Tubular sprouting as a mode of vascular formation in a colonial ascidian (tunicata)

Gasparini, Fabio; Longo, Fabrizio; Manni, Lucia; Burighel, Paolo; Zaniolo, Giovanna

doi:10.1002/dvdy.21073

Cited by 26 publications

(53 citation statements)

References 66 publications

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“…Even in the sea squirt, tip cells use filopodia to build a primitive vascular network. 4 It is therefore not surprising that several classes of molecules and principles, used by navigating axons or epithelial cells, are evolutionary conserved and shared, and even might have been coopted by the migrating endothelial tip cell. 1,2 "Stalk cells" trail behind the tip cell and elongate the stalk of the sprout; they proliferate, form junctions, lay down extracellular matrix, and form a lumen.…”

mentioning

confidence: 99%

Mechanisms of Vessel Branching

Smet

Segura

Bock

et al. 2009

ATVB

336

248

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Abstract-Filopodia, "the fingers that do the walking," have been identified on endothelial cells at the tip of sprouting vessels for half a century, but the key role of the tip cell in vessel branching has been recognized only in the past few years. A model is emerging, whereby tip cells lead the way in a branching vessel, stalk cells elongate the sprout, and a very recently discovered phalanx cell ensures quiescence and perfusion of the newly formed branch. Recent genetic studies have shed light on the molecular signature of these distinct endothelial phenotypes; this provides a novel conceptual framework of how vessel morphogenesis occurs. Here, we will discuss the molecular candidates that participate in the decision of endothelial cells to adapt these distinct fates and highlight the emerging insights on how these cells send out filopodia while navigating.

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confidence: 99%

Mechanisms of Vessel Branching

Smet

Segura

Bock

et al. 2009

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“…It is important to remark that myoepithelial vessel growth by these mechanisms would involve no degradation of the vascular basement membranes, contrarily to what happens in vertebrate angiogenesis. This difference had been already noted by Gasparini et al, 2007) in their report on the growth of the ectodermal vessels of Botryllus.…”

Section: Does Angiogenesis Exist In Invertebrates?mentioning

confidence: 72%

“…In fact, as far as we know, only three cases of vascular growth in adult invertebrates have been reported, in the colonial ascidian Botryllus schloesseri, the leech Hirudo medicinalis, and the squid Idiosepius paradoxus. In the first case, both, the normal growth of the extracorporeal vessels connecting the individuals from a colony and the regeneration of the circulatory system after injury have been described (Gasparini et al, 2007(Gasparini et al, , 2008. In Hirudo, the development of some peculiar vascular-like structures was elicited by injury or by injection of VEGF or other growth factors (de Eguileor et al, 2001a,b;Tettamanti et al, 2003).…”

Section: Vascular Growth In Invertebratesmentioning

confidence: 99%

“…an epithelium with the apical surface abluminal and with the basement membrane lining the vascular lumen. When a new individual arises by asexual reproduction, it develops epidermal sprouts that connect their hemal cavities to the colony vessels (Gasparini et al, 2007(Gasparini et al, , 2008. When the extracorporeal vessels and the common tunica are surgically removed, a new tunica is rapidly synthesized and new vessels are formed by sprouting of the preexisting ones.…”

Section: Vascular Growth In Invertebratesmentioning

confidence: 99%

“…Just to quote two examples, the Drosophila VEGF/PDGF genes, called PVF1-3, are broadly expressed in many tissues, inducing in this way the migration of blood cells throughout the body. In Botryllus, where VEGF and VEGFR seem to be expressed in the growing extracorporal vessels (Gasparini et al, 2007(Gasparini et al, , 2008, it seems highly unlikely that hypoxia exists in the surface of the colony, very close to the oxygenated seawater that surrounds the tunica. Furthermore, the overlapping expression pattern of VEGF and VEGFR in this species is different to the usual expression patterns of these proteins that normally do not coincide.…”

Section: Angiogenic Signalling Mechanisms In Invertebratesmentioning

confidence: 99%

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Evolution of angiogenesis

Muñoz‐Chápuli¹

2011

Int. J. Dev. Biol.

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Endothelial cells, which are the main agents of the angiogenic process in vertebrates, are lacking in the vessels of invertebrates. These are limited by the basement membranes of epithelial or myoepithelial cells. This fact leads to the questions of how vessels grow in invertebrates and how vertebrate angiogenesis evolved. We herein review the knowledge available about vascular growth in invertebrates. The cases described include the ascidian Botryllus, the annelid Hirudo and the squid Idiosepius. All these processes of vascular growth in invertebrates show substantial differences with the vertebrate angiogenesis, although the signalling system mediated by VEGF and its receptor VEGFR seems to be involved in all cases. However, VEGF signalling is used by many processes of cell directional migration, and it cannot be considered as a hallmark of angiogenesis. We also describe the close similarity between the molecular control of the endothelial angiogenesis and the branching morphogenesis of the tracheal system of insects. In both cases, the process is regulated by hypoxia and activates a leading tip cell which inhibits responsiveness of the adjacent cells through a Delta/Notch signalling pathway. We suggest that endothelial angiogenesis in vertebrates arose through cooption of this hypoxia-sensing mechanism by replacing the FGF/ FGFR axis of insects by a VEGF/VEGFR-mediated system, and adding a second layer of control of the endothelial state (quiescent or activated) mediated by angiopoietins and Tie receptors. This evolutionarily new control mechanism of endothelial angiogenesis establishes an endothelial/ perivascular cell crosstalking which does not exist in invertebrates.

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Sexual and asexual reproduction in the colonial ascidian Botryllus schlosseri

Gasparini

Manni

Cima

et al. 2014

Genesis

Self Cite

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Summary: The colonial tunicate Botryllus schlosseri is a widespread filter-feeding ascidian that lives in shallow waters and is easily reared in aquaria. Its peculiar blastogenetic cycle, characterized by the presence of three blastogenetic generations (filtering adults, buds, and budlets) and by recurrent generation changes, has resulted in over 60 years of studies aimed at understanding how sexual and asexual reproduction are coordinated and regulated in the colony. The possibility of using different methodological approaches, from classical genetics to cell transplantation, contributed to the development of this species as a valuable model organism for the study of a variety of biological processes. Here, we review the main studies detailing rearing, staging methods, reproduction and colony growth of this species, emphasizing the asymmetry in sexual and asexual reproduction potential, sexual reproduction in the field and the laboratory, and self-and crossfertilization. These data, opportunely matched with recent tanscriptomic and genomic outcomes, can give a valuable help to the elucidation of some important steps in chordate evolution. genesis 53:105-120, 2015. V C 2014Wiley Periodicals, Inc.

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Tubular sprouting as a mode of vascular formation in a colonial ascidian (tunicata)

Cited by 26 publications

References 66 publications

Mechanisms of Vessel Branching

Mechanisms of Vessel Branching

Evolution of angiogenesis

Sexual and asexual reproduction in the colonial ascidian Botryllus schlosseri

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