Clinical relevance of tumor cells with stem-like properties in pediatric brain tumors
Primitive brain tumors are the leading cause of cancer-related death in children. Tumor cells with stem-like properties (TSCs), thought to account for tumorigenesis and therapeutic resistance, have been isolated from high-grade gliomas in adults. Whether TSCs are a common component of pediatric brai...
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| Veröffentlicht in: | PloS one 2011-01, Vol.6 (1), p.e16375-e16375 |
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| creator | Thirant, Cécile Bessette, Barbara Varlet, Pascale Puget, Stéphanie Cadusseau, Josette Tavares, Silvina Dos Reis Studler, Jeanne-Marie Silvestre, David Carlos Susini, Aurélie Villa, Chiara Miquel, Catherine Bogeas, Alexandra Surena, Anne-Laure Dias-Morais, Amélia Léonard, Nadine Pflumio, Françoise Bièche, Ivan Boussin, François D Sainte-Rose, Christian Grill, Jacques Daumas-Duport, Catherine Chneiweiss, Hervé Junier, Marie-Pierre |
| description | Primitive brain tumors are the leading cause of cancer-related death in children. Tumor cells with stem-like properties (TSCs), thought to account for tumorigenesis and therapeutic resistance, have been isolated from high-grade gliomas in adults. Whether TSCs are a common component of pediatric brain tumors and are of clinical relevance remains to be determined.
Tumor cells with self-renewal properties were isolated with cell biology techniques from a majority of 55 pediatric brain tumors samples, regardless of their histopathologies and grades of malignancy (57% of embryonal tumors, 57% of low-grade gliomas and neuro-glial tumors, 70% of ependymomas, 91% of high-grade gliomas). Most high-grade glioma-derived oncospheres (10/12) sustained long-term self-renewal akin to neural stem cells (>7 self-renewals), whereas cells with limited renewing abilities akin to neural progenitors dominated in all other tumors. Regardless of tumor entities, the young age group was associated with self-renewal properties akin to neural stem cells (P = 0.05, chi-square test). Survival analysis of the cohort showed an association between isolation of cells with long-term self-renewal abilities and a higher patient mortality rate (P = 0.013, log-rank test). Sampling of low- and high-grade glioma cultures showed that self-renewing cells forming oncospheres shared a molecular profile comprising embryonic and neural stem cell markers. Further characterization performed on subsets of high-grade gliomas and one low-grade glioma culture showed combination of this profile with mesenchymal markers, the radio-chemoresistance of the cells and the formation of aggressive tumors after intracerebral grafting.
In brain tumors affecting adult patients, TSCs have been isolated only from high-grade gliomas. In contrast, our data show that tumor cells with stem cell-like or progenitor-like properties can be isolated from a wide range of histological sub-types and grades of pediatric brain tumors. They suggest that cellular mechanisms fueling tumor development differ between adult and pediatric brain tumors. |
| doi_str_mv | 10.1371/journal.pone.0016375 |
| format | Article |
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Tumor cells with self-renewal properties were isolated with cell biology techniques from a majority of 55 pediatric brain tumors samples, regardless of their histopathologies and grades of malignancy (57% of embryonal tumors, 57% of low-grade gliomas and neuro-glial tumors, 70% of ependymomas, 91% of high-grade gliomas). Most high-grade glioma-derived oncospheres (10/12) sustained long-term self-renewal akin to neural stem cells (>7 self-renewals), whereas cells with limited renewing abilities akin to neural progenitors dominated in all other tumors. Regardless of tumor entities, the young age group was associated with self-renewal properties akin to neural stem cells (P = 0.05, chi-square test). Survival analysis of the cohort showed an association between isolation of cells with long-term self-renewal abilities and a higher patient mortality rate (P = 0.013, log-rank test). Sampling of low- and high-grade glioma cultures showed that self-renewing cells forming oncospheres shared a molecular profile comprising embryonic and neural stem cell markers. Further characterization performed on subsets of high-grade gliomas and one low-grade glioma culture showed combination of this profile with mesenchymal markers, the radio-chemoresistance of the cells and the formation of aggressive tumors after intracerebral grafting.
