Cross-species transcriptional analysis reveals conserved and host-specific neoplastic processes in mammalian glioma
Abstract Glioma is a unique neoplastic disease that develops exclusively in the central nervous system (CNS) and rarely metastasizes to other tissues. This feature strongly implicates the tumor-host CNS microenvironment in gliomagenesis and tumor progression. We investigated the differences and simi...
Main Authors: | , , , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Nature Portfolio
2018-01-01
|
Series: | Scientific Reports |
Online Access: | https://doi.org/10.1038/s41598-018-19451-6 |
_version_ | 1818345602161836032 |
---|---|
author | Nina P. Connolly Amol C. Shetty Jesse A. Stokum Ina Hoeschele Marni B. Siegel C. Ryan Miller Anthony J. Kim Cheng-Ying Ho Eduardo Davila J. Marc Simard Scott E. Devine John H. Rossmeisl Eric C. Holland Jeffrey A. Winkles Graeme F. Woodworth |
author_facet | Nina P. Connolly Amol C. Shetty Jesse A. Stokum Ina Hoeschele Marni B. Siegel C. Ryan Miller Anthony J. Kim Cheng-Ying Ho Eduardo Davila J. Marc Simard Scott E. Devine John H. Rossmeisl Eric C. Holland Jeffrey A. Winkles Graeme F. Woodworth |
author_sort | Nina P. Connolly |
collection | DOAJ |
description | Abstract Glioma is a unique neoplastic disease that develops exclusively in the central nervous system (CNS) and rarely metastasizes to other tissues. This feature strongly implicates the tumor-host CNS microenvironment in gliomagenesis and tumor progression. We investigated the differences and similarities in glioma biology as conveyed by transcriptomic patterns across four mammalian hosts: rats, mice, dogs, and humans. Given the inherent intra-tumoral molecular heterogeneity of human glioma, we focused this study on tumors with upregulation of the platelet-derived growth factor signaling axis, a common and early alteration in human gliomagenesis. The results reveal core neoplastic alterations in mammalian glioma, as well as unique contributions of the tumor host to neoplastic processes. Notable differences were observed in gene expression patterns as well as related biological pathways and cell populations known to mediate key elements of glioma biology, including angiogenesis, immune evasion, and brain invasion. These data provide new insights regarding mammalian models of human glioma, and how these insights and models relate to our current understanding of the human disease. |
first_indexed | 2024-12-13T17:04:59Z |
format | Article |
id | doaj.art-f2d89c7796d7442691323a555b449266 |
institution | Directory Open Access Journal |
issn | 2045-2322 |
language | English |
last_indexed | 2024-12-13T17:04:59Z |
publishDate | 2018-01-01 |
publisher | Nature Portfolio |
record_format | Article |
series | Scientific Reports |
spelling | doaj.art-f2d89c7796d7442691323a555b4492662022-12-21T23:37:42ZengNature PortfolioScientific Reports2045-23222018-01-018111510.1038/s41598-018-19451-6Cross-species transcriptional analysis reveals conserved and host-specific neoplastic processes in mammalian gliomaNina P. Connolly0Amol C. Shetty1Jesse A. Stokum2Ina Hoeschele3Marni B. Siegel4C. Ryan Miller5Anthony J. Kim6Cheng-Ying Ho7Eduardo Davila8J. Marc Simard9Scott E. Devine10John H. Rossmeisl11Eric C. Holland12Jeffrey A. Winkles13Graeme F. Woodworth14Department of Neurosurgery, University of Maryland School of MedicineInstitute for Genome Sciences, University of Maryland School of MedicineDepartment of Neurosurgery, University of Maryland School of MedicineVirginia Bioinformatics Institute and Department of Statistics, Virginia TechDepartments of Pathology and Laboratory Medicine, Neurology, and Pharmacology, Lineberger Comprehensive Cancer Center and Neuroscience Center, University of North CarolinaDepartments of Pathology and Laboratory Medicine, Neurology, and Pharmacology, Lineberger Comprehensive Cancer Center and Neuroscience Center, University of North CarolinaDepartment of Neurosurgery, University of Maryland School of MedicineDepartment of Pathology, University of Maryland School of MedicineMarlene and Stewart Greenebaum Comprehensive Cancer Center, University of Maryland School of MedicineDepartment of Neurosurgery, University of Maryland School of MedicineInstitute for Genome Sciences, University of Maryland School of MedicineDepartment of Small Animal Clinical Sciences, Virginia-Maryland College of Veterinary MedicineFred Hutchinson Cancer Research Center, University of WashingtonMarlene