Chemokine-Guided Angiogenesis Directs Coronary Vasculature Formation in Zebrafish

Harrison, Michael R.; Bussmann, Jeroen; Huang, Ying; Zhao, Long; Osorio, Arthela; Burns, C. Geoffrey; Burns, Caroline E.; Sucov, Henry M.; Siekmann, Arndt F.; Lien, Ching‐Ling

doi:10.1016/j.devcel.2015.04.001

Cited by 119 publications

(138 citation statements)

References 57 publications

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“…New vessels initially appear as isolated blood plexuses that subsequently connect to each other to form a network. This is similar to zebrafish coronary vessel development as described by Harrison et al (2015). Compared with wild-type siblings, the v12 mutant has more blood plexuses and vessels at initiation stages (Fig.…”

Section: The Zebrafish V12 Gene-trap Line Displays Specific Gfp Expresupporting

confidence: 57%

Vinculin b deficiency causes epicardial hyperplasia and coronary vessel disorganization in zebrafish

Cheng¹,

Miao²,

Wu³

et al. 2016

Journal of Cell Science

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Coronary vessel development is a highly coordinated process during heart formation. Abnormal development and dysfunction of the coronary network are contributory factors in the majority of heart disease. Understanding the molecular mechanisms that regulate coronary vessel formation is crucial for preventing and treating the disease. We report a zebrafish gene-trap vinculin b (vclb) mutant that displays abnormal coronary vessel development among multiple cardiac defects. The mutant shows overproliferation of epicardiumderived cells and disorganization of coronary vessels, and they eventually die off at juvenile stages. Mechanistically, Vclb deficiency results in the release of another cytoskeletal protein, paxillin, from the Vclb complex and the upregulation of ERK and FAK phosphorylation in epicardium and endocardium, causing disorganization of endothelial cells and pericytes during coronary vessel development. By contrast, cardiac muscle development is relatively normal, probably owing to redundancy with Vcla, a vinculin paralog that is expressed in the myocardium but not epicardium. Together, our results reveal a previously unappreciated function of vinculin in epicardium and endocardium and reinforce the notion that well-balanced FAK activity is essential for coronary vessel development.

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Section: The Zebrafish V12 Gene-trap Line Displays Specific Gfp Expresupporting

confidence: 57%

Vinculin b deficiency causes epicardial hyperplasia and coronary vessel disorganization in zebrafish

Cheng¹,

Miao²,

Wu³

et al. 2016

Journal of Cell Science

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“…To investigate whether some invading vessels also express venous markers, we cryoinjured the hearts of Tg(flt4:YFP) fish. As shown, coronary vessels down-regulating arterial markers did not display flt4:YFP expression (27); indeed, we observed only a few flt4:YFP + vessels, most of which were located in the bulbus arteriosus (Fig. S3H).…”

Section: Resultsmentioning

confidence: 94%

“…Using a recently developed vegfaa mutant (28), we found that rescued vegfaa −/− adult fish displayed coronary vessels. It has been recently shown that the formation of zebrafish coronaries starts at 1-2 mo of age (27), indicating that vegfaa mutants might develop compensatory mechanisms to form a coronary network, as suggested by Rossi et al (28). To completely block angiogenic revascularization after injury, we developed an inducible dn-vegfaa line.…”

Section: Discussionmentioning

confidence: 89%

“…Lastly, recent studies have shown that during coronary development in zebrafish, migratory vessels express cxcr4a:YFP, and upon formation of the coronary network, cxcr4a:YFP expression gets restricted to arteries (27). Therefore, to assess whether revascularizing vessels recapitulate the coronary developmental program, we injured Tg(cxcr4a:YFP) fish.…”

Section: Resultsmentioning

confidence: 99%

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Fast revascularization of the injured area is essential to support zebrafish heart regeneration

Marín-Juez

Marass

Gauvrit

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

158

219

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Zebrafish have a remarkable capacity to regenerate their heart. Efficient replenishment of lost tissues requires the activation of different cell types including the epicardium and endocardium. A complex set of processes is subsequently needed to support cardiomyocyte repopulation. Previous studies have identified important determinants of heart regeneration; however, to date, how revascularization of the damaged area happens remains unknown. Here, we show that angiogenic sprouting into the injured area starts as early as 15 h after injury. To analyze the role of vegfaa in heart regeneration, we used vegfaa mutants rescued to adulthood by vegfaa mRNA injections at the one-cell stage. Surprisingly, vegfaa mutants develop coronaries and revascularize after injury. As a possible explanation for these observations, we find that vegfaa mutant hearts up-regulate the expression of potentially compensating genes. Therefore, to overcome the lack of a revascularization phenotype in vegfaa mutants, we generated fish expressing inducible dominant negative Vegfaa. These fish displayed minimal revascularization of the damaged area. In the absence of fast angiogenic revascularization, cardiomyocyte proliferation did not occur, and the heart failed to regenerate, retaining a fibrotic scar. Hence, our data show that a fast endothelial invasion allows efficient revascularization of the injured area, which is necessary to support replenishment of new tissue and achieve efficient heart regeneration. These findings revisit the model where neovascularization is considered to happen concomitant with the formation of new muscle. Our work also paves the way for future studies designed to understand the molecular mechanisms that regulate fast revascularization.heart regeneration | angiogenesis | revascularization | coronaries | VEGF

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“…EC migration is triggered by a multitude of signaling pathways that can act in a particular manner on different blood vessels, and this selectivity is thought to be important for coordinating the simultaneous formation of separate blood vessels (Vanhollebeke et al, 2015;Wiley et al, 2011;Ulrich et al, 2016). In addition to activating signals, angiogenic sprouts encounter numerous guidance cues that ensure proper pathway finding (reviewed by Carmeliet and Tessier-Lavigne, 2005 invades all organs, it will be essential to dissect the relevant migratory cues in each case individually and identify attractive as well as repulsive cues in order to get a coherent and comprehensive picture of the mechanisms that regulate EC migration during angiogenesis (for examples, see Cha et al, 2012;Harrison et al, 2015;Tata et al, 2015;Thomas et al, 2013;Xu et al, 2014).…”

Section: Endothelial Cell Migrationmentioning

confidence: 99%

Cell behaviors and dynamics during angiogenesis

et al. 2016

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Vascular networks are formed and maintained through a multitude of angiogenic processes, such as sprouting, anastomosis and pruning. Only recently has it become possible to study the behavior of the endothelial cells that contribute to these networks at a single-cell level in vivo. This Review summarizes what is known about endothelial cell behavior during developmental angiogenesis, focusing on the morphogenetic changes that these cells undergo.

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Chemokine-Guided Angiogenesis Directs Coronary Vasculature Formation in Zebrafish

Cited by 119 publications

References 57 publications

Vinculin b deficiency causes epicardial hyperplasia and coronary vessel disorganization in zebrafish

Vinculin b deficiency causes epicardial hyperplasia and coronary vessel disorganization in zebrafish

Fast revascularization of the injured area is essential to support zebrafish heart regeneration

Cell behaviors and dynamics during angiogenesis

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