Retinoid signalling is required for information transfer from mesoderm to neuroectoderm during gastrulation

Lloret-Vilaspasa, Ferran; Jansen, Hans J.; Roos, Koen de; Chandraratna, Rosh; Zile, Maija H.; Stern, Claudio D.; Durston, Antony J.

doi:10.1387/ijdb.082705fl

Cited by 22 publications

(17 citation statements)

References 60 publications

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“…RA is required for hindbrain patterning (Muhr et al, 1999;Niederreither et al, 1999;Begemann et al, 2001;Sakai et al, 2001;Grandel et al, 2002;Kudoh et al, 2002;Emoto et al, 2005;Sirbu et al, 2005;Nordström et al, 2006;Lloret-Vilaspasa et al, 2010); yet, as our experiments show, posterior rhombomeres can develop independently of RA when the hindbrain territory is expanded caudally due to loss of Cdx4 (Fig. 6).…”

Section: Ra and Hindbrain Patterningmentioning

confidence: 49%

“…The alignment of neural and mesodermal tissues at the head-trunk transition requires their development to be coordinated. The present study provides evidence that RA is essential for the accurate alignment of the HB/SC transition to the craniovertebral junction (summarized in Table 1), and that this function is independent from the well-characterized function of RA in hindbrain patterning (Niederreither et al, 1997;Muhr et al, 1999;Begemann et al, 2001;Sakai et al, 2001;Grandel et al, 2002;Kudoh et al, 2002;Emoto et al, 2005;Sirbu et al, 2005;Nordström et al, 2006;Lloret-Vilaspasa et al, 2010). Specification of head and trunk territories in zebrafish is completed by mid to late gastrulation (Kim et al, 2002), shortly after prospective hindbrain cells become committed to their fate (Woo and Fraser, 1998) and prospective paraxial mesoderm cells ingress into the embryo, contributing to occipital and anterior vertebral somites (Muller et al, 1996).…”

Section: Ra Interacts With Fgf and Wnt Pathways To Regulate The Rostrmentioning

confidence: 60%

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Retinoic acid regulates size, pattern and alignment of tissues at the head-trunk transition

Lee

Skromne

2014

Development

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At the head-trunk transition, hindbrain and spinal cord alignment to occipital and vertebral bones is crucial for coherent neural and skeletal system organization. Changes in neural or mesodermal tissue configuration arising from defects in the specification, patterning or relative axial placement of territories can severely compromise their integration and function. Here, we show that coordination of neural and mesodermal tissue at the zebrafish head-trunk transition crucially depends on two novel activities of the signaling factor retinoic acid (RA): one specifying the size and the other specifying the axial position relative to mesodermal structures of the hindbrain territory. These activities are each independent but coordinated with the wellestablished function of RA in hindbrain patterning. Using neural and mesodermal landmarks we demonstrate that the functions of RA in aligning neural and mesodermal tissues temporally precede the specification of hindbrain and spinal cord territories and the activation of hox transcription. Using cell transplantation assays we show that RA activity in the neuroepithelium regulates hindbrain patterning directly and territory size specification indirectly. This indirect function is partially dependent on Wnts but independent of FGFs. Importantly, RA specifies and patterns the hindbrain territory by antagonizing the activity of the spinal cord specification gene cdx4; loss of Cdx4 rescues the defects associated with the loss of RA, including the reduction in hindbrain size and the loss of posterior rhombomeres. We propose that at the head-trunk transition, RA coordinates specification, patterning and alignment of neural and mesodermal tissues that are essential for the organization and function of the neural and skeletal systems.

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Section: Ra and Hindbrain Patterningmentioning

confidence: 49%

Section: Ra Interacts With Fgf and Wnt Pathways To Regulate The Rostrmentioning

confidence: 60%

Retinoic acid regulates size, pattern and alignment of tissues at the head-trunk transition

Lee

Skromne

2014

Development

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“…A recent study in frogs has convincingly shown that the blocking of RA signaling from mesoderm to neuroectoderm suppressed the expression of mid-axial hox genes in neurula embryos and led to distortion of segmental identity and reduction of posterior hindbrain (42). This prompted us to investigate whether the observed reduction of hoxd4 and the posterior hindbrain in rdhe2 morphants reflected a localized decrease in RA signaling.…”

Section: Expression Of Developmental Marker Genes Is Altered In Rdhe2mentioning

confidence: 98%

Short Chain Dehydrogenase/Reductase Rdhe2 Is a Novel Retinol Dehydrogenase Essential for Frog Embryonic Development

Belyaeva

Lee

Adams

et al. 2012

Journal of Biological Chemistry

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Background: Retinoic acid regulates expression of numerous genes, but the enzymes required for its biosynthesis are not fully defined. Results: Rdhe2 oxidizes retinol for retinoic acid biosynthesis, and its down-regulation is lethal for frog embryos. Conclusion: Rdhe2 is a previously unrecognized retinol dehydrogenase required for retinoic acid biosynthesis. Significance: Enzymes homologous to frog rdhe2 may carry out similar functions in other species.

