PDGF-A controls mesoderm cell orientation and radial intercalation during<i>Xenopus</i>gastrulation

Damm, Erich W.; Winklbauer, Rudolf

doi:10.1242/dev.056903

Cited by 54 publications

(82 citation statements)

References 43 publications

(51 reference statements)

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“…As pdgf-b mRNA is extremely poorly expressed during gastrulation, this data corroborates the idea that in the early phases of development, the main role of PDGF signalling is played by the homodimer pdgf-aa via pdgfr-a. This is in line with the observation that in pdgf-a morphants the prechordal mesoderm fails to spread during gastrulation and no compensatory mechanisms occurs (Damm and Winklbauer, 2011). At the end of neurulation (Stage 20), pdgf-b mRNA expression level rose and then decreased again at late tailbud stages (stage 35) (Fig.…”

Section: Pdgf-b Is Expressed During Xenopus Laevis Developmentsupporting

confidence: 89%

“…After the start of the zygotic transcription (stage 8), pdgf-b mRNA was barely detectable and it showed a low expression level both during gastrulation (stage 10.5) and neurulation (stage 13); on the contrary, pdgfr-a was abundantly expressed at these stages. During gastrulation in Xenopus, a crucial role for pdgf-a and pdgfr-a has been demonstrated (Damm and Winklbauer, 2011). As pdgf-b mRNA is extremely poorly expressed during gastrulation, this data corroborates the idea that in the early phases of development, the main role of PDGF signalling is played by the homodimer pdgf-aa via pdgfr-a.…”

Section: Pdgf-b Is Expressed During Xenopus Laevis Developmentsupporting

confidence: 79%

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Platelet derived growth factor B gene expression in the Xenopus laevis developing central nervous system

Giannetti¹,

Corsinovi²,

Rossino³

et al. 2016

Int. J. Dev. Biol.

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Platelet-derived growth factor B (PDGF-B) belongs to the mitogen and growth factor family and like the other members it has many roles in cell differentiation, proliferation and migration during development, adult life and in pathological conditions. Among them it has been observed that aberrant PDGF signalling is frequently linked to glioma development and progression, and Pdgf-b over-expression in mouse neural progenitors leads to the formation of gliomas. Despite this evidence, the mechanisms underlying PDGF-B driven tumorigenesis and its role during brain development are not fully understood. In order to contribute to clarifying possible new roles of pdgf-b signalling, we present here the embryonic gene expression pattern of pdgf-b, so far unknown in early vertebrate development. By using Xenopus laevis as a model system we performed qRT-PCR and whole mount in situ hybridization. Pdgf-b mRNA is expressed in discrete regions of the developing central nervous system, in the cranial nerve placodes and in the notochord. We also compared the gene expression of pdgf-b with that of its receptor pdgfr-a suggesting so far unsuspected roles for this signalling pathway during the development of specific embryonic structures. KEY WORDS: PDGF-B, PDGF receptor a, central nervous system, neural crest, Xenopus laevisPlatelet-derived growth factor (PDGF) family comprises two tyrosine kinase receptors (PDGFR-a and -b) and four ligands (PDGF-A, -B, -C, and -D) that form homodimers or the heterodimer AB (Demoulin and Essaghir, 2014). The active ligand-receptor complex consists of two receptor chains associated with one dimeric ligand. While PDGFR-a binds to all PDGF isoforms except for PDGF-DD, PDGFR-b binds only to PDGF-BB and -DD (Fig.1). Also a heterodimeric ab receptor has been reported that binds to PDGF-AB, -BB and possibly -CC and -DD (Demoulin and Essaghir, 2014). The members of this family have been extensively studied for more than 30 years in development, adult homeostasis and disease (Heldin, 2013, Heldin, 2014, Hoch and Soriano, 2003. Pdgf-a expression was recently characterized in mouse tissues and in early embryonic development, showing its involvement in developmental processes including gastrulation and craniofacial development (Andrae et al., 2014, Eberhart et al., 2008. On the contrary, for pdgf-b the only information available mainly concern its role during embryonic angiogenesis (Hoch and Soriano, 2003, Leveen et al., 1994), and a complete gene expression pattern in vertebrate embryogenesis is still lacking. Functional studies using a knock out mouse for pdgf-b showed abnormal kidney glomeruli, heart and blood vessel dilation, anemia, thrombocytopenia, haemorrhages and perinatal death (Betsholtz, 1995, Leveen et al., 1994. However, in this mutant line, BB homodimer and AB heterodimer were simultaneously abrogated, making difficult to precisely define the specific role of pdgf-b alone during embryogenesis. Furthermore, due to extensive perinatal haemorrhages, other possible phenotypes caused by the...

