Vasculogenesis drives pulmonary vascular growth in the developing chick embryo

Anderson‐Berry, Ann; O’Brien, Elizabeth; Bleyl, Steven B.; Lawson, Angela K.; Gundersen, Nancy; Ryssman, Daniel B.; Sweeley, John; Dahl, Mar Janna; Drake, Christopher J.; Schoenwolf, Gary C.; Albertine, Kurt H.

doi:10.1002/dvdy.20296

Cited by 38 publications

(25 citation statements)

References 57 publications

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“…This was largely based on the observation in histological sections of individual angioblasts, which were not connected to the existing vessels, such as during liver and lung vascular development in mouse and chick embryos (Anderson-Berry et al, 2005; Kingsbury et al, 1956; Matsumoto et al, 2001; Sherer, 1991; Zeng et al, 1998). Based on our results, it is tempting to speculate that in other vertebrates, similar to zebrafish, organ specific vascularization also happens by the migration and coalescence of individual endothelial cells, which are derived from the existing vasculature.…”

Section: Discussionmentioning

confidence: 99%

Vegfa signaling promotes zebrafish intestinal vasculature development through endothelial cell migration from the posterior cardinal vein

Koenig

Baltrunaite

Bower

et al. 2016

Developmental Biology

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The mechanisms underlying organ vascularization are not well understood. The zebrafish intestinal vasculature forms early, is easily imaged using transgenic lines and in-situ hybridization, and develops in a stereotypical pattern thus making it an excellent model for investigating mechanisms of organ specific vascularization. Here, we demonstrate that the sub-intestinal vein (SIV) and supra-intestinal artery (SIA) form by a novel mechanism from angioblasts that migrate out of the posterior cardinal vein and coalesce to form the intestinal vasculature in an anterior to posterior wave with the SIA forming after the SIV. We show that vascular endothelial growth factor aa (vegfaa) is expressed in the endoderm at the site where intestinal vessels form and therefore likely provides a guidance signal. Vegfa/Vegfr2 signaling is required for early intestinal vasculature development with mutation in vegfaa or loss of Vegfr2 homologs causing nearly complete inhibition of the formation of the intestinal vasculature. Vegfc and Vegfr3 function, however, are dispensable for intestinal vascularization. Interestingly, ubiquitous overexpression of Vegfc resulted in an overgrowth of the SIV, suggesting that Vegfc is sufficient to induce SIV development. These results argue that Vegfa signaling directs endothelial cells to migrate out of existing vasculature and coalesce to form the intestinal vessels. It is likely that a similar mechanism is utilized during vascularization of other organs.

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Section: Discussionmentioning

confidence: 99%

Vegfa signaling promotes zebrafish intestinal vasculature development through endothelial cell migration from the posterior cardinal vein

Koenig

Baltrunaite

Bower

et al. 2016

Developmental Biology

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“…The origin of the many cell lineages that comprise the pulmonary vasculature is also unclear and has remained a point of controversy, with data supporting both angiogenic and vasculogenic processes involved in generating the complex vasculature tree of the lungs (deMello et al, 1997;Schachtner et al, 2000;Anderson-Berry et al, 2005;Parera et al, 2005). However, evidence from lineage-tracing experiments has begun to address this controversy.…”

Section: Progenitor Cells In the Developing Lung Mesodermmentioning

confidence: 99%

“…A recently generated Fgf10 cre-ERT2 allele, which appears to be useful for tracking Fgf10 + cells in the lung mesoderm, may provide important insight into lung mesodermal differentiation (El Agha et al, 2012). However, additional markers are required to help sort out the heterogeneity and respective capacity of the mesoderm to generate these differentiated lineages.The origin of the many cell lineages that comprise the pulmonary vasculature is also unclear and has remained a point of controversy, with data supporting both angiogenic and vasculogenic processes involved in generating the complex vasculature tree of the lungs (deMello et al, 1997;Schachtner et al, 2000;Anderson-Berry et al, 2005;Parera et al, 2005). However, evidence from lineage-tracing experiments has begun to address this controversy.…”

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confidence: 99%

Lung development: orchestrating the generation and regeneration of a complex organ

