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Intratumoral heterogeneity of endogenous tumor cell invasive behavior in human glioblastoma

Intratumoral genetic heterogeneity is a widely accepted characteristic of human cancer, including the most common primary malignant brain tumor, glioblastoma. However, the variability in biological behaviors amongst cells within individual tumors is not well described. Invasion into unaffected brain...

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Autores principales: Parker, Jonathon J., Canoll, Peter, Niswander, Lee, Kleinschmidt-DeMasters, B. K., Foshay, Kara, Waziri, Allen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6301947/
https://www.ncbi.nlm.nih.gov/pubmed/30573757
http://dx.doi.org/10.1038/s41598-018-36280-9
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author Parker, Jonathon J.
Canoll, Peter
Niswander, Lee
Kleinschmidt-DeMasters, B. K.
Foshay, Kara
Waziri, Allen
author_facet Parker, Jonathon J.
Canoll, Peter
Niswander, Lee
Kleinschmidt-DeMasters, B. K.
Foshay, Kara
Waziri, Allen
author_sort Parker, Jonathon J.
collection PubMed
description Intratumoral genetic heterogeneity is a widely accepted characteristic of human cancer, including the most common primary malignant brain tumor, glioblastoma. However, the variability in biological behaviors amongst cells within individual tumors is not well described. Invasion into unaffected brain parenchyma is one such behavior, and a leading mechanism of tumor recurrence unaddressed by the current therapeutic armamentarium. Further, providing insight into variability of tumor cell migration within individual tumors may inform discovery of novel anti-invasive therapeutics. In this study, ex vivo organotypic slice cultures from EGFR-wild type and EGFR-amplified patient tumors were treated with the EGFR inhibitor gefitinib to evaluate potential sub-population restricted intratumoral drug-specific responses. High-resolution time-lapse microscopy and quantitative path tracking demonstrated migration of individual cells are punctuated by intermittent bursts of movement. Elevation of population aggregate mean speeds were driven by subpopulations of cells exhibiting frequent high-amplitude bursts, enriched within EGFR-amplified tumors. Treatment with gefitinib specifically targeted high-burst cell subpopulations only in EGFR-amplified tumors, decreasing bursting frequency and amplitude. We provide evidence of intratumoral subpopulations of cells with enhanced migratory behavior in human glioblastoma, selectively targeted via EGFR inhibition. These data justify use of direct human tumor slice cultures to investigate patient-specific therapies designed to limit tumor invasion.
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spelling pubmed-63019472018-12-26 Intratumoral heterogeneity of endogenous tumor cell invasive behavior in human glioblastoma Parker, Jonathon J. Canoll, Peter Niswander, Lee Kleinschmidt-DeMasters, B. K. Foshay, Kara Waziri, Allen Sci Rep Article Intratumoral genetic heterogeneity is a widely accepted characteristic of human cancer, including the most common primary malignant brain tumor, glioblastoma. However, the variability in biological behaviors amongst cells within individual tumors is not well described. Invasion into unaffected brain parenchyma is one such behavior, and a leading mechanism of tumor recurrence unaddressed by the current therapeutic armamentarium. Further, providing insight into variability of tumor cell migration within individual tumors may inform discovery of novel anti-invasive therapeutics. In this study, ex vivo organotypic slice cultures from EGFR-wild type and EGFR-amplified patient tumors were treated with the EGFR inhibitor gefitinib to evaluate potential sub-population restricted intratumoral drug-specific responses. High-resolution time-lapse microscopy and quantitative path tracking demonstrated migration of individual cells are punctuated by intermittent bursts of movement. Elevation of population aggregate mean speeds were driven by subpopulations of cells exhibiting frequent high-amplitude bursts, enriched within EGFR-amplified tumors. Treatment with gefitinib specifically targeted high-burst cell subpopulations only in EGFR-amplified tumors, decreasing bursting frequency and amplitude. We provide evidence of intratumoral subpopulations of cells with enhanced migratory behavior in human glioblastoma, selectively targeted via EGFR inhibition. These data justify use of direct human tumor slice cultures to investigate patient-specific therapies designed to limit tumor invasion. Nature Publishing Group UK 2018-12-20 /pmc/articles/PMC6301947/ /pubmed/30573757 http://dx.doi.org/10.1038/s41598-018-36280-9 Text en © The Author(s) 2018 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Parker, Jonathon J.
Canoll, Peter
Niswander, Lee
Kleinschmidt-DeMasters, B. K.
Foshay, Kara
Waziri, Allen
Intratumoral heterogeneity of endogenous tumor cell invasive behavior in human glioblastoma
title Intratumoral heterogeneity of endogenous tumor cell invasive behavior in human glioblastoma
title_full Intratumoral heterogeneity of endogenous tumor cell invasive behavior in human glioblastoma
title_fullStr Intratumoral heterogeneity of endogenous tumor cell invasive behavior in human glioblastoma
title_full_unstemmed Intratumoral heterogeneity of endogenous tumor cell invasive behavior in human glioblastoma
title_short Intratumoral heterogeneity of endogenous tumor cell invasive behavior in human glioblastoma
title_sort intratumoral heterogeneity of endogenous tumor cell invasive behavior in human glioblastoma
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6301947/
https://www.ncbi.nlm.nih.gov/pubmed/30573757
http://dx.doi.org/10.1038/s41598-018-36280-9
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