In brain tumors affecting adult patients, TSCs have been isolated only from high-grade gliomas. In contrast, our data show that tumor cells with stem cell-like or progenitor-like properties can be isolated from a wide range of histological sub-types and grades of pediatric brain tumors. They suggest that cellular mechanisms fueling tumor development differ between adult and pediatric brain tumors.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0016375</identifier><identifier>PMID: 21297991</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adolescent ; Adults ; Biology ; Biomarkers ; Brain ; Brain cancer ; Brain Neoplasms - pathology ; Brain tumors ; Cancer ; Cell culture ; Cell self-renewal ; Cell Separation ; Cell survival ; Chemoresistance ; Child ; Child, Preschool ; Children ; Clinical outcomes ; Cultures ; Development and progression ; Female ; Flow Cytometry ; Gene expression ; Glioma ; Glioma - pathology ; Gliomas ; Growth factors ; Health aspects ; Humans ; Immunophenotyping ; Infant ; Male ; Malignancy ; Medicine ; Mesenchyme ; Mortality ; Neoplastic Stem Cells - pathology ; Neural Stem Cells ; Neurogenesis ; Neuronal-glial interactions ; Neuropathology ; Pediatrics ; Properties (attributes) ; Refueling ; Signal transduction ; Statistical tests ; Stem cells ; Survival Analysis ; Tumor cells ; Tumorigenesis ; Tumors</subject><ispartof>PloS one, 2011-01, Vol.6 (1), p.e16375-e16375</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>2011 Thirant 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>Thirant et al. 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c724t-6623d5cb3cebb3c2a39600f1ca94427000bf5c8b8ac0a20e55f2c94d5a09d4683</citedby><cites>FETCH-LOGICAL-c724t-6623d5cb3cebb3c2a39600f1ca94427000bf5c8b8ac0a20e55f2c94d5a09d4683</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/PMC3030582/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3030582/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,729,782,786,866,887,2106,2932,23875,27933,27934,53800,53802</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21297991$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Gullberg, Donald</contributor><creatorcontrib>Thirant, Cécile</creatorcontrib><creatorcontrib>Bessette, Barbara</creatorcontrib><creatorcontrib>Varlet, Pascale</creatorcontrib><creatorcontrib>Puget, Stéphanie</creatorcontrib><creatorcontrib>Cadusseau, Josette</creatorcontrib><creatorcontrib>Tavares, Silvina Dos Reis</creatorcontrib><creatorcontrib>Studler, Jeanne-Marie</creatorcontrib><creatorcontrib>Silvestre, David Carlos</creatorcontrib><creatorcontrib>Susini, Aurélie</creatorcontrib><creatorcontrib>Villa, Chiara</creatorcontrib><creatorcontrib>Miquel, Catherine</creatorcontrib><creatorcontrib>Bogeas, Alexandra</creatorcontrib><creatorcontrib>Surena, Anne-Laure</creatorcontrib><creatorcontrib>Dias-Morais, Amélia</creatorcontrib><creatorcontrib>Léonard, Nadine</creatorcontrib><creatorcontrib>Pflumio, Françoise</creatorcontrib><creatorcontrib>Bièche, Ivan</creatorcontrib><creatorcontrib>Boussin, François D</creatorcontrib><creatorcontrib>Sainte-Rose, Christian</creatorcontrib><creatorcontrib>Grill, Jacques</creatorcontrib><creatorcontrib>Daumas-Duport, Catherine</creatorcontrib><creatorcontrib>Chneiweiss, Hervé</creatorcontrib><creatorcontrib>Junier, Marie-Pierre</creatorcontrib><title>Clinical relevance of tumor cells with stem-like properties in pediatric brain tumors</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Primitive brain tumors are the leading cause of cancer-related death in children. Tumor cells with stem-like properties (TSCs), thought to account for tumorigenesis and therapeutic resistance, have been isolated from high-grade gliomas in adults. Whether TSCs are a common component of pediatric brain tumors and are of clinical relevance remains to be determined.
Tumor cells with self-renewal properties were isolated with cell biology techniques from a majority of 55 pediatric brain tumors samples, regardless of their histopathologies and grades of malignancy (57% of embryonal tumors, 57% of low-grade gliomas and neuro-glial tumors, 70% of ependymomas, 91% of high-grade gliomas). Most high-grade glioma-derived oncospheres (10/12) sustained long-term self-renewal akin to neural stem cells (>7 self-renewals), whereas cells with limited renewing abilities akin to neural progenitors dominated in all other tumors. Regardless of tumor entities, the young age group was associated with self-renewal properties akin to neural stem cells (P = 0.05, chi-square test). Survival analysis of the cohort showed an association between isolation of cells with long-term self-renewal abilities and a higher patient mortality rate (P = 0.013, log-rank test). Sampling of low- and high-grade glioma cultures showed that self-renewing cells forming oncospheres shared a molecular profile comprising embryonic and neural stem cell markers. Further characterization performed on subsets of high-grade gliomas and one low-grade glioma culture showed combination of this profile with mesenchymal markers, the radio-chemoresistance of the cells and the formation of aggressive tumors after intracerebral grafting.
