Haemodynamics-Driven Developmental Pruning of Brain Vasculature in Zebrafish

Chen, Qi; Jiang, Luan; Li, Chun; Huang, Dan; Bu, Ji wen; Cai, David; Du, Jiu lin

doi:10.1371/journal.pbio.1001374

Cited by 231 publications

(258 citation statements)

References 72 publications

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“…Indeed, studies in zebrafish have shown that while EC apoptosis is associated with vessel pruning, it is largely dispensable for this process, with EC rearrangements being the primary driver of vessel pruning. 36,37 Recent detailed analysis of the angiogenic retinal vasculature in mice found that only~5% of regressing vessels found during normal angiogenesis actually contained apoptotic ECs. 38 Whether EC apoptosis is functionally necessary for vessel pruning in the mouse retina is yet to be determined.…”

Section: Discussionmentioning

confidence: 99%

Endothelial cell survival during angiogenesis requires the pro-survival protein MCL1

Whitehead

Adams

et al. 2016

Cell Death Differ

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Angiogenesis is essential to match the size of blood vessel networks to the metabolic demands of growing tissues. While many genes and pathways necessary for regulating angiogenesis have been identified, those responsible for endothelial cell (EC) survival during angiogenesis remain largely unknown. We have investigated the in vivo role of myeloid cell leukemia 1 (MCL1), a pro-survival member of the BCL2 family, in EC survival during angiogenesis. EC-specific deletion of Mcl1 resulted in a dosedependent increase in EC apoptosis in the angiogenic vasculature and a corresponding decline in vessel density. Our results suggest this apoptosis was independent of the BH3-only protein BIM. Despite the known link between apoptosis and blood vessel regression, this was not the cause of reduced vessel density observed in the absence of endothelial MCL1. Rather, the reduction in vessel density was linked to ectopic apoptosis in regions of the angiogenic vasculature where EC proliferation and new vessel growth occurs. We have therefore identified MCL1 as an essential survival factor for ECs that is required for blood vessel production during angiogenesis.

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Section: Discussionmentioning

confidence: 99%

Endothelial cell survival during angiogenesis requires the pro-survival protein MCL1

Whitehead

Adams

et al. 2016

Cell Death Differ

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“…Genome-wide expression analysis in cell culture shows that endothelial cells discriminate between multiple flow profiles by expressing different sets of genes (Boon and Horrevoets, 2009) and regulating basic cell functions (Hahn and Schwartz, 2008). Furthermore, flow forces have been shown to control heart development, patterning of the vascular network and hematopoiesis in vertebrates (Hove et al, 2003;le Noble et al, 2004;Yashiro et al, 2007;Adamo et al, 2009;North et al, 2009;Vermot et al, 2009;Buschmann et al, 2010;Liu et al, 2010;Nicoli et al, 2010;Bussmann et al, 2011;Corti et al, 2011;Chen et al, 2012;Lin et al, 2012). Nevertheless, despite the crucial role of blood flow in cardiovascular development (Jones, 2011;Freund et al, 2012), very little is known about flow forces propagation at the embryonic scales, where viscous forces dominate.…”

Section: Introductionmentioning

confidence: 99%

Pulse propagation by a capacitive mechanism drives embryonic blood flow

et al. 2013

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SUMMARYPulsatile flow is a universal feature of the blood circulatory system in vertebrates and can lead to diseases when abnormal. In the embryo, blood flow forces stimulate vessel remodeling and stem cell proliferation. At these early stages, when vessels lack muscle cells, the heart is valveless and the Reynolds number (Re) is low, few details are available regarding the mechanisms controlling pulses propagation in the developing vascular network. Making use of the recent advances in optical-tweezing flow probing approaches, fast imaging and elastic-network viscous flow modeling, we investigated the blood-flow mechanics in the zebrafish main artery and show how it modifies the heart pumping input to the network. The movement of blood cells in the embryonic artery suggests that elasticity of the network is an essential factor mediating the flow. Based on these observations, we propose a model for embryonic blood flow where arteries act like a capacitor in a way that reduces heart effort. These results demonstrate that biomechanics is key in controlling early flow propagation and argue that intravascular elasticity has a role in determining embryonic vascular function.

