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Expression and regulation of a sea urchin Msx class homeobox gene: insights into the evolution and function of a gene family that participates in the patterning of the early embryo.

Inductive tissue interactions, in which signals from one tissue alter the fate of another, are an essential feature of the development of all metazoans. Secreted and membrane-bound signaling molecules, their receptors, and a series of intracellular signal transducers are key molecular components of inductive interactions. Equally important are systems of transcription factors that respond to and regulate such intracellular signaling pathways (Davidson, 1990). Among these transcription factors are the Msx proteins. Named for the Drosophila msh, the Msx proteins are homeodomain-containing DNA-binding proteins that can function as both transcriptional activators and repressors (Davidson, 1995). Characterized by a distinct and highly conserved homeodomain, Msx proteins have been identified in a wide variety of metazoans from vertebrates to coelenterates. Although there is evidence that they participate in inductive tissue interactions that underlie vertebrate organogenesis, including those that pattern the neural crest, there is little information about their function in simple deuterostomes.

To learn more about the ancient function of Msx genes, to shed light on the evolution of developmental mechanisms within the lineage that gave rise to vertebrates, and finally, to provide a molecular baseline for assessing the effects of microgravity on key regulatory events of embryonic patterning, we have isolated and characterized Msx genes from ascidians and echinoderms (Ma et al., 1995; Dobias et al., 1996). We demonstrate that portions of the Msx protein sequence, including the homeodomain and flanking amino acids, are highly conserved across wide phylogenetic distances. Also conserved, particularly among echinoderms, ascidians, and vertebrates, are aspects of Msx expression patterns during early embryogenesis. In an analysis of Msx gene function, we show that overexpression of a sea urchin Msx gene (SpMsx) causes profound anomalies in gastrulation and spiculogenesis, but does not alter the specification of the major embryonic territories. Further, SpMsx, like its mammalian congeners, is regulated by members of the BMP family (TGF-[Beta] superfamily) of signaling molecules, and that the downstream targets of SpMsx likely includes components of the extracellular matrix. We conclude that Msx genes function in signaling processes that underlie patterning of early embryos. We suggest that Msx gene activity may provide a useful marker for inductive interactions that may be perturbed during the stresses of space flight.

Literature Cited

Davidson, D. 1995. The function and evolution of Msx genes: pointers and paradoxes. Trends Genet. 11:405-411.

Davidson, E. H. 1990. How embryos work: a comparative view of diverse modes of cell fate specification. Development 108: 365-369.

Dobias, S. L., L. Ma, J. R. Bell, and R. Maxson. 1996. Expression and regulation of a sea urchin Msx class homeobox gene: insights into the evolution of Msx gene function. Mech. Dev. In press.

Ma, L., B. J. Swalla, J. Zhou, J. Chen, R. Maxson, and W. Jeffery. 1995. Expression of an Msx homeobox gene in ascidians: developmental insights into the origin and evolution of vertebrates. Dev. Dyn. 205: 308-318.

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Title Annotation:The Future of Aquatic Research in Space: Neurobiology, Cellular and Molecular Biology
Author:Maxson, Rob; Tan, Hongying; Dobias, Sonia L.; Wu, Hailin; Bell, Jeffrey R.; Ma, Liang
Publication:The Biological Bulletin
Date:Feb 1, 1997
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