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Originally published In Press as doi:10.1074/jbc.M109219200 on January 25, 2002

J. Biol. Chem., Vol. 277, Issue 14, 12001-12008, April 5, 2002
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Apoptotic Release of Histones from Nucleosomes*

Dongcheng WuDagger , Alistair IngramDagger §, Jill H. Lahti, Brie MazzaDagger , Jose Grenet, Anil KapoorDagger ||, Lieqi LiuDagger , Vincent J. Kidd, and Damu TangDagger §**

From the § Department of Medicine and || Department of Surgery, McMaster University, and Dagger  Father Sean O'Sullivan Research Institute, St. Joseph's Hospital, Hamilton, Ontario L8N 1Y2, Canada and the  Department of Tumor Cell Biology, St. Jude Children's Research Hospital, Memphis, Tennessee 38105

Chromatin structure is influenced by histone modification, and this may help direct chromatin behavior to facilitate transcription, DNA replication, and DNA repair. Chromatin condensation and DNA fragmentation are the classic nuclear features but remain poorly characterized. It is highly probable that nucleosomal structure must be altered to allow these features to become apparent, but data to support this construct are lacking. We report here that in response to apoptotic signals from a death receptor (CD95 and tumor necrosis factor-alpha ) or mitochondrial (staurosporine) apoptotic stimulus, the core nucleosomal histones H2A, H2B, H3, and H4 become separated from DNA during apoptosis in Jurkat and HeLa cells and are consequently detectable in the cell lysate prepared using a non-ionic detergent. The timing of this histone release from DNA correlates well with the progression of apoptosis. We also show expression of a caspase cleavage-resistant form of ICAD (ICAD-DM) in Jurkat and HeLa cells abolished DNA fragmentation and also dramatically reduced histone release in apoptotic cells. However, we demonstrate that apoptotic histone release is not an inevitable consequence of CAD/DFF-40-mediated DNA destruction as DNA fragmentation but not histone release occurs efficiently in tumor necrosis factor-alpha - and etoposide-treated NIH3T3 cells. Furthermore, in an in vitro apoptotic assay, incubation of apoptotic Jurkat cellular extract with non-apoptotic Jurkat nuclei led to nuclear DNA fragmentation without obvious histone release. Taken together, these data demonstrate that CAD/DFF-40 functions indirectly in mediating nucleosomal destruction during apoptosis.

* This work was supported partially by a grant from the Father Sean O'Sullivan Research Foundation and a grant from the Kidney Foundation of Canada (to D. T.), by a grant from the Kidney Foundation of Canada (to A. I.), by the Prostate Research Foundation of Canada (to D. T.), by the American Lebanese Syrian Associated Charities (ALSAC), and by National Institutes of Health Grant CA67938 (to V. J. K.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

** To whom correspondence should be addressed: 708-25 Charlton Ave. East, Hamilton, Ontario L8N 1Y2, Canada. Tel.: 905-521-6151; Fax: 905-521-6153; E-mail: damut@mcmaster.ca.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.


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