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A hallmark of mitosis is the appearance of high levels of histone phosphorylation, yet the roles of these modifications remain largely unknown. Here, we demonstrate that histone H3 phosphorylated at threonine 3 is directly recognized by an evolutionarily conserved binding pocket in the BIR domain of Survivin, which is a member of the chromosomal passenger complex (CPC). This binding mediates recruitment of the CPC to chromosomes and the resulting activation of its kinase subunit Aurora B. Consistently, modulation of the kinase activity of Haspin, which phosphorylates H3T3, leads to defects in the Aurora B-dependent processes of spindle assembly and inhibition of nuclear reformation. These findings establish a direct cellular role for mitotic histone H3T3 phosphorylation, which is read and translated by the CPC to ensure accurate cell division.
Adams,
INCENP binds the Aurora-related kinase AIRK2 and is required to target it to chromosomes, the central spindle and cleavage furrow.
2000, Pubmed,
Xenbase
Adams,
INCENP binds the Aurora-related kinase AIRK2 and is required to target it to chromosomes, the central spindle and cleavage furrow.
2000,
Pubmed
,
Xenbase
Cao,
Survivin mutant (Surv-DD70, 71AA) disrupts the interaction of Survivin with Aurora B and causes multinucleation in HeLa cells.
2006,
Pubmed
Crosio,
Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian Aurora kinases.
2002,
Pubmed
Dai,
The kinase haspin is required for mitotic histone H3 Thr 3 phosphorylation and normal metaphase chromosome alignment.
2005,
Pubmed
Jeyaprakash,
Structure of a Survivin-Borealin-INCENP core complex reveals how chromosomal passengers travel together.
2007,
Pubmed
Kelly,
Chromosomal enrichment and activation of the aurora B pathway are coupled to spatially regulate spindle assembly.
2007,
Pubmed
,
Xenbase
Liu,
Structural basis for binding of Smac/DIABLO to the XIAP BIR3 domain.
,
Pubmed
Markaki,
Phosphorylation of histone H3 at Thr3 is part of a combinatorial pattern that marks and configures mitotic chromatin.
2009,
Pubmed
Musacchio,
Molecular biology. Surfing chromosomes (and Survivin).
2010,
Pubmed
Polioudaki,
Mitotic phosphorylation of histone H3 at threonine 3.
2004,
Pubmed
Ramadan,
Cdc48/p97 promotes reformation of the nucleus by extracting the kinase Aurora B from chromatin.
2007,
Pubmed
,
Xenbase
Rosasco-Nitcher,
Centromeric Aurora-B activation requires TD-60, microtubules, and substrate priming phosphorylation.
2008,
Pubmed
,
Xenbase
Ruchaud,
Chromosomal passengers: conducting cell division.
2007,
Pubmed
Sampath,
The chromosomal passenger complex is required for chromatin-induced microtubule stabilization and spindle assembly.
2004,
Pubmed
,
Xenbase
Sessa,
Mechanism of Aurora B activation by INCENP and inhibition by hesperadin.
2005,
Pubmed
,
Xenbase
Shiozaki,
Mechanism of XIAP-mediated inhibition of caspase-9.
2003,
Pubmed
Sun,
Solution structure of human survivin and its binding interface with Smac/Diablo.
2005,
Pubmed
Ubersax,
Mechanisms of specificity in protein phosphorylation.
2007,
Pubmed
Wu,
Structural basis of IAP recognition by Smac/DIABLO.
,
Pubmed
Yue,
Deconstructing Survivin: comprehensive genetic analysis of Survivin function by conditional knockout in a vertebrate cell line.
2008,
Pubmed
