Glioblastoma multiforme restructures the topological connectivity of cerebrovascular networks

Abstract Glioblastoma multiforme alters healthy tissue vasculature by inducing angiogenesis and vascular remodeling. To fully comprehend the structural and functional properties of the resulting vascular network, it needs to be studied collectively by considering both geometric and topological prope...

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Autores principales:	Artur Hahn, Julia Bode, Thomas Krüwel, Gergely Solecki, Sabine Heiland, Martin Bendszus, Björn Tews, Frank Winkler, Michael O. Breckwoldt, Felix T. Kurz
Formato:	article
Lenguaje:	EN
Publicado:	Nature Portfolio 2019
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/c52a1c805c874baa838ea36edac69ca7
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spelling	oai:doaj.org-article:c52a1c805c874baa838ea36edac69ca72021-12-02T15:09:15ZGlioblastoma multiforme restructures the topological connectivity of cerebrovascular networks10.1038/s41598-019-47567-w2045-2322https://doaj.org/article/c52a1c805c874baa838ea36edac69ca72019-08-01T00:00:00Zhttps://doi.org/10.1038/s41598-019-47567-whttps://doaj.org/toc/2045-2322Abstract Glioblastoma multiforme alters healthy tissue vasculature by inducing angiogenesis and vascular remodeling. To fully comprehend the structural and functional properties of the resulting vascular network, it needs to be studied collectively by considering both geometric and topological properties. Utilizing Single Plane Illumination Microscopy (SPIM), the detailed capillary structure in entire healthy and tumor-bearing mouse brains could be resolved in three dimensions. At the scale of the smallest capillaries, the entire vascular systems of bulk U87- and GL261-glioblastoma xenografts, their respective cores, and healthy brain hemispheres were modeled as complex networks and quantified with fundamental topological measures. All individual vessel segments were further quantified geometrically and modular clusters were uncovered and characterized as meta-networks, facilitating an analysis of large-scale connectivity. An inclusive comparison of large tissue sections revealed that geometric properties of individual vessels were altered in glioblastoma in a relatively subtle way, with high intra- and inter-tumor heterogeneity, compared to the impact on the vessel connectivity. A network topology analysis revealed a clear decomposition of large modular structures and hierarchical network organization, while preserving most fundamental topological classifications, in both tumor models with distinct growth patterns. These results augment our understanding of cerebrovascular networks and offer a topological assessment of glioma-induced vascular remodeling. The findings may help understand the emergence of hypoxia and necrosis, and prove valuable for therapeutic interventions such as radiation or antiangiogenic therapy.Artur HahnJulia BodeThomas KrüwelGergely SoleckiSabine HeilandMartin BendszusBjörn TewsFrank WinklerMichael O. BreckwoldtFelix T. KurzNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 9, Iss 1, Pp 1-17 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Artur Hahn Julia Bode Thomas Krüwel Gergely Solecki Sabine Heiland Martin Bendszus Björn Tews Frank Winkler Michael O. Breckwoldt Felix T. Kurz Glioblastoma multiforme restructures the topological connectivity of cerebrovascular networks
description	Abstract Glioblastoma multiforme alters healthy tissue vasculature by inducing angiogenesis and vascular remodeling. To fully comprehend the structural and functional properties of the resulting vascular network, it needs to be studied collectively by considering both geometric and topological properties. Utilizing Single Plane Illumination Microscopy (SPIM), the detailed capillary structure in entire healthy and tumor-bearing mouse brains could be resolved in three dimensions. At the scale of the smallest capillaries, the entire vascular systems of bulk U87- and GL261-glioblastoma xenografts, their respective cores, and healthy brain hemispheres were modeled as complex networks and quantified with fundamental topological measures. All individual vessel segments were further quantified geometrically and modular clusters were uncovered and characterized as meta-networks, facilitating an analysis of large-scale connectivity. An inclusive comparison of large tissue sections revealed that geometric properties of individual vessels were altered in glioblastoma in a relatively subtle way, with high intra- and inter-tumor heterogeneity, compared to the impact on the vessel connectivity. A network topology analysis revealed a clear decomposition of large modular structures and hierarchical network organization, while preserving most fundamental topological classifications, in both tumor models with distinct growth patterns. These results augment our understanding of cerebrovascular networks and offer a topological assessment of glioma-induced vascular remodeling. The findings may help understand the emergence of hypoxia and necrosis, and prove valuable for therapeutic interventions such as radiation or antiangiogenic therapy.
format	article
author	Artur Hahn Julia Bode Thomas Krüwel Gergely Solecki Sabine Heiland Martin Bendszus Björn Tews Frank Winkler Michael O. Breckwoldt Felix T. Kurz
author_facet	Artur Hahn Julia Bode Thomas Krüwel Gergely Solecki Sabine Heiland Martin Bendszus Björn Tews Frank Winkler Michael O. Breckwoldt Felix T. Kurz
author_sort	Artur Hahn
title	Glioblastoma multiforme restructures the topological connectivity of cerebrovascular networks
title_short	Glioblastoma multiforme restructures the topological connectivity of cerebrovascular networks
title_full	Glioblastoma multiforme restructures the topological connectivity of cerebrovascular networks
title_fullStr	Glioblastoma multiforme restructures the topological connectivity of cerebrovascular networks
title_full_unstemmed	Glioblastoma multiforme restructures the topological connectivity of cerebrovascular networks
title_sort	glioblastoma multiforme restructures the topological connectivity of cerebrovascular networks
publisher	Nature Portfolio
publishDate	2019
url	https://doaj.org/article/c52a1c805c874baa838ea36edac69ca7
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Glioblastoma multiforme restructures the topological connectivity of cerebrovascular networks

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