Formation of cardiovascular tubes in invertebrates and vertebrates

Strilić, Boris; Kučera, Tomáš; Lammert, Eckhard

doi:10.1007/s00018-010-0400-0

Cited by 26 publications

(16 citation statements)

References 129 publications

(116 reference statements)

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“…Many invertebrates have an open cardiovascular system, with hemolymph being pumped from the heart through blood vessels into the open hemocoel (Strilić et al, 2010). One might therefore speculate that the initially open CCV reflects an evolutionarily primitive stage of cardiovascular development.…”

Section: Discussionmentioning

confidence: 99%

The zebrafish common cardinal veins develop by a novel mechanism: lumen ensheathment

et al. 2013

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SUMMARYThe formation and lumenization of blood vessels has been studied in some detail, but there is little understanding of the morphogenetic mechanisms by which endothelial cells (ECs) forming large caliber vessels aggregate, align themselves and finally form a lumen that can support blood flow. Here, we focus on the development of the zebrafish common cardinal veins (CCVs), which collect all the blood from the embryo and transport it back to the heart. We show that the angioblasts that eventually form the definitive CCVs become specified as a separate population distinct from the angioblasts that form the lateral dorsal aortae. The subsequent development of the CCVs represents a novel mechanism of vessel formation, during which the ECs delaminate and align along the inner surface of an existing luminal space. Thereby, the CCVs are initially established as open-ended endothelial tubes, which extend as single EC sheets along the flow routes of the circulating blood and eventually enclose the entire lumen in a process that we term 'lumen ensheathment'. Furthermore, we found that the initial delamination of the ECs as well as the directional migration within the EC sheet depend on Cadherin 5 function. By contrast, EC proliferation within the growing CCV is controlled by Vascular endothelial growth factor C, which is provided by circulating erythrocytes. Our findings not only identify a novel mechanism of vascular lumen formation, but also suggest a new form of developmental crosstalk between hematopoietic and endothelial cell lineages.

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Section: Discussionmentioning

confidence: 99%

The zebrafish common cardinal veins develop by a novel mechanism: lumen ensheathment

et al. 2013

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“…During tube maturation, the initially narrow lumen, formed by the apical domains of one or several cells, is considerably expanded before becoming fully functional. Although tube formation and tube branching differ mechanistically between tubular organs (Andrew and Ewald, 2010;Baer et al, 2009;Bryant and Mostov, 2008;Chung and Andrew, 2008;Strilic et al, 2010), epithelial polarization is common to all systems with the orchestrated activity of the secretory pathway representing a prerequisite for polarization. In addition to the delivery of proteins to distinct membrane compartments, sorting machineries at the membrane are required that define, for example, adhesive domains to mediate cell-cell contact between lumen-forming cells and luminal membrane regions established at the luminal surface.…”

Section: Introductionmentioning

confidence: 99%

GBF1 (Gartenzwerg)-dependent secretion is required for Drosophila tubulogenesis

Wang

Meyer

Ochoa-Espinosa

et al. 2012

Journal of Cell Science

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SummaryHere we report on the generation and in vivo analysis of a series of loss-of-function mutants for the Drosophila ArfGEF, Gartenzwerg. The Drosophila gene gartenzwerg (garz) encodes the orthologue of mammalian GBF1. garz is expressed ubiquitously in embryos with substantially higher abundance in cells forming diverse tubular structures such as salivary glands, trachea, proventriculus or hindgut. In the absence of functional Garz protein, the integrity of the Golgi complex is impaired. As a result, both vesicle transport of cargo proteins and directed apical membrane delivery are severely disrupted. Dysfunction of the Arf1-COPI machinery caused by a loss of Garz leads to perturbations in establishing a polarized epithelial architecture of tubular organs. Furthermore, insufficient apical transport of proteins and other membrane components causes incomplete luminal diameter expansion and deficiencies in extracellular matrix assembly. The fact that homologues of Garz are present in every annotated metazoan genome indicates that secretion processes mediated by the GBF-type ArfGEFs play a universal role in animal development.

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“…It is tightly associated with iron homeostasis and cellular proliferation (Scotland et al 2012). These physiologic roles are strongly tied to embryonic morphogenetic events, including those that occur in the neural crest and heart (Strilic et al 2010). Since PICALM functions as a clathrin recruiter (Maritzen et al 2012), the role of PICALM in cardiac morphogenesis was investigated in X. laevis embryos by inhibiting clathrin to demonstrate the likely impact of a PICALM mutation.…”

Section: Discussionmentioning

confidence: 99%

A single codon insertion in PICALM is associated with development of familial subvalvular aortic stenosis in Newfoundland dogs

Stern

White

Lehmkuhl³

et al. 2014

Hum Genet

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Familial subvalvular aortic stenosis (SAS) is one of the most common congenital heart defects in dogs and is an inherited defect of Newfoundlands, golden retrievers and human children. Although SAS is known to be inherited, specific genes involved in Newfoundlands with SAS have not been defined. We hypothesized that SAS in Newfoundlands is inherited in an autosomal dominant pattern and caused by a single genetic variant. We studied 93 prospectively recruited Newfoundland dogs, and 180 control dogs of 30 breeds. By providing cardiac screening evaluations for Newfoundlands we conducted a pedigree evaluation, genome-wide association study and RNA sequence analysis to identify a proposed pattern of inheritance and genetic loci associated with the development of SAS. We identified a three-nucleotide exonic insertion in phosphatidylinositol-binding clathrin assembly protein (PICALM) that is associated with the development of SAS in Newfoundlands. Pedigree evaluation best supported an autosomal dominant pattern of inheritance and provided evidence that equivocally affected individuals may pass on SAS in their progeny. Immunohistochemistry demonstrated the presence of PICALM in the canine myocardium and area of the subvalvular ridge. Additionally, small molecule inhibition of clathrin-mediated endocytosis resulted in developmental abnormalities within the outflow tract (OFT) of Xenopus laevis embryos. The ability to test for presence of this PICALM insertion may impact dog-breeding decisions and facilitate reduction of SAS disease prevalence in Newfoundland dogs. Understanding the role of PICALM in OFT development may aid in future molecular and genetic investigations into other congenital heart defects of various species.

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Formation of cardiovascular tubes in invertebrates and vertebrates

Cited by 26 publications

References 129 publications

The zebrafish common cardinal veins develop by a novel mechanism: lumen ensheathment

The zebrafish common cardinal veins develop by a novel mechanism: lumen ensheathment

GBF1 (Gartenzwerg)-dependent secretion is required for Drosophila tubulogenesis

A single codon insertion in PICALM is associated with development of familial subvalvular aortic stenosis in Newfoundland dogs

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