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Efficient vasculature investment in tissues can be determined without global information

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Duran-Nebreda, Salva, Johnston, Iain G. and Bassel, George (2020) Efficient vasculature investment in tissues can be determined without global information. Journal of The Royal Society Interface, 17 (165). 20200137. doi:10.1098/rsif.2020.0137

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Official URL: http://dx.doi.org/10.1098/rsif.2020.0137

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Abstract

Cells are the fundamental building blocks of organs and tissues. Information and mass flow through cellular contacts in these structures is vital for the orchestration of organ function. Constraints imposed by packing and cell immobility limit intercellular communication, particularly as organs and organisms scale up to greater sizes. In order to transcend transport limitations, delivery systems including vascular and respiratory systems evolved to facilitate the movement of matter and information. The construction of these delivery systems has an associated cost, as vascular elements do not perform the metabolic functions of the organs they are part of. This study investigates a fundamental trade-off in vascularization in multicellular tissues: the reduction of path lengths for communication versus the cost associated with producing vasculature. Biologically realistic generative models, using multicellular templates of different dimensionalities, revealed a limited advantage to the vascularization of two-dimensional tissues. Strikingly, scale-free improvements in transport efficiency can be achieved even in the absence of global knowledge of tissue organization. A point of diminishing returns in the investment of additional vascular tissue to the increased reduction of path length in 2.5- and three-dimensional tissues was identified. Applying this theory to experimentally determined biological tissue structures, we show the possibility of a co-dependency between the method used to limit path length and the organization of cells it acts upon. These results provide insight as to why tissues are or are not vascularized in nature, the robustness of developmental generative mechanisms and the extent to which vasculature is advantageous in the support of organ function.

Item Type: Journal Article
Subjects: Q Science > QH Natural history > QH301 Biology
Divisions: Faculty of Science, Engineering and Medicine > Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH): Cells -- Evolution, Blood-vessels, Biocomplexity, Computational biology, Systems biology, Biological systems -- Computer simulation
Journal or Publication Title: Journal of The Royal Society Interface
Publisher: The Royal Society Publishing
ISSN: 1742-5689
Official Date: 22 April 2020
Dates:
DateEvent
22 April 2020Published
24 March 2020Accepted
Volume: 17
Number: 165
Article Number: 20200137
DOI: 10.1098/rsif.2020.0137
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Open Access
RIOXX Funder/Project Grant:
Project/Grant IDRIOXX Funder NameFunder ID
RPG-2016-049Leverhulme Trusthttp://dx.doi.org/10.13039/501100000275
BB/ L010232/1[BBSRC] Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
BB/J017604/1[BBSRC] Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
BB/N009754/1[BBSRC] Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
UNSPECIFIEDAlan Turing Institutehttp://dx.doi.org/10.13039/100012338
805046European Research Councilhttp://dx.doi.org/10.13039/501100000781

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