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Haemodynamics-driven developmental pruning of brain vasculature in zebrafish

Chen, Qi ; Jiang, Luan ; Li, Chun ; Hu, Dan ; Bu, Ji-wen ; Cai, David ; Du, Jiu-lin Krasnow, Mark

PLoS biology, 2012-08, Vol.10 (8), p.e1001374-e1001374 [Periódico revisado por pares]

United States: Public Library of Science

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Título:
Haemodynamics-driven developmental pruning of brain vasculature in zebrafish
Autor: Chen, Qi ; Jiang, Luan ; Li, Chun ; Hu, Dan ; Bu, Ji-wen ; Cai, David ; Du, Jiu-lin
Krasnow, Mark
Assuntos: Angiogenesis ; Animals ; Animals, Genetically Modified - physiology ; Biology ; Blood Flow Velocity ; Blood vessels ; Brain research ; Cell Movement ; Embryo, Nonmammalian - blood supply ; Embryo, Nonmammalian - embryology ; Embryo, Nonmammalian - physiology ; Embryonic Development ; Endothelial Cells - physiology ; Experiments ; Hemodynamics ; Larva - physiology ; Macrophages - physiology ; Mathematical models ; Mesencephalon - anatomy & histology ; Mesencephalon - blood supply ; Mesencephalon - physiology ; Microscopy, Confocal - methods ; Migration ; Models, Biological ; Neovascularization, Physiologic ; Zebrafish - anatomy & histology ; Zebrafish - genetics ; Zebrafish - physiology
É parte de: PLoS biology, 2012-08, Vol.10 (8), p.e1001374-e1001374
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The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: QC JLD. Performed the experiments: QC JWB. Analyzed the data: QC LJ CL DH. Contributed reagents/materials/analysis tools: LJ CL DH DC. Wrote the paper: QC JLD. Designed research, carried out all experiments, analyzed data and wrote the paper: QC. Developed analysis methods of vasculature and analyzed data: LJ CL. Performed bead microinjection and TUNEL: JWB. Performed numerical simulation: DH DC. Designed research and wrote the paper: JLD.
The authors have declared that no competing interests exist.
Descrição: The brain blood vasculature consists of a highly ramified vessel network that is tailored to meet its physiological functions. How the brain vasculature is formed has long been fascinating biologists. Here we report that the developing vasculature in the zebrafish midbrain undergoes not only angiogenesis but also extensive vessel pruning, which is driven by changes in blood flow. This pruning process shapes the initial exuberant interconnected meshwork into a simplified architecture. Using in vivo long-term serial confocal imaging of the same zebrafish larvae during 1.5-7.5 d post-fertilization, we found that the early formed midbrain vasculature consisted of many vessel loops and higher order segments. Vessel pruning occurred preferentially at loop-forming segments via a process mainly involving lateral migration of endothelial cells (ECs) from pruned to unpruned segments rather than EC apoptosis, leading to gradual reduction in the vasculature complexity with development. Compared to unpruned ones, pruned segments exhibited a low and variable blood flow, which further decreased irreversibly prior to the onset of pruning. Local blockade of blood flow with micro-bead obstruction led to vessel pruning, whereas increasing blood flow by noradrenergic elevation of heartbeat impeded the pruning process. Furthermore, the occurrence of vessel pruning could be largely predicted by haemodynamics-based numerical simulation of vasculature refinement. Thus, changes of blood flow drive vessel pruning via lateral migration of ECs, leading to the simplification of the vasculature and possibly efficient routing of blood flow in the developing brain.
Editor: United States: Public Library of Science
Idioma: Inglês

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Haemodynamics-driven developmental pruning of brain vasculature in zebrafish

Chen, Qi ; Jiang, Luan ; Li, Chun ; Hu, Dan ; Bu, Ji-wen ; Cai, David ; Du, Jiu-lin Krasnow, Mark

United States: Public Library of Science

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