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J. Biol. Chem., Vol. 279, Issue 45, 46826-46834, November 5, 2004

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YY1 Regulates the Neural Crest-associated slug Gene in Xenopus laevis^*

Matthew J. Morgan, Joost M. Woltering¶, Paul M. J. In der Rieden¶, Antony J. Durston¶, and Jean Paul Thiery

From the Institut Curie-CNRS UMR144, Morphogénèse Cellulaire et Progression Tumorale, 26 Rue d'Ulm, 75248 Paris Cedex 05, France and ^¶Hubrecht Laboratory, Netherlands Institute for Developmental Biology, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands

slug gene expression is associated with the specification and migration of neural crest cells in the African clawed frog Xenopus laevis. We provide evidence that the protein Ying-Yang 1 (YY1) regulates the slug gene expression both indirectly and directly, via a YY1 cis-element in the slug promoter, during Xenopus development. The ability of the YY1 to bind this YY1 cis-element was confirmed by electromobility shift assays and reporter assays. YY1 was detected in the nuclei of ectodermal cells contemporaneously with the process of neural crest specification. The injection of anti-YY1 morpholino, which targeted both YY1 and YY1 gene products, depleted YY1 expression below 20% and was lethal at gastrulation. Sublethal depletion of YY1 reduced the length of the anterior-posterior axis and severely inhibited the expression of the neural marker Nrp1 and of the slug gene. Overexpression of YY1 or mutation of the YY1 cis-element reduced the restricted spatial expression of the slug reporter gene in the neural ectoderm border and provoked its expression in the nonneural ectoderm. Chromatin immunoprecipitation indicated that endogenous YY1 interacts directly with the YY1 cis-element of the endogenous slug gene and with the slug gene reporter sequence injected into embryos. The results suggest that YY1 is essential for Xenopus development; is necessary for neural ectoderm differentiation, a prerequisite for neural crest specification; and restricts which cells can form neural crest mesenchyme through directly blocking slug gene activity.

Received for publication, June 2, 2004 , and in revised form, August 19, 2004.

^* This work was supported by the European Union Framework V program for finance. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence should be addressed. Tel.: 33-1-42-34-63-38; Fax: 33-1-42-34-63-49; E-mail: matthew.morgan{at}curie.fr.

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