Reduction in subventricular zone-derived olfactory bulb neurogenesis in a rat model of Huntington's disease is accompanied by striatal invasion of neuroblasts
Huntington's disease (HD) is an inherited progressive neurodegenerative disorder caused by an expanded CAG repeat in exon 1 of the huntingtin gene (HTT). The primary neuropathology of HD has been attributed to the preferential degeneration of medium spiny neurons (MSN) in the striatum. Reports...
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| creator | Kandasamy, Mahesh Rosskopf, Michael Wagner, Katrin Klein, Barbara Couillard-Despres, Sebastien Reitsamer, Herbert A Stephan, Michael Nguyen, Huu Phuc Riess, Olaf Bogdahn, Ulrich Winkler, Jürgen von Hörsten, Stephan Aigner, Ludwig |
| description | Huntington's disease (HD) is an inherited progressive neurodegenerative disorder caused by an expanded CAG repeat in exon 1 of the huntingtin gene (HTT). The primary neuropathology of HD has been attributed to the preferential degeneration of medium spiny neurons (MSN) in the striatum. Reports on striatal neurogenesis have been a subject of debate; nevertheless, it should be considered as an endogenous attempt to repair the brain. The subventricular zone (SVZ) might offer a close-by region to supply the degenerated striatum with new cells. Previously, we have demonstrated that R6/2 mice, a widely used preclinical model representing an early onset HD, showed reduced olfactory bulb (OB) neurogenesis but induced striatal migration of neuroblasts without affecting the proliferation of neural progenitor cell (NPCs) in the SVZ. The present study revisits these findings, using a clinically more relevant transgenic rat model of late onset HD (tgHD rats) carrying the human HTT gene with 51 CAG repeats and mimicking many of the neuropathological features of HD seen in patients. We demonstrate that cell proliferation is reduced in the SVZ and OB of tgHD rats compared to WT rats. In the OB of tgHD rats, although cell survival was reduced, the frequency of neuronal differentiation was not altered in the granule cell layer (GCL) compared to the WT rats. However, an increased frequency of dopamenergic neuronal differentiation was noticed in the glomerular layer (GLOM) of tgHD rats. Besides this, we observed a selective proliferation of neuroblasts in the adjacent striatum of tgHD rats. There was no evidence for neuronal maturation and survival of these striatal neuroblasts. Therefore, the functional role of these invading neuroblasts still needs to be determined, but they might offer an endogenous alternative for stem or neuronal cell transplantation strategies. |
| doi_str_mv | 10.1371/journal.pone.0116069 |
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The primary neuropathology of HD has been attributed to the preferential degeneration of medium spiny neurons (MSN) in the striatum. Reports on striatal neurogenesis have been a subject of debate; nevertheless, it should be considered as an endogenous attempt to repair the brain. The subventricular zone (SVZ) might offer a close-by region to supply the degenerated striatum with new cells. Previously, we have demonstrated that R6/2 mice, a widely used preclinical model representing an early onset HD, showed reduced olfactory bulb (OB) neurogenesis but induced striatal migration of neuroblasts without affecting the proliferation of neural progenitor cell (NPCs) in the SVZ. The present study revisits these findings, using a clinically more relevant transgenic rat model of late onset HD (tgHD rats) carrying the human HTT gene with 51 CAG repeats and mimicking many of the neuropathological features of HD seen in patients. We demonstrate that cell proliferation is reduced in the SVZ and OB of tgHD rats compared to WT rats. In the OB of tgHD rats, although cell survival was reduced, the frequency of neuronal differentiation was not altered in the granule cell layer (GCL) compared to the WT rats. However, an increased frequency of dopamenergic neuronal differentiation was noticed in the glomerular layer (GLOM) of tgHD rats. Besides this, we observed a selective proliferation of neuroblasts in the adjacent striatum of tgHD rats. There was no evidence for neuronal maturation and survival of these striatal neuroblasts. Therefore, the functional role of these invading neuroblasts still needs to be determined, but they might offer an endogenous alternative for stem or neuronal cell transplantation strategies.