Cargando…

Vein fate determined by flow-based but time-delayed integration of network architecture

Veins in vascular networks, such as in blood vasculature or leaf networks, continuously reorganize, grow or shrink, to minimize energy dissipation. Flow shear stress on vein walls has been set forth as the local driver for a vein’s continuous adaptation. Yet, shear feedback alone cannot account for...

Descripción completa

Detalles Bibliográficos
Autores principales: Marbach, Sophie, Ziethen, Noah, Bastin, Leonie, Bäuerle, Felix K, Alim, Karen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10234634/
https://www.ncbi.nlm.nih.gov/pubmed/36916885
http://dx.doi.org/10.7554/eLife.78100
_version_ 1785052537909411840
author Marbach, Sophie
Ziethen, Noah
Bastin, Leonie
Bäuerle, Felix K
Alim, Karen
author_facet Marbach, Sophie
Ziethen, Noah
Bastin, Leonie
Bäuerle, Felix K
Alim, Karen
author_sort Marbach, Sophie
collection PubMed
description Veins in vascular networks, such as in blood vasculature or leaf networks, continuously reorganize, grow or shrink, to minimize energy dissipation. Flow shear stress on vein walls has been set forth as the local driver for a vein’s continuous adaptation. Yet, shear feedback alone cannot account for the observed diversity of vein dynamics – a puzzle made harder by scarce spatiotemporal data. Here, we resolve network-wide vein dynamics and shear rate during spontaneous reorganization in the prototypical vascular networks of Physarum polycephalum. Our experiments reveal a plethora of vein dynamics (stable, growing, shrinking) where the role of shear is ambiguous. Quantitative analysis of our data reveals that (a) shear rate indeed feeds back on vein radius, yet, with a time delay of 1–3 min. Further, we reconcile the experimentally observed disparate vein fates by developing a model for vein adaptation within a network and accounting for the observed time delay. The model reveals that (b) vein fate is determined by parameters – local pressure or relative vein resistance – which integrate the entire network’s architecture, as they result from global conservation of fluid volume. Finally, we observe avalanches of network reorganization events that cause entire clusters of veins to vanish. Such avalanches are consistent with network architecture integrating parameters governing vein fate as vein connections continuously change. As the network architecture integrating parameters intrinsically arise from laminar fluid flow in veins, we expect our findings to play a role across flow-based vascular networks.
format Online
Article
Text
id pubmed-10234634
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-102346342023-06-02 Vein fate determined by flow-based but time-delayed integration of network architecture Marbach, Sophie Ziethen, Noah Bastin, Leonie Bäuerle, Felix K Alim, Karen eLife Physics of Living Systems Veins in vascular networks, such as in blood vasculature or leaf networks, continuously reorganize, grow or shrink, to minimize energy dissipation. Flow shear stress on vein walls has been set forth as the local driver for a vein’s continuous adaptation. Yet, shear feedback alone cannot account for the observed diversity of vein dynamics – a puzzle made harder by scarce spatiotemporal data. Here, we resolve network-wide vein dynamics and shear rate during spontaneous reorganization in the prototypical vascular networks of Physarum polycephalum. Our experiments reveal a plethora of vein dynamics (stable, growing, shrinking) where the role of shear is ambiguous. Quantitative analysis of our data reveals that (a) shear rate indeed feeds back on vein radius, yet, with a time delay of 1–3 min. Further, we reconcile the experimentally observed disparate vein fates by developing a model for vein adaptation within a network and accounting for the observed time delay. The model reveals that (b) vein fate is determined by parameters – local pressure or relative vein resistance – which integrate the entire network’s architecture, as they result from global conservation of fluid volume. Finally, we observe avalanches of network reorganization events that cause entire clusters of veins to vanish. Such avalanches are consistent with network architecture integrating parameters governing vein fate as vein connections continuously change. As the network architecture integrating parameters intrinsically arise from laminar fluid flow in veins, we expect our findings to play a role across flow-based vascular networks. eLife Sciences Publications, Ltd 2023-03-14 /pmc/articles/PMC10234634/ /pubmed/36916885 http://dx.doi.org/10.7554/eLife.78100 Text en © 2023, Marbach, Ziethen et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Physics of Living Systems
Marbach, Sophie
Ziethen, Noah
Bastin, Leonie
Bäuerle, Felix K
Alim, Karen
Vein fate determined by flow-based but time-delayed integration of network architecture
title Vein fate determined by flow-based but time-delayed integration of network architecture
title_full Vein fate determined by flow-based but time-delayed integration of network architecture
title_fullStr Vein fate determined by flow-based but time-delayed integration of network architecture
title_full_unstemmed Vein fate determined by flow-based but time-delayed integration of network architecture
title_short Vein fate determined by flow-based but time-delayed integration of network architecture
title_sort vein fate determined by flow-based but time-delayed integration of network architecture
topic Physics of Living Systems
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10234634/
https://www.ncbi.nlm.nih.gov/pubmed/36916885
http://dx.doi.org/10.7554/eLife.78100
work_keys_str_mv AT marbachsophie veinfatedeterminedbyflowbasedbuttimedelayedintegrationofnetworkarchitecture
AT ziethennoah veinfatedeterminedbyflowbasedbuttimedelayedintegrationofnetworkarchitecture
AT bastinleonie veinfatedeterminedbyflowbasedbuttimedelayedintegrationofnetworkarchitecture
AT bauerlefelixk veinfatedeterminedbyflowbasedbuttimedelayedintegrationofnetworkarchitecture
AT alimkaren veinfatedeterminedbyflowbasedbuttimedelayedintegrationofnetworkarchitecture