and Stewart Greenebaum Comprehensive Cancer Center, University of Maryland School of MedicineDepartment of Neurosurgery, University of Maryland School of MedicineAbstract Glioma is a unique neoplastic disease that develops exclusively in the central nervous system (CNS) and rarely metastasizes to other tissues. This feature strongly implicates the tumor-host CNS microenvironment in gliomagenesis and tumor progression. We investigated the differences and similarities in glioma biology as conveyed by transcriptomic patterns across four mammalian hosts: rats, mice, dogs, and humans. Given the inherent intra-tumoral molecular heterogeneity of human glioma, we focused this study on tumors with upregulation of the platelet-derived growth factor signaling axis, a common and early alteration in human gliomagenesis. The results reveal core neoplastic alterations in mammalian glioma, as well as unique contributions of the tumor host to neoplastic processes. Notable differences were observed in gene expression patterns as well as related biological pathways and cell populations known to mediate key elements of glioma biology, including angiogenesis, immune evasion, and brain invasion. These data provide new insights regarding mammalian models of human glioma, and how these insights and models relate to our current understanding of the human disease.https://doi.org/10.1038/s41598-018-19451-6 |
spellingShingle | Nina P. Connolly Amol C. Shetty Jesse A. Stokum Ina Hoeschele Marni B. Siegel C. Ryan Miller Anthony J. Kim Cheng-Ying Ho Eduardo Davila J. Marc Simard Scott E. Devine John H. Rossmeisl Eric C. Holland Jeffrey A. Winkles Graeme F. Woodworth Cross-species transcriptional analysis reveals conserved and host-specific neoplastic processes in mammalian glioma Scientific Reports |
title | Cross-species transcriptional analysis reveals conserved and host-specific neoplastic processes in mammalian glioma |
title_full | Cross-species transcriptional analysis reveals conserved and host-specific neoplastic processes in mammalian glioma |
title_fullStr | Cross-species transcriptional analysis reveals conserved and host-specific neoplastic processes in mammalian glioma |
title_full_unstemmed | Cross-species transcriptional analysis reveals conserved and host-specific neoplastic processes in mammalian glioma |
title_short | Cross-species transcriptional analysis reveals conserved and host-specific neoplastic processes in mammalian glioma |
title_sort | cross species transcriptional analysis reveals conserved and host specific neoplastic processes in mammalian glioma |
url | https://doi.org/10.1038/s41598-018-19451-6 |
work_keys_str_mv | AT ninapconnolly crossspeciestranscriptionalanalysisrevealsconservedandhostspecificneoplasticprocessesinmammalianglioma AT amolcshetty crossspeciestranscriptionalanalysisrevealsconservedandhostspecificneoplasticprocessesinmammalianglioma AT jesseastokum crossspeciestranscriptionalanalysisrevealsconservedandhostspecificneoplasticprocessesinmammalianglioma AT inahoeschele crossspeciestranscriptionalanalysisrevealsconservedandhostspecificneoplasticprocessesinmammalianglioma AT marnibsiegel crossspeciestranscriptionalanalysisrevealsconservedandhostspecificneoplasticprocessesinmammalianglioma AT cryanmiller crossspeciestranscriptionalanalysisrevealsconservedandhostspecificneoplasticprocessesinmammalianglioma AT anthonyjkim crossspeciestranscriptionalanalysisrevealsconservedandhostspecificneoplasticprocessesinmammalianglioma AT chengyingho crossspeciestranscriptionalanalysisrevealsconservedandhostspecificneoplasticprocessesinmammalianglioma AT eduardodavila crossspeciestranscriptionalanalysisrevealsconservedandhostspecificneoplasticprocessesinmammalianglioma AT jmarcsimard crossspeciestranscriptionalanalysisrevealsconservedandhostspecificneoplasticprocessesinmammalianglioma AT scottedevine crossspeciestranscriptionalanalysisrevealsconservedandhostspecificneoplasticprocessesinmammalianglioma AT johnhrossmeisl crossspeciestranscriptionalanalysisrevealsconservedandhostspecificneoplasticprocessesinmammalianglioma AT ericcholland crossspeciestranscriptionalanalysisrevealsconservedandhostspecificneoplasticprocessesinmammalianglioma AT jeffreyawinkles crossspeciestranscriptionalanalysisrevealsconservedandhostspecificneoplasticprocessesinmammalianglioma AT graemefwoodworth crossspeciestranscriptionalanalysisrevealsconservedandhostspecificneoplasticprocessesinmammalianglioma |