Calcium signalling during neural induction in Xenopus laevis embryos

In Xenopus, experiments performed with isolated ectoderm suggest that neural determination is a ‘by default’ mechanism, which occurs when bone morphogenetic proteins (BMPs) are antagonized by extracellular antagonists, BMP being responsible for the determination of epidermis. However, Ca2+ imaging of intact Xenopus embryos reveals patterns of Ca2+ transients which are generated via the activation of dihydropyridine-sensitive Ca2+ channels in the dorsal ectoderm but not in the ventral ectoderm. These increases in the concentration of intracellular Ca2+([Ca2+]i) appear to be necessary and sufficient to orient the ectodermal cells towards a neural fate as increasing the [Ca2+]i artificially results in neuralization of the ectoderm. We constructed a subtractive cDNA library between untreated and caffeine-treated ectoderms (to increase [Ca2+]i) and then identified early Ca2+-sensitive target genes expressed in the neural territories. One of these genes, an arginine methyltransferase, controls the expression of the early proneural gene, Zic3. Here, we discuss the evidence for the existence of an alternative model to the ‘by default’ mechanism, where Ca2+ plays a central regulatory role in the expression of Zic3, an early proneural gene, and in epidermal determination which only occurs when the Ca2+-dependent signalling pathways are inactive.

[1]  R. Dolmetsch,et al.  The C Terminus of the L-Type Voltage-Gated Calcium Channel CaV1.2 Encodes a Transcription Factor , 2006, Cell.

[2]  I. Néant,et al.  The Ca2+-induced methyltransferase xPRMT1b controls neural fate in amphibian embryo. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[3]  C. Stern Neural induction: old problem, new findings, yet more questions , 2005, Development.

[4]  P. Lemaire,et al.  Neural induction in Xenopus requires early FGF signalling in addition to BMP inhibition , 2005, Development.

[5]  E. Robertis,et al.  Neural Induction in Xenopus: Requirement for Ectodermal and Endomesodermal Signals via Chordin, Noggin, β-Catenin, and Cerberus , 2004, PLoS biology.

[6]  A. Fiorio Pla,et al.  Control of endothelial cell proliferation by calcium influx and arachidonic acid metabolism: A pharmacological approach , 2003, Journal of cellular physiology.

[7]  Vincent Bertrand,et al.  Neural Tissue in Ascidian Embryos Is Induced by FGF9/16/20, Acting via a Combination of Maternal GATA and Ets Transcription Factors , 2003, Cell.

[8]  Andrew L. Miller,et al.  Calcium transients triggered by planar signals induce the expression of ZIC3 gene during neural induction in Xenopus. , 2003, Developmental biology.

[9]  K. Mikoshiba,et al.  Molecular cloning and expression profile of Xenopus calcineurin A subunit(1). , 2000, Biochimica et biophysica acta.

[10]  S. Webb,et al.  Imaging patterns of calcium transients during neural induction in Xenopus laevis embryos. , 2000, Journal of cell science.

[11]  M Whitman,et al.  Endogenous patterns of TGFbeta superfamily signaling during early Xenopus development. , 2000, Development.

[12]  A. Duprat,et al.  Noggin upregulates Fos expression by a calcium‐mediated pathway in amphibian embryos , 1999, Development, growth & differentiation.

[13]  Britt Mellström,et al.  DREAM is a Ca2+-regulated transcriptional repressor , 1999, Nature.

[14]  S. Webb,et al.  Localized calcium transients accompany furrow positioning, propagation, and deepening during the early cleavage period of zebrafish embryos. , 1997, Developmental biology.

[15]  K. Mikoshiba,et al.  Xenopus Zic3, a primary regulator both in neural and neural crest development. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[16]  T. Yokota,et al.  Xenopus FK 506-binding protein homolog induces a secondary axis in frog embryos, which is inhibited by coexisting BMP 4 signaling. , 1997, Biochemical and biophysical research communications.

[17]  A. Duprat,et al.  L-type calcium channel activation controls the in vivo transduction of the neuralizing signal in the amphibian embryos , 1997, Mechanisms of Development.

[18]  Y. Sasai,et al.  Ectodermal patterning in vertebrate embryos. , 1997, Developmental biology.

[19]  D. Shi,et al.  A truncated FGF receptor blocks neural induction by endogenous Xenopus inducers. , 1996, Development.

[20]  F. Laezza,et al.  Basic Fibroblast Growth Factor Opens Calcium‐Permeable Channels in Quail Mesencephalic Neural Crest Neurons , 1995, The European journal of neuroscience.

[21]  V. Agarwal,et al.  XIPOU 2, a noggin-inducible gene, has direct neuralizing activity. , 1995, Development.

[22]  A. Duprat,et al.  Increased internal Ca2+ mediates neural induction in the amphibian embryo. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[23]  J. Saint-Jeannet,et al.  Experimentally provoked neural induction results in an incomplete expression of neuronal traits. , 1993, Experimental Cell Research.

[24]  J. Saint-Jeannet,et al.  Modulation of neural commitment by changes in target cell contacts in Pleurodeles waltl. , 1990, Developmental biology.

[25]  L. Tacke,et al.  Neural differentiation of Xenopus laevis ectoderm takes place after disaggregation and delayed reaggregation without inducer. , 1989, Cell differentiation and development : the official journal of the International Society of Developmental Biologists.

[26]  C. Goridis,et al.  Expression of N-CAM precedes neural induction in Pleurodeles waltl (urodele, amphibian). , 1989, Development.

[27]  R. Keller,et al.  Regional expression, pattern and timing of convergence and extension during gastrulation of Xenopus laevis. , 1988, Development.

[28]  L. G. Barth,et al.  SEQUENTIAL INDUCTION OF THE PRESUMPTIVE EPIDERMIS OF THE RANA PIPIENS GASTRULA , 1964 .

[29]  I. Néant,et al.  [xMLP is an early response calcium target gene in neural determination in Xenopus laevis]. , 2003, Journal de la Societe de biologie.

[30]  M. Moreau,et al.  xMLP est un gène de réponse précoce au calcium lors de la détermination neurale chez Xenopus laevis , 2003 .

[31]  B. Augé,et al.  [Neural determination in Xenopus laevis embryos: control of early neural gene expression by calcium]. , 2001, Journal de la Societe de biologie.

[32]  M. Moreau,et al.  La détermination neurale dans l'embryon de Xenopus laevis : Contrôle de l'expression des gènes neuraux précoces par le calcium : Rôle du calcium dans la signalisation cellulaire , 2001 .

[33]  A. Duprat,et al.  An Elevation of Internal Calcium Occurring Via L-Type Channels Mediates Neural Induction in the Amphibian Embryo , 1995 .