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Section: Pdgf-b Is Expressed During Xenopus Laevis Developmentsupporting

confidence: 89%

Section: Pdgf-b Is Expressed During Xenopus Laevis Developmentsupporting

confidence: 79%

Platelet derived growth factor B gene expression in the Xenopus laevis developing central nervous system

Giannetti¹,

Corsinovi²,

Rossino³

et al. 2016

Int. J. Dev. Biol.

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“…In several organisms, it has been shown that a single growth factor influences multiple cell behaviors, although the details vary. During Xenopus gastrulation, PDGF regulates the orientation, radial intercalation and directional migration of mesodermal cells (Nagel et al, 2004;Damm and Winklbauer, 2011). PDGF signaling also regulates cell polarization and the formation of cellular processes by mesendodermal cells in zebrafish, but apparently not their directional migration (Montero et al, 2003).…”

Section: Discussionmentioning

confidence: 99%

Growth factor-mediated mesodermal cell guidance and skeletogenesis during sea urchin gastrulation

2013

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Growth factor signaling pathways provide essential cues to mesoderm cells during gastrulation in many metazoans. Recent studies have implicated the VEGF and FGF pathways in providing guidance and differentiation cues to primary mesenchyme cells (PMCs) during sea urchin gastrulation, although the relative contributions of these pathways and the cell behaviors they regulate are not fully understood. Here, we show that FGF and VEGF ligands are expressed in distinct domains in the embryonic ectoderm of Lytechinus variegatus. We find that PMC guidance is specifically disrupted in Lv-vegf3 morphants and these embryos fail to form skeletal elements. By contrast, PMC migration is unaffected in Lv-fgfa morphants, and well-patterned but shortened skeletal elements form. We use a VEGFR inhibitor, axitinib, to show that VEGF signaling is essential not only for the initial phase of PMC migration (subequatorial ring formation), but also for the second phase (migration towards the animal pole). VEGF signaling is not required, however, for PMC fusion. Inhibition of VEGF signaling after the completion of PMC migration causes significant defects in skeletogenesis, selectively blocking the elongation of skeletal rods that support the larval arms, but not rods that form in the dorsal region of the embryo. Nanostring nCounter analysis of ∼100 genes in the PMC gene regulatory network shows a decrease in the expression of many genes with proven or predicted roles in biomineralization in vegf3 morphants. Our studies lead to a better understanding of the roles played by growth factors in sea urchin gastrulation and skeletogenesis.

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“…In both models, migrating mesendoderm cells orient their protrusions toward the direction of migration (Fig. 2 j; Davidson et al, 2002;Montero et al, 2003;Diz-Muñoz et al, 2010;Damm and Winklbauer, 2011;Dumortier et al, 2012;Weber et al, 2012). Similar to the neural crest, the Wnt/planar cell polarity (PCP) pathway has been suggested to contribute to orientation of protrusions and coordination of migration of mesendodermal cells (Ulrich et al, 2003;Dumortier et al, 2012).…”

Section: Polarization Of the Collective: Leaders And Followersmentioning

confidence: 98%

“…2 i) and to regulate directional migration of leading edge precursors in a PDG FR/PI3K-dependent manner (Nagel et al, 2004). A shorter, soluble one instead regulates protrusion orientation and directionality of migration of deep mesoderm prechordal cells (Damm and Winklbauer, 2011).…”

Section: The Role Of Chemotactic Cues In Guiding the Collectivementioning

confidence: 99%

Collective cell migration in development

Scarpa¹,

Mayor²

2016

J Exp Med

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PDGF-A controls mesoderm cell orientation and radial intercalation duringXenopusgastrulation

Cited by 54 publications

References 43 publications

Platelet derived growth factor B gene expression in the Xenopus laevis developing central nervous system

Platelet derived growth factor B gene expression in the Xenopus laevis developing central nervous system

Growth factor-mediated mesodermal cell guidance and skeletogenesis during sea urchin gastrulation

Collective cell migration in development

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