In brain tumors affecting adult patients, TSCs have been isolated only from high-grade gliomas. In contrast, our data show that tumor cells with stem cell-like or progenitor-like properties can be isolated from a wide range of histological sub-types and grades of pediatric brain tumors. They suggest that cellular mechanisms fueling tumor development differ between adult and pediatric brain tumors.</description><subject>Adolescent</subject><subject>Adults</subject><subject>Biology</subject><subject>Biomarkers</subject><subject>Brain</subject><subject>Brain cancer</subject><subject>Brain Neoplasms - pathology</subject><subject>Brain tumors</subject><subject>Cancer</subject><subject>Cell culture</subject><subject>Cell self-renewal</subject><subject>Cell Separation</subject><subject>Cell survival</subject><subject>Chemoresistance</subject><subject>Child</subject><subject>Child, Preschool</subject><subject>Children</subject><subject>Clinical outcomes</subject><subject>Cultures</subject><subject>Development and progression</subject><subject>Female</subject><subject>Flow Cytometry</subject><subject>Gene expression</subject><subject>Glioma</subject><subject>Glioma - pathology</subject><subject>Gliomas</subject><subject>Growth factors</subject><subject>Health aspects</subject><subject>Humans</subject><subject>Immunophenotyping</subject><subject>Infant</subject><subject>Male</subject><subject>Malignancy</subject><subject>Medicine</subject><subject>Mesenchyme</subject><subject>Mortality</subject><subject>Neoplastic Stem Cells - pathology</subject><subject>Neural Stem Cells</subject><subject>Neurogenesis</subject><subject>Neuronal-glial interactions</subject><subject>Neuropathology</subject><subject>Pediatrics</subject><subject>Properties (attributes)</subject><subject>Refueling</subject><subject>Signal transduction</subject><subject>Statistical tests</subject><subject>Stem cells</subject><subject>Survival Analysis</subject><subject>Tumor 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Abstracts</collection><collection>MEDLINE - Academic</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>Thirant, Cécile</au><au>Bessette, Barbara</au><au>Varlet, Pascale</au><au>Puget, Stéphanie</au><au>Cadusseau, Josette</au><au>Tavares, Silvina Dos Reis</au><au>Studler, Jeanne-Marie</au><au>Silvestre, David Carlos</au><au>Susini, Aurélie</au><au>Villa, Chiara</au><au>Miquel, Catherine</au><au>Bogeas, Alexandra</au><au>Surena, Anne-Laure</au><au>Dias-Morais, Amélia</au><au>Léonard, Nadine</au><au>Pflumio, Françoise</au><au>Bièche, Ivan</au><au>Boussin, François D</au><au>Sainte-Rose, Christian</au><au>Grill, Jacques</au><au>Daumas-Duport, Catherine</au><au>Chneiweiss, Hervé</au><au>Junier, Marie-Pierre</au><au>Gullberg, Donald</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Clinical relevance of tumor cells with stem-like properties in pediatric brain tumors</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2011-01-28</date><risdate>2011</risdate><volume>6</volume><issue>1</issue><spage>e16375</spage><epage>e16375</epage><pages>e16375-e16375</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Primitive brain tumors are the leading cause of cancer-related death in children. Tumor cells with stem-like properties (TSCs), thought to account for tumorigenesis and therapeutic resistance, have been isolated from high-grade gliomas in adults. Whether TSCs are a common component of pediatric brain tumors and are of clinical relevance remains to be determined.
Tumor cells with self-renewal properties were isolated with cell biology techniques from a majority of 55 pediatric brain tumors samples, regardless of their histopathologies and grades of malignancy (57% of embryonal tumors, 57% of low-grade gliomas and neuro-glial tumors, 70% of ependymomas, 91% of high-grade gliomas). Most high-grade glioma-derived oncospheres (10/12) sustained long-term self-renewal akin to neural stem cells (>7 self-renewals), whereas cells with limited renewing abilities akin to neural progenitors dominated in all other tumors. Regardless of tumor entities, the young age group was associated with self-renewal properties akin to neural stem cells (P = 0.05, chi-square test). Survival analysis of the cohort showed an association between isolation of cells with long-term self-renewal abilities and a higher patient mortality rate (P = 0.013, log-rank test). Sampling of low- and high-grade glioma cultures showed that self-renewing cells forming oncospheres shared a molecular profile comprising embryonic and neural stem cell markers. Further characterization performed on subsets of high-grade gliomas and one low-grade glioma culture showed combination of this profile with mesenchymal markers, the radio-chemoresistance of the cells and the formation of aggressive tumors after intracerebral grafting.
In brain tumors affecting adult patients, TSCs have been isolated only from high-grade gliomas. In contrast, our data show that tumor cells with stem cell-like or progenitor-like properties can be isolated from a wide range of histological sub-types and grades of pediatric brain tumors. They suggest that cellular mechanisms fueling tumor development differ between adult and pediatric brain tumors.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21297991</pmid><doi>10.1371/journal.pone.0016375</doi><tpages>e16375</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2011-01, Vol.6 (1), p.e16375-e16375 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1294207472 |
| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Adolescent Adults Biology Biomarkers Brain Brain cancer Brain Neoplasms - pathology Brain tumors Cancer Cell culture Cell self-renewal Cell Separation Cell survival Chemoresistance Child Child, Preschool Children Clinical outcomes Cultures Development and progression Female Flow Cytometry Gene expression Glioma Glioma - pathology Gliomas Growth factors Health aspects Humans Immunophenotyping Infant Male Malignancy Medicine Mesenchyme Mortality Neoplastic Stem Cells - pathology Neural Stem Cells Neurogenesis Neuronal-glial interactions Neuropathology Pediatrics Properties (attributes) Refueling Signal transduction Statistical tests Stem cells Survival Analysis Tumor cells Tumorigenesis Tumors |
| title | Clinical relevance of tumor cells with stem-like properties in pediatric brain tumors |
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