Differential Gene Expression Profiling of Dystrophic Dog Muscle after MuStem Cell Transplantation
Several adult stem cell populations exhibit myogenic regenerative potential, thus representing attractive candidates for therapeutic approaches of neuromuscular diseases such as Duchenne Muscular Dystrophy (DMD). We have recently shown that systemic delivery of MuStem cells, skeletal muscle-resident...
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| creator | Robriquet, Florence Lardenois, Aurélie Babarit, Candice Larcher, Thibaut Dubreil, Laurence Leroux, Isabelle Zuber, Céline Ledevin, Mireille Deschamps, Jack-Yves Fromes, Yves Cherel, Yan Guevel, Laetitia Rouger, Karl |
| description | Several adult stem cell populations exhibit myogenic regenerative potential, thus representing attractive candidates for therapeutic approaches of neuromuscular diseases such as Duchenne Muscular Dystrophy (DMD). We have recently shown that systemic delivery of MuStem cells, skeletal muscle-resident stem cells isolated in healthy dog, generates the remodelling of muscle tissue and gives rise to striking clinical benefits in Golden Retriever Muscular Dystrophy (GRMD) dog. This global effect, which is observed in the clinically relevant DMD animal model, leads us to question here the molecular pathways that are impacted by MuStem cell transplantation. To address this issue, we compare the global gene expression profile between healthy, GRMD and MuStem cell treated GRMD dog muscle, four months after allogenic MuStem cell transplantation.
In the dystrophic context of the GRMD dog, disease-related deregulation is observed in the case of 282 genes related to various processes such as inflammatory response, regeneration, calcium ion binding, extracellular matrix organization, metabolism and apoptosis regulation. Importantly, we reveal the impact of MuStem cell transplantation on several molecular and cellular pathways based on a selection of 31 genes displaying signals specifically modulated by the treatment. Concomitant with a diffuse dystrophin expression, a histological remodelling and a stabilization of GRMD dog clinical status, we show that cell delivery is associated with an up-regulation of genes reflecting a sustained enhancement of muscle regeneration. We also identify a decreased mRNA expression of a set of genes having metabolic functions associated with lipid homeostasis and energy. Interestingly, ubiquitin-mediated protein degradation is highly enhanced in GRMD dog muscle after systemic delivery of MuStem cells.
Overall, our results provide the first high-throughput characterization of GRMD dog muscle and throw new light on the complex molecular/cellular effects associated with muscle repair and the clinical efficacy of MuStem cell-based therapy. |
| doi_str_mv | 10.1371/journal.pone.0123336 |
| format | Article |
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In the dystrophic context of the GRMD dog, disease-related deregulation is observed in the case of 282 genes related to various processes such as inflammatory response, regeneration, calcium ion binding, extracellular matrix organization, metabolism and apoptosis regulation. Importantly, we reveal the impact of MuStem cell transplantation on several molecular and cellular pathways based on a selection of 31 genes displaying signals specifically modulated by the treatment. Concomitant with a diffuse dystrophin expression, a histological remodelling and a stabilization of GRMD dog clinical status, we show that cell delivery is associated with an up-regulation of genes reflecting a sustained enhancement of muscle regeneration. We also identify a decreased mRNA expression of a set of genes having metabolic functions associated with lipid homeostasis and energy. Interestingly, ubiquitin-mediated protein degradation is highly enhanced in GRMD dog muscle after systemic delivery of MuStem cells.
Overall, our results provide the first high-throughput characterization of GRMD dog muscle and throw new light on the complex molecular/cellular effects associated with muscle repair and the clinical efficacy of MuStem cell-based therapy.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0123336</identifier><identifier>PMID: 25955839</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Animals ; Apoptosis ; Autophagy ; Calcium ; Calcium (extracellular) ; Deregulation ; Diabetes ; Disease Models, Animal ; Dogs ; Duchenne's muscular dystrophy ; Dystrophin ; Dystrophy ; Extracellular matrix ; Follow-Up Studies ; Gangrene ; Gene expression ; Gene Expression Profiling ; Gene regulation ; Genes ; Genomics ; Health aspects ; Homeostasis ; Human health and pathology ; Humans ; Inflammation ; Inflammatory response ; Insulin ; Life Sciences ; Metabolism ; Muscle, Skeletal - metabolism ; Muscle, Skeletal - pathology ; Muscles ; Muscular dystrophy ; Muscular Dystrophy, Animal - genetics ; Muscular Dystrophy, Animal - therapy ; Musculoskeletal system ; Neuromuscular diseases ; Oligonucleotide Array Sequence Analysis ; Proteolysis ; Quality Control ; Real-Time Polymerase Chain Reaction ; Regeneration ; Reproducibility of Results ; RNA ; Rodents ; Skeletal muscle ; Stem Cell Transplantation ; Stem cells ; Studies ; Transplantation ; Ubiquitin ; Utrophin</subject><ispartof>PloS one, 2015-05, Vol.10 (5), p.e0123336-e0123336</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Robriquet 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>Attribution</rights><rights>2015 Robriquet et al 2015 Robriquet et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c726t-e7e3fcc4729d68ee4377dad2b2f5f7c7b97bfb9d9dedf5158016e6d35ad1b9953</citedby><cites>FETCH-LOGICAL-c726t-e7e3fcc4729d68ee4377dad2b2f5f7c7b97bfb9d9dedf5158016e6d35ad1b9953</cites><orcidid>0000-0002-4892-0426 ; 0000-0002-0396-3190 ; 0000-0003-3363-7457</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4425432/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4425432/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79569,79570</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25955839$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01222898$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Robriquet, Florence</creatorcontrib><creatorcontrib>Lardenois, Aurélie</creatorcontrib><creatorcontrib>Babarit, Candice</creatorcontrib><creatorcontrib>Larcher, Thibaut</creatorcontrib><creatorcontrib>Dubreil, Laurence</creatorcontrib><creatorcontrib>Leroux, Isabelle</creatorcontrib><creatorcontrib>Zuber, Céline</creatorcontrib><creatorcontrib>Ledevin, Mireille</creatorcontrib><creatorcontrib>Deschamps, Jack-Yves</creatorcontrib><creatorcontrib>Fromes, Yves</creatorcontrib><creatorcontrib>Cherel, Yan</creatorcontrib><creatorcontrib>Guevel, Laetitia</creatorcontrib><creatorcontrib>Rouger, Karl</creatorcontrib><title>Differential Gene Expression Profiling of Dystrophic Dog Muscle after MuStem Cell Transplantation</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Several adult stem cell populations exhibit myogenic regenerative potential, thus representing attractive candidates for therapeutic approaches of neuromuscular diseases such as Duchenne Muscular Dystrophy (DMD). We have recently shown that systemic delivery of MuStem cells, skeletal muscle-resident stem cells isolated in healthy dog, generates the remodelling of muscle tissue and gives rise to striking clinical benefits in Golden Retriever Muscular Dystrophy (GRMD) dog. This global effect, which is observed in the clinically relevant DMD animal model, leads us to question here the molecular pathways that are impacted by MuStem cell transplantation. To address this issue, we compare the global gene expression profile between healthy, GRMD and MuStem cell treated GRMD dog muscle, four months after allogenic MuStem cell transplantation.
In the dystrophic context of the GRMD dog, disease-related deregulation is observed in the case of 282 genes related to various processes such as inflammatory response, regeneration, calcium ion binding, extracellular matrix organization, metabolism and apoptosis regulation. Importantly, we reveal the impact of MuStem cell transplantation on several molecular and cellular pathways based on a selection of 31 genes displaying signals specifically modulated by the treatment. Concomitant with a diffuse dystrophin expression, a histological remodelling and a stabilization of GRMD dog clinical status, we show that cell delivery is associated with an up-regulation of genes reflecting a sustained enhancement of muscle regeneration. We also identify a decreased mRNA expression of a set of genes having metabolic functions associated with lipid homeostasis and energy. Interestingly, ubiquitin-mediated protein degradation is highly enhanced in GRMD dog muscle after systemic delivery of MuStem cells.
Overall, our results provide the first high-throughput characterization of GRMD dog muscle and throw new light on the complex molecular/cellular effects associated with muscle repair and the clinical efficacy of MuStem cell-based therapy.</description><subject>Analysis</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>Autophagy</subject><subject>Calcium</subject><subject>Calcium (extracellular)</subject><subject>Deregulation</subject><subject>Diabetes</subject><subject>Disease Models, Animal</subject><subject>Dogs</subject><subject>Duchenne's muscular dystrophy</subject><subject>Dystrophin</subject><subject>Dystrophy</subject><subject>Extracellular matrix</subject><subject>Follow-Up Studies</subject><subject>Gangrene</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene regulation</subject><subject>Genes</subject><subject>Genomics</subject><subject>Health aspects</subject><subject>Homeostasis</subject><subject>Human health and pathology</subject><subject>Humans</subject><subject>Inflammation</subject><subject>Inflammatory response</subject><subject>Insulin</subject><subject>Life Sciences</subject><subject>Metabolism</subject><subject>Muscle, Skeletal - metabolism</subject><subject>Muscle, Skeletal - pathology</subject><subject>Muscles</subject><subject>Muscular dystrophy</subject><subject>Muscular Dystrophy, Animal - genetics</subject><subject>Muscular Dystrophy, Animal - therapy</subject><subject>Musculoskeletal system</subject><subject>Neuromuscular diseases</subject><subject>Oligonucleotide Array Sequence Analysis</subject><subject>Proteolysis</subject><subject>Quality Control</subject><subject>Real-Time