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J. Biol. Chem., Vol. 280, Issue 4, 2847-2856, January 28, 2005
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Degradation of MyoD Mediated by the SCF (MAFbx) Ubiquitin Ligase*
¶¶**
From the
Laboratoire de Génomique Fonctionnelle et Myogénèse, UMR866 Différenciation Cellulaire et Croissance, INRA UM II, Campus INRA/ENSA, 2 Place Pierre Viala, 34060, Montpellier, Cedex 1, France and the ||Institut Jacques Monod, UMR 7592 CNRS, 75251 Paris, France
MyoD controls myoblast identity and differentiation and is required for myogenic stem cell function in adult skeletal muscle. MyoD is degraded by the ubiquitin-proteasome pathway mediated by different E3 ubiquitin ligases not identified as yet. Here we report that MyoD interacts with Atrogin-1/MAFbx (MAFbx), a striated muscle-specific E3 ubiquitin ligase dramatically up-regulated in atrophying muscle. A core LXXLL motif sequence in MyoD is necessary for binding to MAFbx. MAFbx associates with MyoD through an inverted LXXLL motif located in a series of helical leucine-charged residue-rich domains. Mutation in the LXXLL core motif represses ubiquitination and degradation of MyoD induced by MAFbx. Overexpression of MAFbx suppresses MyoD-induced differentiation and inhibits myotube formation. Finally the purified recombinant SCFMAFbx complex (SCF, Skp1, Cdc53/Cullin 1, F-box protein) mediated MyoD ubiquitination in vitro in a lysine-dependent pathway. Mutation of the lysine 133 in MyoD prevented its ubiquitination by the recombinant SCFMAFbx complex. These observations thus demonstrated that MAFbx functions in ubiquitinating MyoD via a sequence found in transcriptional coactivators. These transcriptional coactivators mediate the binding to liganded nuclear receptors. We also identified a novel protein-protein interaction module not yet identified in F-box proteins. MAFbx may play an important role in the course of muscle differentiation by determining the abundance of MyoD.
Received for publication, October 5, 2004 , and in revised form, October 28, 2004.
* This work was supported in part by grants from Association Française contre les myophaties (AFM), Ligue Nationale contre le Cancer, l'Association pour le Recherche contre le Cancer (ARC), and INRA. 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.
The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. 1-3.
Present address: Growth Control Laboratory, FMI, Maulbeerstrasse 66, 4058, Basel, Switzerland.
¶ Fellows of Ministère de la Recherche et de la Technologie (MRT).
** To whom correspondence should be addressed. Tel.: 33-04-99-61-29-76; Fax: 33-04-67-54-56-94; E-mail: serge.leibovitch{at}ensam.inra.fr.
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