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Molecular and Cellular Biology, February 2002, p. 874-885, Vol. 22, No. 3
0270-7306/01/$04.00+0     DOI: 10.1128/MCB.22.3.874-885.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Mitotic Phosphorylation of Histone H3: Spatio-Temporal Regulation by Mammalian Aurora Kinases

Claudia Crosio,1 Gian Maria Fimia,1,{dagger} Romain Loury,1 Masashi Kimura,2 Yukio Okano,2 Hongyi Zhou,3 Subrata Sen,3 C. David Allis,4 and Paolo Sassone-Corsi1*

Institut de Génétique et de Biologie Moléculaire et Cellulaire, CNRS-INSERM-Université Louis Pasteur, 67404 Illkirch-Strasbourg, France,1 Department of Molecular Pathobiochemistry, Gifu University School of Medicine, Gifu 500-8705, Japan,2 Division of Pathology & Laboratory Medicine, The University of Texas M. D. Anderson Cancer Center, Houston, Texas 77030,3 Department of Biochemistry and Molecular Genetics, University of Virginia H.S.C., Charlottesville, Virginia 229084

Received 18 July 2001/ Returned for modification 7 September 2001/ Accepted 29 October 2001

Phosphorylation at a highly conserved serine residue (Ser-10) in the histone H3 tail is considered to be a crucial event for the onset of mitosis. This modification appears early in the G2 phase within pericentromeric heterochromatin and spreads in an ordered fashion coincident with mitotic chromosome condensation. Mutation of Ser-10 is essential in Tetrahymena, since it results in abnormal chromosome segregation and extensive chromosome loss during mitosis and meiosis, establishing a strong link between signaling and chromosome dynamics. Although mitotic H3 phosphorylation has been long recognized, the transduction routes and the identity of the protein kinases involved have been elusive. Here we show that the expression of Aurora-A and Aurora-B, two kinases of the Aurora/AIK family, is tightly coordinated with H3 phosphorylation during the G2/M transition. During the G2 phase, the Aurora-A kinase is coexpressed while the Aurora-B kinase colocalizes with phosphorylated histone H3. At prophase and metaphase, Aurora-A is highly localized in the centrosomic region and in the spindle poles while Aurora-B is present in the centromeric region concurrent with H3 phosphorylation, to then translocate by cytokinesis to the midbody region. Both Aurora-A and Aurora-B proteins physically interact with the H3 tail and efficiently phosphorylate Ser10 both in vitro and in vivo, even if Aurora-A appears to be a better H3 kinase than Aurora-B. Since Aurora-A and Aurora-B are known to be overexpressed in a variety of human cancers, our findings provide an attractive link between cell transformation, chromatin modifications and a specific kinase system.

* Corresponding author. Mailing address: Institut de Génétique et de Biologie Moléculaire et Cellulaire, CNRS-INSERM-Université Louis Pasteur, 1 rue Laurent Fries, 67404 Illkirch-Strasbourg, France. Phone: 33 388 653410. Fax: 33 388 653246. E-mail: paolosc{at}igbmc.u-strasbg.fr.

{dagger} Present address: National Institute for Infectious Diseases, IRCCS, L. Spallanzani, 00149 Rome, Italy.

Molecular and Cellular Biology, February 2002, p. 874-885, Vol. 22, No. 3
0022-538X/01/$04.00+0     DOI: 10.1128/MCB.22.3.874-885.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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