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“…By observing P. polycephalum we learned that pruning increases transport properties tremendously. It is fascinating to speculate that pruning in other biological systems, for example, during vessel development in zebra fish brain development [21] or during growth of a large fungal body [22], serve a similar objective of enhanced effective dispersion. Pruning itself might be triggered by the concentration of specific dispersing particles.…”

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confidence: 99%

Pruning to Increase Taylor Dispersion inPhysarum polycephalumNetworks

et al. 2016

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How do the topology and geometry of a tubular network affect the spread of particles within fluid flows? We investigate patterns of effective dispersion in the hierarchical, biological transport network formed by Physarum polycephalum. We demonstrate that a change in topology -pruning in the foraging state -causes a large increase in effective dispersion throughout the network. By comparison, changes in the hierarchy of tube radii result in smaller and more localized differences. Pruned networks capitalize on Taylor dispersion to increase the dispersion capability.PACS numbers: 87.18. Vf, 87.16.Wd Transport due to fluid flowing through tubular networks is of great interest, because it has technological applications to biomimetic microfluidic devices [1][2][3], foams [4], fuel cells [5], and other filtration systems [6] and lies at the heart of extended organisms that rely on transport networks to function: animal vasculature [7,8], fungal mycelia [9], and plant tubes [10][11][12]. A big challenge regarding transport networks is to understand how network architecture changes the efficiency of particle spread throughout a network. While it is experimentally tedious to map particle transport in a network, predicting the spread of particles is also a theoretical challenge [13][14][15][16][17][18][19][20]. Attempts to understand how the network topology and geometry affect the transport of particles are scarce [17]. Alternatively, we can study the dynamic changes of tubular network architecture in living beings. Organisms spontaneously reorganize their transport networks, including tube pruning [21][22][23][24]. Examples are vessel development in zebra fish brain development [21], or growth of a large foraging fungal body [22]. Here, we study the slime mold Physarum polycephalum which emerged as an inspiring and yet puzzling model for 'intelligent' living transport networks.P. polycephalum like foraging fungi, actively adapts its network to environmental cues [25][26][27][28][29]. Networks connecting multiple food sources are a good compromise between efficiency, reliability, and cost, comparable to human transport networks [29]. Fluid cytoplasm enclosed in the tubular network exhibits nonstationary shuttle flows [30][31][32] driven by a peristaltic wave of contractions spanning the entire organism [33]. Investigations of transport in these networks are so far limited to estimates based on the minimal distance between tubes [29,34,35]. We tracked a well-reticulated individual trimmed from a larger network (Fig. 1). After several hours, the thin central tubes were abandoned in favor of a few large central tubes and globular structures at the periphery. How does this radical change of topology affect the transport capabilities of the individual? What role do hierarchical tube radii play? We present a method to efficiently map the effective dispersion of particles from any initiation site throughout any network with nonstationary but periodic fluid flows. We use this method to study the change in dispersion patterns ...

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Haemodynamics-Driven Developmental Pruning of Brain Vasculature in Zebrafish

Abstract: This in vivo time-lapse imaging study in zebrafish reveals how changes to brain blood flow drive vessel pruning via endothelial cell migration, and how pruning leads to the simplification of the brain vasculature during development.

Cited by 231 publications

References 72 publications

Endothelial cell survival during angiogenesis requires the pro-survival protein MCL1

Endothelial cell survival during angiogenesis requires the pro-survival protein MCL1

Pulse propagation by a capacitive mechanism drives embryonic blood flow

Pruning to Increase Taylor Dispersion inPhysarum polycephalumNetworks

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