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Molecular and Cellular Biology, July 2004, p. 6253-6267, Vol. 24, No. 14
0270-7306/04/$08.00+0     DOI: 10.1128/MCB.24.14.6253-6267.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Six1 and Eya1 Expression Can Reprogram Adult Muscle from the Slow-Twitch Phenotype into the Fast-Twitch Phenotype

Raphaelle Grifone,1 Christine Laclef,1 François Spitz,1,{dagger} Soledad Lopez,1 Josiane Demignon,1 Jacques-Emmanuel Guidotti,1 Kiyoshi Kawakami,2 Pin-Xian Xu,3 Robert Kelly,4 Basil J. Petrof,1,{ddagger} Dominique Daegelen,1 Jean-Paul Concordet,1 and Pascal Maire1*

Departement Génétique, Développement et Pathologie Moléculaire, Institut Cochin-INSERM 567, CNRS UMR 8104, Université Paris V, 75014 Paris,1 Pasteur Institute, 75015 Paris, France,4 Department of Biology, Jichi Medical School, Minamikawachi, Kawachi, Tochigi 329-0498, Japan,2 McLaughlin Research Institute for Biomedical Sciences, Great Falls, Montana 594053

Received 17 December 2003/ Returned for modification 4 February 2004/ Accepted 26 April 2004

Muscle fibers show great differences in their contractile and metabolic properties. This diversity enables skeletal muscles to fulfill and adapt to different tasks. In this report, we show that the Six/Eya pathway is implicated in the establishment and maintenance of the fast-twitch skeletal muscle phenotype. We demonstrate that the MEF3/Six DNA binding element present in the aldolase A pM promoter mediates the high level of activation of this promoter in fast-twitch glycolytic (but not in slow-twitch) muscle fibers. We also show that among the Six and Eya gene products expressed in mouse skeletal muscle, Six1 and Eya1 proteins accumulate preferentially in the nuclei of fast-twitch muscles. The forced expression of Six1 and Eya1 together in the slow-twitch soleus muscle induced a fiber-type transition characterized by the replacement of myosin heavy chain I and IIA isoforms by the faster IIB and/or IIX isoforms, the activation of fast-twitch fiber-specific genes, and a switch toward glycolytic metabolism. Collectively, these data identify Six1 and Eya1 as the first transcriptional complex that is able to reprogram adult slow-twitch oxidative fibers toward a fast-twitch glycolytic phenotype.

* Corresponding author. Mailing address: Departement Génétique, Développement et Pathologie Moléculaire, Institut Cochin-INSERM 567, CNRS UMR 8104, Université Paris V, 24 Rue du Faubourg Saint Jacques, 75014 Paris, France. Phone: 33 1 44 41 24 16. Fax: 33 1 44 41 24 21. E-mail: maire{at}mail.cochin.inserm.fr.

{dagger} Present address: Department of Zoology and Animal Biology, University of Geneva-Sciences III, 1211 Geneva 4, Switzerland.

{ddagger} Present address: Respiratory Division and Meakins-Christie Laboratories, McGill University Health Center, Montreal, Quebec, Canada.

Molecular and Cellular Biology, July 2004, p. 6253-6267, Vol. 24, No. 14
0022-538X/04/$08.00+0     DOI: 10.1128/MCB.24.14.6253-6267.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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