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Epigenetics & Chromatin
Open Access
Research
Both telomeric and non-telomeric DNA damage are determinants
of mammalian cellular senescence
Asako J Nakamura*
1
, Y Jeffrey Chiang
2
, Karen S Hathcock
2
,
Izumi Horikawa
3
, Olga A Sedelnikova
1
, Richard J Hodes
2,4
and
William M Bonner*
1
Address:
1
Laboratory of Molecular Pharmacology, National Cancer Institute, National Institutes of Health, Rockville Pike, Bethesda, MD 20892,
USA,
2
Experimental Immunology Branch, National Cancer Institute, National Institutes of Health, Rockville Pike, Bethesda, MD 20892, USA,
3
Laboratory of Biosystems and Cancer, National Cancer Institute, National Institutes of Health, Rockville Pike, Bethesda, MD 20892, USA and
4
National Institute on Aging, National Institutes of Health, Rockville Pike, Bethesda MD 20892, USA
Email: Asako J Nakamura* - nakamuraa@mail.nih.gov; Y Jeffrey Chiang - chiangj@mail.nih.gov;
Karen S Hathcock - hathcock@exchange.nih.gov; Izumi Horikawa - horikawi@mail.nih.gov; Olga A Sedelnikova - SedelniO@mail.nih.gov;
Richard J Hodes - hodesr@31.nia.nih.gov; William M Bonner* - bonnerw@mail.nih.gov
* Corresponding authors
Abstract
Background: Cellular senescence is a state reached by normal mammalian cells after a finite number of
cell divisions and is characterized by morphological and physiological changes including terminal cell-cycle
arrest. The limits on cell division imposed by senescence may play an important role in both organismal
aging and in preventing tumorigenesis. Cellular senescence and organismal aging are both accompanied by
increased DNA damage, seen as the formation of γ-H2AX foci (γ-foci), which may be found on uncapped
telomeres or at non-telomeric sites of DNA damage. However, the relative importance of telomere- and
non-telomere-associated DNA damage to inducing senescence has never been demonstrated. Here we
present a new approach to determine accurately the chromosomal location of γ-foci and quantify the
number of telomeric versus non-telomeric γ-foci associated with senescence in both human and mouse
cells. This approach enables researchers to obtain accurate values and to avoid various possible
misestimates inherent in earlier methods.
Results: Using combined immunofluorescence and telomere fluorescence in situ hybridization on
metaphase chromosomes, we show that human cellular senescence is not solely determined by telomeric
DNA damage. In addition, mouse cellular senescence is not solely determined by non-telomeric DNA
damage. By comparing cells from different generations of telomerase-null mice with human cells, we show
that cells from late generation telomerase-null mice, which have substantially short telomeres, contain
mostly telomeric γ-foci. Most notably, we report that, as human and mouse cells approach senescence, all
cells exhibit similar numbers of total γ-foci per cell, irrespective of chromosomal locations.
Conclusion: Our results suggest that the chromosome location of senescence-related γ-foci is
determined by the telomere length rather than species differences per se. In addition, our data indicate
that both telomeric and non-telomeric DNA damage responses play equivalent roles in signaling the
initiation of cellular senescence and organismal aging. These data have important implications in the study
of mechanisms to induce or delay cellular senescence in different species.
Published: 3 November 2008
Epigenetics & Chromatin 2008, 1:6 doi:10.1186/1756-8935-1-6
Received: 25 June 2008
Accepted: 3 November 2008
This article is available from: http://www.epigeneticsandchromatin.com/content/1/1/6
© 2008 Nakamura et al; licensee BioMed Central Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0 ),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.