Clinical relevance of tumor cells with stem-like properties in pediatric brain tumors.
<h4>Background</h4>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 com...
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2011
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oai:doaj.org-article:f701510a0d5548259cc87a1a8a01b4402021-11-18T06:59:38ZClinical relevance of tumor cells with stem-like properties in pediatric brain tumors.1932-620310.1371/journal.pone.0016375https://doaj.org/article/f701510a0d5548259cc87a1a8a01b4402011-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21297991/?tool=EBIhttps://doaj.org/toc/1932-6203<h4>Background</h4>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.<h4>Methodology/principal findings</h4>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.<h4>Conclusions/significance</h4>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.Cécile ThirantBarbara BessettePascale VarletStéphanie PugetJosette CadusseauSilvina Dos Reis TavaresJeanne-Marie StudlerDavid Carlos SilvestreAurélie SusiniChiara VillaCatherine MiquelAlexandra BogeasAnne-Laure SurenaAmélia Dias-MoraisNadine LéonardFrançoise PflumioIvan BiècheFrançois D BoussinChristian Sainte-RoseJacques GrillCatherine Daumas-DuportHervé ChneiweissMarie-Pierre JunierPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 6, Iss 1, p e16375 (2011) |
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Medicine R Science Q Cécile Thirant Barbara Bessette Pascale Varlet Stéphanie Puget Josette Cadusseau Silvina Dos Reis Tavares Jeanne-Marie Studler David Carlos Silvestre Aurélie Susini Chiara Villa Catherine Miquel Alexandra Bogeas Anne-Laure Surena Amélia Dias-Morais Nadine Léonard Françoise Pflumio Ivan Bièche François D Boussin Christian Sainte-Rose Jacques Grill Catherine Daumas-Duport Hervé Chneiweiss Marie-Pierre Junier Clinical relevance of tumor cells with stem-like properties in pediatric brain tumors. |
| description |
<h4>Background</h4>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.<h4>Methodology/principal findings</h4>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.<h4>Conclusions/significance</h4>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. |
| format |
article |
| author |
Cécile Thirant Barbara Bessette Pascale Varlet Stéphanie Puget Josette Cadusseau Silvina Dos Reis Tavares Jeanne-Marie Studler David Carlos Silvestre Aurélie Susini Chiara Villa Catherine Miquel Alexandra Bogeas Anne-Laure Surena Amélia Dias-Morais Nadine Léonard Françoise Pflumio Ivan Bièche François D Boussin Christian Sainte-Rose Jacques Grill Catherine Daumas-Duport Hervé Chneiweiss Marie-Pierre Junier |
| author_facet |
Cécile Thirant Barbara Bessette Pascale Varlet Stéphanie Puget Josette Cadusseau Silvina Dos Reis Tavares Jeanne-Marie Studler David Carlos Silvestre Aurélie Susini Chiara Villa Catherine Miquel Alexandra Bogeas Anne-Laure Surena Amélia Dias-Morais Nadine Léonard Françoise Pflumio Ivan Bièche François D Boussin Christian Sainte-Rose Jacques Grill Catherine Daumas-Duport Hervé Chneiweiss Marie-Pierre Junier |
| author_sort |
Cécile Thirant |
| title |
Clinical relevance of tumor cells with stem-like properties in pediatric brain tumors. |
| title_short |
Clinical relevance of tumor cells with stem-like properties in pediatric brain tumors. |
| title_full |
Clinical relevance of tumor cells with stem-like properties in pediatric brain tumors. |
| title_fullStr |
Clinical relevance of tumor cells with stem-like properties in pediatric brain tumors. |
| title_full_unstemmed |
Clinical relevance of tumor cells with stem-like properties in pediatric brain tumors. |
| title_sort |
clinical relevance of tumor cells with stem-like properties in pediatric brain tumors. |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2011 |
| url |
https://doaj.org/article/f701510a0d5548259cc87a1a8a01b440 |
| work_keys_str_mv |
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