apoptosis ; Astrocytes ; Astrocytes - drug effects ; Astrocytes - metabolism ; Astrocytes - pathology ; Biology ; Brain ; Brain-derived neurotrophic factor ; Central nervous system ; Central Nervous System - drug effects ; Central Nervous System - metabolism ; Central Nervous System - pathology ; Cerebral cortex ; Cerebral Cortex - drug effects ; Cerebral Cortex - metabolism ; Cerebral Cortex - pathology ; Ciliary neurotrophic factor ; Corpus callosum ; Corpus Callosum - drug effects ; Corpus Callosum - metabolism ; Corpus Callosum - pathology ; Cortex (temporal) ; Cuprizone ; Cuprizone - administration & dosage ; Cuprizone - pharmacology ; Demyelinating Diseases - genetics ; Demyelinating Diseases - pathology ; Demyelination ; Ethanol ; Fibroblast growth factor 2 ; Fibroblast growth factors ; Fibroblasts ; Gene expression ; Gene Expression Profiling ; Gene Expression Regulation - drug effects ; Glial cell line-derived neurotrophic factor ; Growth factors ; Insulin-like growth factor I ; Insulin-like growth factors ; Intercellular Signaling Peptides and Proteins - genetics ; Intercellular Signaling Peptides and Proteins - metabolism ; Intermediate Filament Proteins - metabolism ; Laboratory animals ; Lesions ; Male ; Medical schools ; Medicine ; Mice ; Mice, Inbred C57BL ; Microglia ; Multiple sclerosis ; Myelin ; Myelination ; Nerve Tissue Proteins - metabolism ; Nervous system diseases ; Nestin ; Neurological diseases ; Neurology ; Neurosciences ; Oligodendrocytes ; Priming ; RNA ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Rodents ; Spinal cord ; Substantia grisea ; Time Factors ; Transforming growth factors ; Wound Healing - drug effects</subject><ispartof>PloS one, 2011-07, Vol.6 (7), p.e22623</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>2011 Gudi 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>Gudi et al. 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c757t-ac3bce39bb4d82f8e6cb7342b833c58e00f1f32d122f14f95a6d4f3e1124a1103</citedby><cites>FETCH-LOGICAL-c757t-ac3bce39bb4d82f8e6cb7342b833c58e00f1f32d122f14f95a6d4f3e1124a1103</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/PMC3144923/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3144923/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21818353$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gudi, Viktoria</creatorcontrib><creatorcontrib>Škuljec, Jelena</creatorcontrib><creatorcontrib>Yildiz, Özlem</creatorcontrib><creatorcontrib>Frichert, Konstantin</creatorcontrib><creatorcontrib>Skripuletz, Thomas</creatorcontrib><creatorcontrib>Moharregh-Khiabani, Darius</creatorcontrib><creatorcontrib>Voss, Elke</creatorcontrib><creatorcontrib>Wissel, Kirsten</creatorcontrib><creatorcontrib>Wolter, Sabine</creatorcontrib><creatorcontrib>Stangel, Martin</creatorcontrib><title>Spatial and temporal profiles of growth factor expression during CNS demyelination reveal the dynamics of repair priming</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Demyelination is the cause of disability in various neurological disorders. It is therefore crucial to understand the molecular regulation of oligodendrocytes, the myelin forming cells in the CNS. Growth factors are known to be essential for the development and maintenance of oligodendrocytes and are involved in the regulation of glial responses in various pathological conditions. We employed the well established murine cuprizone model of toxic demyelination to analyze the expression of 13 growth factors in the CNS during de- and remyelination. The temporal mRNA expression profile during demyelination and the subsequent remyelination were analyzed separately in the corpus callosum and cerebral cortex using laser microdissection and real-time PCR techniques. During demyelination a similar pattern of growth factor mRNA expression was observed in both areas with a strong up-regulation of NRG1 and GDNF and a slight increase of CNTF in the first week of cuprizone treatment. HGF, FGF-2, LIF, IGF-I, and TGF-ß1 were up-regulated mainly during peak demyelination. In contrast, during remyelination there were regional differences in growth factor mRNA expression levels. GDNF, CNTF, HGF, FGF-2, and BDNF were elevated in the corpus callosum but not in the cortex, suggesting tissue differences in the molecular regulation of remyelination in the white and grey matter. To clarify the cellular source we isolated microglia from the cuprizone lesions. GDNF, IGF-1, and FGF mRNA were detected in the microglial fraction with a temporal pattern corresponding to that from whole tissue PCR. In addition, immunohistochemical analysis revealed IGF-1 protein expression also in the reactive astrocytes. CNTF was located in astrocytes. This study identified seven different temporal expression patterns for growth factors in white and grey matter and demonstrated the importance of early tissue priming and exact orchestration of different steps during callosal and cortical de- and remyelination.