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Anisotropic Organization of Circumferential Actomyosin Characterizes Hematopoietic Stem Cells Emergence in the Zebrafish

Overview
Journal Elife
Specialty Biology
Date 2018 Aug 23
PMID 30132756
Citations 24
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Abstract

Hematopoiesis leads to the formation of blood and immune cells. Hematopoietic stem cells emerge during development, from vascular components, via a process called the endothelial-to-hematopoietic transition (EHT). Here, we reveal essential biomechanical features of the EHT, using the zebrafish embryo imaged at unprecedented spatio-temporal resolution and an algorithm to unwrap the aorta into 2D-cartography. We show that the transition involves anisotropic contraction along the antero-posterior axis, with heterogenous organization of contractile circumferential actomyosin. The biomechanics of the contraction is oscillatory, with unusually long periods in comparison to other apical constriction mechanisms described so far in morphogenesis, and is supported by the anisotropic reinforcement of junctional contacts. Finally, we show that abrogation of blood flow impairs the actin cytoskeleton, the morphodynamics of EHT cells, and the orientation of the emergence. Overall, our results underline the peculiarities of the EHT biomechanics and the influence of the mechanical forces exerted by blood flow.

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References
1.
North T, Goessling W, Peeters M, Li P, Ceol C, Lord A . Hematopoietic stem cell development is dependent on blood flow. Cell. 2009; 137(4):736-48. PMC: 2722870. DOI: 10.1016/j.cell.2009.04.023. View

2.
Ciau-Uitz A, Patient R . The embryonic origins and genetic programming of emerging haematopoietic stem cells. FEBS Lett. 2016; 590(22):4002-4015. DOI: 10.1002/1873-3468.12363. View

3.
Ikebe M, Hartshorne D, Elzinga M . Phosphorylation of the 20,000-dalton light chain of smooth muscle myosin by the calcium-activated, phospholipid-dependent protein kinase. Phosphorylation sites and effects of phosphorylation. J Biol Chem. 1987; 262(20):9569-73. View

4.
Isogai S, Horiguchi M, Weinstein B . The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development. Dev Biol. 2001; 230(2):278-301. DOI: 10.1006/dbio.2000.9995. View

5.
Yvernogeau L, Gautier R, Khoury H, Menegatti S, Schmidt M, Gilles J . An in vitro model of hemogenic endothelium commitment and hematopoietic production. Development. 2016; 143(8):1302-12. DOI: 10.1242/dev.126714. View