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0116069</identifier><identifier>PMID: 25719447</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animal cognition ; Animals ; Behavior disorders ; Brain ; Cell Movement ; Cell proliferation ; Cell survival ; Corpus Striatum - pathology ; Degeneration ; Differentiation ; Dopaminergic Neurons - cytology ; Dopaminergic Neurons - physiology ; Gene expression ; Genetic engineering ; Humans ; Huntingtin ; Huntingtin Protein ; Huntington Disease - genetics ; Huntington Disease - pathology ; Huntington's disease ; Huntingtons disease ; Lateral Ventricles - pathology ; Male ; Medicine ; Mimicry ; Neostriatum ; Nerve Tissue Proteins - genetics ; Neural Stem Cells - cytology ; Neural Stem Cells - physiology ; Neuroblasts ; Neurodegeneration ; Neurodegenerative diseases ; Neurogenesis ; Neurology ; Neurons ; Neurosciences ; Olfactory bulb ; Olfactory Bulb - pathology ; Polyglutamine ; Progenitor cells ; Proteins ; Quantitative analysis ; Rats ; Rodents ; Spinal cord injuries ; Spiny neurons ; Subventricular zone ; Survival ; Tissue engineering ; Transplantation ; Trinucleotide repeat diseases ; Trinucleotide repeats</subject><ispartof>PloS one, 2015-02, Vol.10 (2), p.e0116069-e0116069</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Kandasamy et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://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>2015 Kandasamy et al 2015 Kandasamy et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-67b11a639118e767a69cd06c6d73fad4a6f4af42873b0b0a7c68f0f5fc4c04f93</citedby><cites>FETCH-LOGICAL-c692t-67b11a639118e767a69cd06c6d73fad4a6f4af42873b0b0a7c68f0f5fc4c04f93</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/PMC4342015/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4342015/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25719447$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kandasamy, Mahesh</creatorcontrib><creatorcontrib>Rosskopf, Michael</creatorcontrib><creatorcontrib>Wagner, Katrin</creatorcontrib><creatorcontrib>Klein, Barbara</creatorcontrib><creatorcontrib>Couillard-Despres, Sebastien</creatorcontrib><creatorcontrib>Reitsamer, Herbert A</creatorcontrib><creatorcontrib>Stephan, Michael</creatorcontrib><creatorcontrib>Nguyen, Huu Phuc</creatorcontrib><creatorcontrib>Riess, Olaf</creatorcontrib><creatorcontrib>Bogdahn, Ulrich</creatorcontrib><creatorcontrib>Winkler, Jürgen</creatorcontrib><creatorcontrib>von Hörsten, Stephan</creatorcontrib><creatorcontrib>Aigner, Ludwig</creatorcontrib><title>Reduction in subventricular zone-derived olfactory bulb neurogenesis in a rat model of Huntington's disease is accompanied by striatal invasion of neuroblasts</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Huntington's disease (HD) is an inherited progressive neurodegenerative disorder caused by an expanded CAG repeat in exon 1 of the huntingtin gene (HTT). The primary neuropathology of HD has been attributed to the preferential degeneration of medium spiny neurons (MSN) in the striatum. Reports on striatal neurogenesis have been a subject of debate; nevertheless, it should be considered as an endogenous attempt to repair the brain. The subventricular zone (SVZ) might offer a close-by region to supply the degenerated striatum with new cells. Previously, we have demonstrated that R6/2 mice, a widely used preclinical model representing an early onset HD, showed reduced olfactory bulb (OB) neurogenesis but induced striatal migration of neuroblasts without affecting the proliferation of neural progenitor cell (NPCs) in the SVZ. The present study revisits these findings, using a clinically more relevant transgenic rat model of late onset HD (tgHD rats) carrying the human HTT gene with 51 CAG repeats and mimicking many of the neuropathological features of HD seen in patients. We demonstrate that cell proliferation is reduced in the SVZ and OB of tgHD rats compared to WT rats. In the OB of tgHD rats, although cell survival was reduced, the frequency of neuronal differentiation was not altered in the granule cell layer (GCL) compared to the WT rats. However, an increased frequency of dopamenergic neuronal differentiation was noticed in the glomerular layer (GLOM) of tgHD rats. Besides this, we observed a selective proliferation of neuroblasts in the adjacent striatum of tgHD rats. There was no evidence for neuronal maturation and survival of these striatal neuroblasts. Therefore, the functional role of these invading neuroblasts still needs to be determined, but they might offer an endogenous alternative for stem or neuronal cell transplantation strategies.</description><subject>Animal cognition</subject><subject>Animals</subject><subject>Behavior disorders</subject><subject>Brain</subject><subject>Cell Movement</subject><subject>Cell proliferation</subject><subject>Cell survival</subject><subject>Corpus Striatum - pathology</subject><subject>Degeneration</subject><subject>Differentiation</subject><subject>Dopaminergic Neurons - cytology</subject><subject>Dopaminergic Neurons - physiology</subject><subject>Gene expression</subject><subject>Genetic engineering</subject><subject>Humans</subject><subject>Huntingtin</subject><subject>Huntingtin Protein</subject><subject>Huntington Disease - genetics</subject><subject>Huntington Disease - pathology</subject><subject>Huntington's disease</subject><subject>Huntingtons disease</subject><subject>Lateral Ventricles - pathology</subject><subject>Male</subject><subject>Medicine</subject><subject>Mimicry</subject><subject>Neostriatum</subject><subject>Nerve Tissue