</description><subject>Analysis</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>Astrocytes</subject><subject>Astrocytes - drug effects</subject><subject>Astrocytes - metabolism</subject><subject>Astrocytes - pathology</subject><subject>Biology</subject><subject>Brain</subject><subject>Brain-derived neurotrophic factor</subject><subject>Central nervous system</subject><subject>Central Nervous System - drug effects</subject><subject>Central Nervous System - metabolism</subject><subject>Central Nervous System - pathology</subject><subject>Cerebral cortex</subject><subject>Cerebral Cortex - drug effects</subject><subject>Cerebral Cortex - metabolism</subject><subject>Cerebral Cortex - pathology</subject><subject>Ciliary neurotrophic factor</subject><subject>Corpus callosum</subject><subject>Corpus Callosum - drug effects</subject><subject>Corpus Callosum - metabolism</subject><subject>Corpus Callosum - pathology</subject><subject>Cortex (temporal)</subject><subject>Cuprizone</subject><subject>Cuprizone - administration & dosage</subject><subject>Cuprizone - pharmacology</subject><subject>Demyelinating Diseases - genetics</subject><subject>Demyelinating Diseases - pathology</subject><subject>Demyelination</subject><subject>Ethanol</subject><subject>Fibroblast growth factor 2</subject><subject>Fibroblast growth factors</subject><subject>Fibroblasts</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation - drug effects</subject><subject>Glial cell line-derived neurotrophic factor</subject><subject>Growth factors</subject><subject>Insulin-like growth factor I</subject><subject>Insulin-like growth factors</subject><subject>Intercellular Signaling Peptides and Proteins - genetics</subject><subject>Intercellular Signaling Peptides and Proteins - 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drug effects</topic><topic>Glial cell line-derived neurotrophic factor</topic><topic>Growth factors</topic><topic>Insulin-like growth factor I</topic><topic>Insulin-like growth factors</topic><topic>Intercellular Signaling Peptides and Proteins - genetics</topic><topic>Intercellular Signaling Peptides and Proteins - metabolism</topic><topic>Intermediate Filament Proteins - metabolism</topic><topic>Laboratory animals</topic><topic>Lesions</topic><topic>Male</topic><topic>Medical schools</topic><topic>Medicine</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Microglia</topic><topic>Multiple sclerosis</topic><topic>Myelin</topic><topic>Myelination</topic><topic>Nerve Tissue Proteins - metabolism</topic><topic>Nervous system diseases</topic><topic>Nestin</topic><topic>Neurological diseases</topic><topic>Neurology</topic><topic>Neurosciences</topic><topic>Oligodendrocytes</topic><topic>Priming</topic><topic>RNA</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>Rodents</topic><topic>Spinal cord</topic><topic>Substantia grisea</topic><topic>Time Factors</topic><topic>Transforming growth factors</topic><topic>Wound Healing - drug effects</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gudi, Viktoria</creatorcontrib><creatorcontrib>Škuljec, Jelena</creatorcontrib><creatorcontrib>Yildiz, Özlem</creatorcontrib><creatorcontrib>Frichert, Konstantin</creatorcontrib><creatorcontrib>Skripuletz, Thomas</creatorcontrib><creatorcontrib>Moharregh-Khiabani, Darius</creatorcontrib><creatorcontrib>Voss, Elke</creatorcontrib><creatorcontrib>Wissel, Kirsten</creatorcontrib><creatorcontrib>Wolter, Sabine</creatorcontrib><creatorcontrib>Stangel, Martin</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</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>Gudi, Viktoria</au><au>Škuljec, Jelena</au><au>Yildiz, Özlem</au><au>Frichert, Konstantin</au><au>Skripuletz, Thomas</au><au>Moharregh-Khiabani, Darius</au><au>Voss, Elke</au><au>Wissel, Kirsten</au><au>Wolter, Sabine</au><au>Stangel, Martin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Spatial