Polymerase Chain Reaction</subject><subject>Regeneration</subject><subject>Reproducibility of Results</subject><subject>RNA</subject><subject>Rodents</subject><subject>Skeletal muscle</subject><subject>Stem Cell Transplantation</subject><subject>Stem 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Aurélie</au><au>Babarit, Candice</au><au>Larcher, Thibaut</au><au>Dubreil, Laurence</au><au>Leroux, Isabelle</au><au>Zuber, Céline</au><au>Ledevin, Mireille</au><au>Deschamps, Jack-Yves</au><au>Fromes, Yves</au><au>Cherel, Yan</au><au>Guevel, Laetitia</au><au>Rouger, Karl</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Differential Gene Expression Profiling of Dystrophic Dog Muscle after MuStem Cell Transplantation</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-05-08</date><risdate>2015</risdate><volume>10</volume><issue>5</issue><spage>e0123336</spage><epage>e0123336</epage><pages>e0123336-e0123336</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Several adult stem cell populations exhibit myogenic regenerative potential, thus representing attractive candidates for therapeutic approaches of neuromuscular diseases such as Duchenne Muscular Dystrophy (DMD). We have recently shown that systemic delivery of MuStem cells, skeletal muscle-resident stem cells isolated in healthy dog, generates the remodelling of muscle tissue and gives rise to striking clinical benefits in Golden Retriever Muscular Dystrophy (GRMD) dog. This global effect, which is observed in the clinically relevant DMD animal model, leads us to question here the molecular pathways that are impacted by MuStem cell transplantation. To address this issue, we compare the global gene expression profile between healthy, GRMD and MuStem cell treated GRMD dog muscle, four months after allogenic MuStem cell transplantation.
In the dystrophic context of the GRMD dog, disease-related deregulation is observed in the case of 282 genes related to various processes such as inflammatory response, regeneration, calcium ion binding, extracellular matrix organization, metabolism and apoptosis regulation. Importantly, we reveal the impact of MuStem cell transplantation on several molecular and cellular pathways based on a selection of 31 genes displaying signals specifically modulated by the treatment. Concomitant with a diffuse dystrophin expression, a histological remodelling and a stabilization of GRMD dog clinical status, we show that cell delivery is associated with an up-regulation of genes reflecting a sustained enhancement of muscle regeneration. We also identify a decreased mRNA expression of a set of genes having metabolic functions associated with lipid homeostasis and energy. Interestingly, ubiquitin-mediated protein degradation is highly enhanced in GRMD dog muscle after systemic delivery of MuStem cells.
Overall, our results provide the first high-throughput characterization of GRMD dog muscle and throw new light on the complex molecular/cellular effects associated with muscle repair and the clinical efficacy of MuStem cell-based therapy.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25955839</pmid><doi>10.1371/journal.pone.0123336</doi><orcidid>https://orcid.org/0000-0002-4892-0426</orcidid><orcidid>https://orcid.org/0000-0002-0396-3190</orcidid><orcidid>https://orcid.org/0000-0003-3363-7457</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2015-05, Vol.10 (5), p.e0123336-e0123336 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1982585756 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Analysis Animals Apoptosis Autophagy Calcium Calcium (extracellular) Deregulation Diabetes Disease Models, Animal Dogs Duchenne's muscular dystrophy Dystrophin Dystrophy Extracellular matrix Follow-Up Studies Gangrene Gene expression Gene Expression Profiling Gene regulation Genes Genomics Health aspects Homeostasis Human health and pathology Humans Inflammation Inflammatory response Insulin Life Sciences Metabolism Muscle, Skeletal - metabolism Muscle, Skeletal - pathology Muscles Muscular dystrophy Muscular Dystrophy, Animal - genetics Muscular Dystrophy, Animal - therapy Musculoskeletal system Neuromuscular diseases Oligonucleotide Array Sequence Analysis Proteolysis Quality Control Real-Time Polymerase Chain Reaction Regeneration Reproducibility of Results RNA Rodents Skeletal muscle Stem Cell Transplantation Stem cells Studies Transplantation Ubiquitin Utrophin |
| title | Differential Gene Expression Profiling of Dystrophic Dog Muscle after MuStem Cell Transplantation |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-13T17%3A44%3A11IST&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=Differential%20Gene%20Expression%20Profiling%20of%20Dystrophic%20Dog%20Muscle%20after%20MuStem%20Cell%20Transplantation&rft.jtitle=PloS%20one&rft.au=Robriquet,%20Florence&rft.date=2015-05-08&rft.volume=10&rft.issue=5&rft.spage=e0123336&rft.epage=e0123336&rft.pages=e0123336-e0123336&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0123336&rft_dat=%3Cgale_plos_%3EA413203725%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=1982585756&rft_id=info:pmid/25955839&rft_galeid=A413203725&rft_doaj_id=oai_doaj_org_article_326afcc66b9241d0aa7718770ea0975c&rfr_iscdi=true |