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First published online 23 January 2003
doi: 10.1242/jcs.00330


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Journal of Cell Science 116, 961-974 (2003)
doi: 10.1242/jcs.00330


Research Article

Dynamic relocalization of the chromosomal passenger complex proteins inner centromere protein (INCENP) and aurora-B kinase during male mouse meiosis

María Teresa Parra1, Alberto Viera1, Rocío Gómez1, Jesús Page1, Mar Carmena2, William C. Earnshaw2, Julio S. Rufas1 and José A. Suja1,*

1 Departamento de Biología, Edificio de Biológicas, Universidad Autónoma de Madrid, E-28049 Madrid, Spain
2 Institute of Cell and Molecular Biology, University of Edinburgh, Swann Building, King's Buildings, Mayfield Road, Edinburgh EH9 3JR, Scotland, UK

* Author for correspondence (e-mail: jose.suja{at}uam.es)

Accepted 18 December 2002

INCENP and aurora-B kinase are two chromosomal passenger proteins that are thought to play key roles in coordinating chromosome segregation with cytokinesis in somatic cells. Here we have analyzed their subcellular distribution, and that of phosphorylated histone H3, and the timing of their relative appearance in mouse spermatocytes during both meiotic divisions. Our results show that in mitotic spermatogonial cells, INCENP and aurora-B show the same pattern of distribution as they do in cultured somatic cells. INCENP labels the synaptonemal complex central element from zygotene up to late pachytene when it begins to relocalize to heterochromatic chromocentres. Aurora-B first appears at chromocentres in late diplotene before the initial phosphorylation of histone H3. INCENP and aurora-B concentrate at centromeres during diakinesis and appear during metaphase I as T-shaped signals at their inner domains, just below associated sister kinetochores. During late anaphase I both proteins relocalize to the spindle midzone. Both proteins colocalize at a connecting strand traversing the centromere region and joining sister kinetochores, in metaphase II centromeres. This strand disappears at the metaphase II/anaphase II transition and relocalizes to the spindle midzone. We discuss the complex dynamic relocalization of the chromosomal passenger complex during prophase I. Additionally, we suggest that this complex may regulate sister-chromatid centromere cohesion during both meiotic divisions.

Key words: INCENP, Aurora-B kinase, Phosphorylated histone H3, Meiosis, Centromere, Sister-chromatid cohesion




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