Proteins - genetics</subject><subject>Neural Stem Cells - cytology</subject><subject>Neural Stem Cells - physiology</subject><subject>Neuroblasts</subject><subject>Neurodegeneration</subject><subject>Neurodegenerative diseases</subject><subject>Neurogenesis</subject><subject>Neurology</subject><subject>Neurons</subject><subject>Neurosciences</subject><subject>Olfactory bulb</subject><subject>Olfactory Bulb - pathology</subject><subject>Polyglutamine</subject><subject>Progenitor cells</subject><subject>Proteins</subject><subject>Quantitative analysis</subject><subject>Rats</subject><subject>Rodents</subject><subject>Spinal cord injuries</subject><subject>Spiny neurons</subject><subject>Subventricular zone</subject><subject>Survival</subject><subject>Tissue engineering</subject><subject>Transplantation</subject><subject>Trinucleotide repeat diseases</subject><subject>Trinucleotide 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Michael</au><au>Wagner, Katrin</au><au>Klein, Barbara</au><au>Couillard-Despres, Sebastien</au><au>Reitsamer, Herbert A</au><au>Stephan, Michael</au><au>Nguyen, Huu Phuc</au><au>Riess, Olaf</au><au>Bogdahn, Ulrich</au><au>Winkler, Jürgen</au><au>von Hörsten, Stephan</au><au>Aigner, Ludwig</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Reduction in subventricular zone-derived olfactory bulb neurogenesis in a rat model of Huntington's disease is accompanied by striatal invasion of neuroblasts</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-02-26</date><risdate>2015</risdate><volume>10</volume><issue>2</issue><spage>e0116069</spage><epage>e0116069</epage><pages>e0116069-e0116069</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Huntington's disease (HD) is an inherited progressive neurodegenerative disorder caused by an expanded CAG repeat in exon 1 of the huntingtin gene (HTT). The primary neuropathology of HD has been attributed to the preferential degeneration of medium spiny neurons (MSN) in the striatum. Reports on striatal neurogenesis have been a subject of debate; nevertheless, it should be considered as an endogenous attempt to repair the brain. The subventricular zone (SVZ) might offer a close-by region to supply the degenerated striatum with new cells. Previously, we have demonstrated that R6/2 mice, a widely used preclinical model representing an early onset HD, showed reduced olfactory bulb (OB) neurogenesis but induced striatal migration of neuroblasts without affecting the proliferation of neural progenitor cell (NPCs) in the SVZ. The present study revisits these findings, using a clinically more relevant transgenic rat model of late onset HD (tgHD rats) carrying the human HTT gene with 51 CAG repeats and mimicking many of the neuropathological features of HD seen in patients. We demonstrate that cell proliferation is reduced in the SVZ and OB of tgHD rats compared to WT rats. In the OB of tgHD rats, although cell survival was reduced, the frequency of neuronal differentiation was not altered in the granule cell layer (GCL) compared to the WT rats. However, an increased frequency of dopamenergic neuronal differentiation was noticed in the glomerular layer (GLOM) of tgHD rats. Besides this, we observed a selective proliferation of neuroblasts in the adjacent striatum of tgHD rats. There was no evidence for neuronal maturation and survival of these striatal neuroblasts. Therefore, the functional role of these invading neuroblasts still needs to be determined, but they might offer an endogenous alternative for stem or neuronal cell transplantation strategies.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25719447</pmid><doi>10.1371/journal.pone.0116069</doi><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2015-02, Vol.10 (2), p.e0116069-e0116069 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1658702061 |
| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Animal cognition Animals Behavior disorders Brain Cell Movement Cell proliferation Cell survival Corpus Striatum - pathology Degeneration Differentiation Dopaminergic Neurons - cytology Dopaminergic Neurons - physiology Gene expression Genetic engineering Humans Huntingtin Huntingtin Protein Huntington Disease - genetics Huntington Disease - pathology Huntington's disease Huntingtons disease Lateral Ventricles - pathology Male Medicine Mimicry Neostriatum Nerve Tissue Proteins - genetics Neural Stem Cells - cytology Neural Stem Cells - physiology Neuroblasts Neurodegeneration Neurodegenerative diseases Neurogenesis Neurology Neurons Neurosciences Olfactory bulb Olfactory Bulb - pathology Polyglutamine Progenitor cells Proteins Quantitative analysis Rats Rodents Spinal cord injuries Spiny neurons Subventricular zone Survival Tissue engineering Transplantation Trinucleotide repeat diseases Trinucleotide repeats |
| title | Reduction in subventricular zone-derived olfactory bulb neurogenesis in a rat model of Huntington's disease is accompanied by striatal invasion of neuroblasts |
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