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“…RARs function as ligand-modulated transcription factors that activate expression of their target genes (Chambon, 1996;Mangelsdorf et al, 1995;Mark et al, 2009). Studies in a variety of systems have shown that retinoic acid (RA) is an important component of the neural posteriorizing signal (Blumberg et al, 1997;Durston et al, 1989;Lloret-Vilaspasa et al, 2010;Papalopulu and Kintner, 1996;Shiotsugu et al, 2004) as well as of the AP patterning of the neural crest, somites and limbs (Moreno et al, 2008;Moreno and Kintner, 2004;Niederreither et al, 2002;Stratford et al, 1999;Villanueva et al, 2002). Retinoid signaling also establishes AP identity in the endoderm and mesoderm (Bayha et al, 2009;Deimling and Drysdale, 2009;Pan et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

RIPPLY3 is a retinoic acid-inducible repressor required for setting the borders of the pre-placodal ectoderm

et al. 2012

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SUMMARYRetinoic acid signaling is a major component of the neural posteriorizing process in vertebrate development. Here, we identify a new role for the retinoic acid receptor (RAR) in the anterior of the embryo, where RAR regulates Fgf8 expression and formation of the pre-placodal ectoderm (PPE). RAR2 signaling induces key pre-placodal genes and establishes the posterolateral borders of the PPE. RAR signaling upregulates two important genes, Tbx1 and Ripply3, during early PPE development. In the absence of RIPPLY3, TBX1 is required for the expression of Fgf8 and hence, PPE formation. In the presence of RIPPLY3, TBX1 acts as a transcriptional repressor, and functions to restrict the positional expression of Fgf8, a key regulator of PPE gene expression. These results establish a novel role for RAR as a regulator of spatial patterning of the PPE through Tbx1 and RIPPLY3. Moreover, we demonstrate that Ripply3, acting downstream of RAR signaling, is a key player in establishing boundaries in the PPE. represses the ability of TBX1 to activate reporter gene constructs in vivo and this inhibition depends on the association of RIPPLY3 with its co-repressor GROUCHO and with TBX1. In agreement with our predictions, RIPPLY3 knockdown perturbs the borders of PPE marker expression. These results demonstrate a novel role for RAR in the precise positioning of the PPE boundaries and establish RIPPLY3 as a key factor that demarcates the boundaries of the PPE. MATERIALS AND METHODS Ripply3 alignment and construction of a phylogenetic treeRipply sequences were obtained from Genbank and Uniprot databases (Benson et al., 2008;Uniprot Consortium, 2009), aligned with MAFFT (L-INS-i algorithm) (Katoh et al., 2009;Katoh et al., 2005) and a phylogenetic tree constructed with PROml, version 3.69 (Protein Maximum Likelihood) (Felsenstein, 2005). Default settings were used, global rearrangements (-G) were performed, and the outgroup (-O) was set to amphioxus. The resultant tree was drawn with FigTree (Rambaut, 2007). Conserved domains of the Ripply gene family were visualized with WebLogo (Crooks et al., 2004;Schneider and Stephens, 1990). EmbryosXenopus eggs were fertilized in vitro as described previously (Blumberg et al., 1997;Koide et al., 2001) and embryos staged according to Nieuwkoop and Faber (Nieuwkoop and Faber, 1967). Embryos were maintained in 0.1ϫ MBS until appropriate stages or treated with 1 M agonist (TTNPB) and 1 M antagonist (AGN193109) as described (Arima et al., 2005). MicroinjectionEmbryos were injected bilaterally or unilaterally at the two-cell stage with combinations of gene specific morpholinos (MO), mRNAs and 100 pg/embryo -galactosidase mRNA lineage tracer. MOs used for this study are found in supplementary material Table S1. Control embryos were injected with 20 ng standard control MO: CCT CTT ACC TCA GTT ACA ATT TAT A (GeneTools). The following plasmids were constructed by PCR amplification of the protein-coding regions of the indicated genes and cloning into the expression vector pCDG1: xRARa2.2 (Sharpe, ...

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Retinoid signalling is required for information transfer from mesoderm to neuroectoderm during gastrulation

Cited by 22 publications

References 60 publications

Retinoic acid regulates size, pattern and alignment of tissues at the head-trunk transition

Retinoic acid regulates size, pattern and alignment of tissues at the head-trunk transition

Short Chain Dehydrogenase/Reductase Rdhe2 Is a Novel Retinol Dehydrogenase Essential for Frog Embryonic Development

RIPPLY3 is a retinoic acid-inducible repressor required for setting the borders of the pre-placodal ectoderm

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