and temporal profiles of growth factor expression during CNS demyelination reveal the dynamics of repair priming</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2011-07-27</date><risdate>2011</risdate><volume>6</volume><issue>7</issue><spage>e22623</spage><pages>e22623-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Demyelination is the cause of disability in various neurological disorders. It is therefore crucial to understand the molecular regulation of oligodendrocytes, the myelin forming cells in the CNS. Growth factors are known to be essential for the development and maintenance of oligodendrocytes and are involved in the regulation of glial responses in various pathological conditions. We employed the well established murine cuprizone model of toxic demyelination to analyze the expression of 13 growth factors in the CNS during de- and remyelination. The temporal mRNA expression profile during demyelination and the subsequent remyelination were analyzed separately in the corpus callosum and cerebral cortex using laser microdissection and real-time PCR techniques. During demyelination a similar pattern of growth factor mRNA expression was observed in both areas with a strong up-regulation of NRG1 and GDNF and a slight increase of CNTF in the first week of cuprizone treatment. HGF, FGF-2, LIF, IGF-I, and TGF-ß1 were up-regulated mainly during peak demyelination. In contrast, during remyelination there were regional differences in growth factor mRNA expression levels. GDNF, CNTF, HGF, FGF-2, and BDNF were elevated in the corpus callosum but not in the cortex, suggesting tissue differences in the molecular regulation of remyelination in the white and grey matter. To clarify the cellular source we isolated microglia from the cuprizone lesions. GDNF, IGF-1, and FGF mRNA were detected in the microglial fraction with a temporal pattern corresponding to that from whole tissue PCR. In addition, immunohistochemical analysis revealed IGF-1 protein expression also in the reactive astrocytes. CNTF was located in astrocytes. This study identified seven different temporal expression patterns for growth factors in white and grey matter and demonstrated the importance of early tissue priming and exact orchestration of different steps during callosal and cortical de- and remyelination.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21818353</pmid><doi>10.1371/journal.pone.0022623</doi><tpages>e22623</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2011-07, Vol.6 (7), p.e22623 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1306216179 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Analysis Animals Apoptosis Astrocytes Astrocytes - drug effects Astrocytes - metabolism Astrocytes - pathology Biology Brain Brain-derived neurotrophic factor Central nervous system Central Nervous System - drug effects Central Nervous System - metabolism Central Nervous System - pathology Cerebral cortex Cerebral Cortex - drug effects Cerebral Cortex - metabolism Cerebral Cortex - pathology Ciliary neurotrophic factor Corpus callosum Corpus Callosum - drug effects Corpus Callosum - metabolism Corpus Callosum - pathology Cortex (temporal) Cuprizone Cuprizone - administration & dosage Cuprizone - pharmacology Demyelinating Diseases - genetics Demyelinating Diseases - pathology Demyelination Ethanol Fibroblast growth factor 2 Fibroblast growth factors Fibroblasts Gene expression Gene Expression Profiling Gene Expression Regulation - drug effects Glial cell line-derived neurotrophic factor Growth factors Insulin-like growth factor I Insulin-like growth factors Intercellular Signaling Peptides and Proteins - genetics Intercellular Signaling Peptides and Proteins - metabolism Intermediate Filament Proteins - metabolism Laboratory animals Lesions Male Medical schools Medicine Mice Mice, Inbred C57BL Microglia Multiple sclerosis Myelin Myelination Nerve Tissue Proteins - metabolism Nervous system diseases Nestin Neurological diseases Neurology Neurosciences Oligodendrocytes Priming RNA RNA, Messenger - genetics RNA, Messenger - metabolism Rodents Spinal cord Substantia grisea Time Factors Transforming growth factors Wound Healing - drug effects |
| title | Spatial and temporal profiles of growth factor expression during CNS demyelination reveal the dynamics of repair priming |
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