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First published online 28 August 2008
doi: 10.1242/dev.018861

Development 135, 3271-3280 (2008)
Published by The Company of Biologists 2008
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A ryanodine receptor-dependent Cai2+ asymmetry at Hensen's node mediates avian lateral identity

Ana Garic-Stankovic1, Marcos Hernandez1, George R. Flentke1, Maija H. Zile2 and Susan M. Smith1,*

1 Department of Nutritional Sciences, University of Wisconsin-Madison, Madison, WI 53706, USA.
2 Department of Food Science and Human Nutrition, Michigan State University, East Lansing, MI 48824, USA.

* Author for correspondence (e-mail: suesmith{at}nutrisci.wisc.edu)

Accepted 31 July 2008

In mouse, the establishment of left-right (LR) asymmetry requires intracellular calcium (Cai2+) enrichment on the left of the node. The use of Cai2+ asymmetry by other vertebrates, and its origins and relationship to other laterality effectors are largely unknown. Additionally, the architecture of Hensen's node raises doubts as to whether Cai2+ asymmetry is a broadly conserved mechanism to achieve laterality. We report here that the avian embryo uses a left-side enriched Cai2+ asymmetry across Hensen's node to govern its lateral identity. Elevated Cai2+ was first detected along the anterior node at early HH4, and its emergence and left-side enrichment by HH5 required both ryanodine receptor (RyR) activity and extracellular calcium, implicating calcium-induced calcium release (CICR) as the novel source of the Cai2+. Targeted manipulation of node Cai2+ randomized heart laterality and affected nodal expression. Bifurcation of the Cai2+ field by the emerging prechordal plate may permit the independent regulation of LR Cai2+ levels. To the left of the node, RyR/CICR and H+V-ATPase activity sustained elevated Cai2+. On the right, Cai2+ levels were actively repressed through the activities of H+K+ ATPase and serotonin-dependent signaling, thus identifying a novel mechanism for the known effects of serotonin on laterality. Vitamin A-deficient quail have a high incidence of situs inversus hearts and had a reversed calcium asymmetry. Thus, Cai2+ asymmetry across the node represents a more broadly conserved mechanism for laterality among amniotes than had been previously believed.

Key words: Chick embryo, Hensen's node, Intracellular calcium, Left-right asymmetry, Proton ATPases, Ratiometric calcium imaging, Retinoic acid, Ryanodine receptors, Serotonin


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Development 2008 135: e1902. [Full Text]  





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