2014

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The respiratory system, which consists of the lungs, trachea and associated vasculature, is essential for terrestrial life. In recent years, extensive progress has been made in defining the temporal progression of lung development, and this has led to exciting discoveries, including the derivation of lung epithelium from pluripotent stem cells and the discovery of developmental pathways that are targets for new therapeutics. These discoveries have also provided new insights into the regenerative capacity of the respiratory system. This Review highlights recent advances in our understanding of lung development and regeneration, which will hopefully lead to better insights into both congenital and acquired lung diseases. KEY WORDS: Branching morphogenesis, Epigenetics, Lung, Regeneration IntroductionThe primary function of the lungs is to exchange oxygen in the external environment with carbon dioxide in the cardiovascular system. Although this process sounds straightforward, it is fraught with multiple barriers to its success. The entire airway, like the skin, is constantly exposed to the external environment and must cope with challenges including temperature, particulate matter and allergens. Terrestrial life has adapted to these and other challenges through the evolution of a complex respiratory system consisting of a multitude of cell lineages. These cellular components are constantly communicating with each other to exchange gas efficiently while preventing blood and fluid loss and dangerous infection from pathogens.Lung development has been studied extensively in recent years, generating new insights into the origins of the different cell lineages that exist in the lung as well as the molecular pathways that regulate these lineages. This has led to novel insights into congenital lung diseases, lung abnormalities and acquired lung diseases (Box 1), including asthma and chronic obstructive pulmonary disease (COPD), and the lung's response to acute injury. In addition, these studies have revealed that some cell lineages within the mammalian respiratory system can regenerate after injury through the activation of stem/progenitor populations or through proliferation-induced cellular expansion. The molecular pathways that regulate these regenerative processes have been identified, raising the hope that these can be harnessed to promote lung regeneration in humans. Moreover, using the robust knowledge of pathways that regulate early lung development, lung epithelial cells can now be generated from embryonic stem cells (ESCs) and induced pluripotent stem cells (iPSCs), providing an additional source of cells for disease modeling and potential cell-based therapies (Longmire et al., 2012;Mou et al., 2012). In this Review, we highlight recent advances in the basic understanding of lung development and regeneration with a focus on the cell biology of the developing lung epithelium, the role of endoderm progenitors, and the epigenetic regulation of lung development and regeneration. We also discuss how these adv...

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“…Alveolar capillaries, where the gas exchange occcurs, sprout from this network by angiogenesis. The bronchial circulation is formed mainly by angiogenesis from the dorsal aorta [57] [58]. Under normal conditions, about 5% of the total blood volume to the lungs is supplied by the bronchial circulation, which vascularizes the airway wall and the large pulmonary vessels [2].…”

Section: Lung Circulationsmentioning

confidence: 99%

Pro-angiogenic hematopoietic progenitor cells and endothelial colony-forming cells in pathological angiogenesis of bronchial and pulmonary circulation

2011

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Dysregulation of angiogenesis is a common feature of many disease processes. Vascular remodeling is believed to depend on the participation of endothelial progenitor cells, but the identification of endothelial progenitors in postnatal neovascularization remains elusive. Current understanding posits a role for circulating pro-angiogenic hematopoietic cells, which interact with local endothelial cells to establish an environment that favors angiogenesis in physiologic and pathophysiologic responses. In the lung, increased and dysregulated angiogenesis is a hallmark of diseases of the bronchial and pulmonary circulations, manifested by asthma and pulmonary arterial hypertension (PAH), respectively. In asthma THelper-2 immune cells produce angiogenic factors that mobilize and recruit pro-inflammatory and pro-angiogenic precursors from the bone marrow into the airway wall where they induce angiogenesis and fuel inflammation. In contrast, in PAH, upregulation of hypoxia-inducible factor (HIF) in vascular cells leads to the production of bone marrow-mobilizing factors that recruit pro-angiogenic progenitor cells to the pulmonary circulation where they contribute to angiogenic remodeling of the vessel wall. This review focuses on current knowledge of pro-angiogenic progenitor cells in the pathogenesis of asthma and PAH.

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Vasculogenesis drives pulmonary vascular growth in the developing chick embryo

Cited by 38 publications

References 57 publications

Vegfa signaling promotes zebrafish intestinal vasculature development through endothelial cell migration from the posterior cardinal vein

Vegfa signaling promotes zebrafish intestinal vasculature development through endothelial cell migration from the posterior cardinal vein

Lung development: orchestrating the generation and regeneration of a complex organ

Pro-angiogenic hematopoietic progenitor cells and endothelial colony-forming cells in pathological angiogenesis of bronchial and pulmonary circulation

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