Significant correlation of species longevity with DNA double strand break recognition but not with telomere length

Mechanisms of Ageing and Development

Volumn 130, Issue 11-12, 2009, Pages 784-792

  Lorenzini, Antonello ^a   Johnson, F Brad ^c   Oliver, Anthony ^d   Tresini, Maria ^d   Smith, Jasmine S ^c   Hdeib, Mona ^c   Sell, Christian ^b   Cristofalo, Vincent J ^d   Stamato, Thomas D ^d  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b Laboratory Medicine   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d LANKENAU INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

DNA double strand break repair; DNA end binding activity; Ku protein; Species life span; Telomere length

Indexed keywords

GENOMIC DNA; KU ANTIGEN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; COW; DNA BINDING; DOUBLE STRANDED DNA BREAK; EMBRYO; HUMAN; HUMAN CELL; LONGEVITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; SKIN FIBROBLAST; SPECIES DIFFERENCE; TELOMERE;

ADULT; AGING; ANIMALS; CATS; CATTLE; CHIROPTERA; CHO CELLS; CRICETINAE; CRICETULUS; DNA; DNA DAMAGE; DOGS; EMBRYO, MAMMALIAN; FIBROBLASTS; GORILLA GORILLA; HELA CELLS; HORSES; HUMANS; LONGEVITY; LUNG; MACACA MULATTA; MALE; MICE; NUCLEAR PROTEINS; RABBITS; SKIN; SPECIES SPECIFICITY; TELOMERE;

MAMMALIA;

EID: 72149095996     PISSN: 00476374     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mad.2009.10.004     Document Type: Article

References (50)

1. Adkins R.M., Walton A.H., and Honeycutt R.L. Higher-level systematics of rodents and divergence time estimates based on two congruent nuclear genes. Mol. Phylogenet. Evol. 26 (2003) 409-420
2. Argyle D., Ellsmore V., Gault E.A., Munro A.F., and Nasir L. Equine telomeres and telomerase in cellular immortalisation and ageing. Mech. Ageing Dev. 124 (2003) 759-764
3. Austad S.N. Why We Age (1997), John Wiley & Sons, Inc., New York, NY pp. 140-145
4. Blier P.R., Griffith A.J., Craft J., and Hardin J.A. Binding of Ku protein to DNA. Measurement of affinity for ends and demonstration of binding to nicks. J. Biol. Chem. 268 (1993) 7594-7601
5. Bryans M., Valenzano M.C., and Stamato T.D. Absence of DNA ligase IV protein in XR-1 cells: evidence for stabilization by XRCC4. Mutat. Res. 433 (1999) 53-58
6. Busuttil R.A., Rubio M., Dolle M.E., Campisi J., and Vijg J. Oxygen accelerates the accumulation of mutations during the senescence and immortalization of murine cells in culture. Aging Cell 2 (2003) 287-294
7. Cherif H., Tarry J.L., Ozanne S.E., and Hales C.N. Ageing and telomeres: a study into organ- and gender-specific telomere shortening. Nucleic Acids Res. 31 (2003) 1576-1583
8. Cristofalo V.J., and Charpentier R. A standard procedure for cultivating human diploid fibroblastlike cells to study cellular aging. J. Tissue Cult. Methods 6 (1980) 117-121
9. Denko N., Giaccia A., Peters B., and Stamato T.D. An asymmetric field inversion gel electrophoresis method for the separation of large DNA molecules. Anal. Biochem. 178 (1989) 172-176
10. Dignam J., Lebovitz R., and Roeder R. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11 (1983) 1475-1489
11. Dip R., and Naegeli H. More than just strand breaks: the recognition of structural DNA discontinuities by DNA-dependent protein kinase catalytic subunit. Faseb J. 19 (2005) 704-715
12. Downs J.A., and Jackson S.P. A means to a DNA end: the many roles of Ku. Nat. Rev. Mol. Cell. Biol. 5 (2004) 367-378
13. Evans H.H., Ricanati M., Horng M.F., Jiang Q., Mencl J., and Olive P. DNA double-strand break rejoining deficiency in TK6 and other human B-lymphoblast cell lines. Radiat. Res. 134 (1993) 307-315
14. Falzon M., Fewell J.W., and Kuff E.L. EBP-80, a transcription factor closely resembling the human autoantigen Ku, recognizes single- to double-strand transitions in DNA. J. Biol. Chem. 268 (1993) 10546-10552
15. Fattah K.R., Ruis B.L., and Hendrickson E.A. Mutations to Ku reveal differences in human somatic cell lines. DNA Repair (Amst.) 7 (2008) 762-774
16. Felsenstein J. Phylogenies and the comparative method. Am. Nat. 125 (1985) 1-15
17. Finnie N.J., Gottlieb T.M., Blunt T., Jeggo P.A., and Jackson S.P. DNA-dependent protein kinase activity is absent in xrs-6 cells: implications for site-specific recombination and DNA double-strand break repair. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 320-324
18. Flentje M., Asadpour B., Latz D., and Weber K.J. Sensitivity of neutral filter elution but not PFGE can be modified by non-dsb chromatin damage. Int. J. Radiat. Biol. 63 (1993) 715-724
19. Garland Jr. T., Bennett A.F., and Rezende E.L. Phylogenetic approaches in comparative physiology. J. Exp. Biol. 208 (2005) 3015-3035
20. Gauter B., Zlobinskaya O., and Weber K.J. Rejoining of radiation-induced DNA double-strand breaks: pulsed-field electrophoresis analysis of fragment size distributions after incubation for repair. Radiat. Res. 157 (2002) 721-733
21. Getts R.C., and Stamato T.D. Absence of a Ku-like DNA end binding activity in the xrs double-strand DNA repair-deficient mutant. J. Biol. Chem. 269 (1994) 15981-15984
22. Herbig U., Ferreira M., Condel L., Carey D., and Sedivy J.M. Cellular senescence in aging primates. Science 311 (2006) 1257
23. Jaco I., Munoz P., and Blasco M.A. Role of human Ku86 in telomere length maintenance and telomere capping. Cancer Res. 64 (2004) 7271-7278
24. Kozik A., Bradbury E.M., and Zalensky A. Increased telomere size in sperm cells of mammals with long terminal (TTAGGG)n arrays. Mol. Reprod. Dev. 51 (1998) 98-104
25. Lee S.E., Pellicioli A., Vaze M.B., Sugawara N., Malkova A., Foiani M., and Haber J.E. Yeast Rad52 and Rad51 recombination proteins define a second pathway of DNA damage assessment in response to a single double-strand break. Mol. Cell. Biol. 23 (2003) 8913-8923
26. Lees-Miller S.P., Sakaguchi K., Ullrich S.J., Appella E., and Anderson C.W. Human DNA-activated protein kinase phosphorylates serines 15 and 37 in the amino-terminal transactivation domain of human p53. Mol. Cell. Biol. 12 (1992) 5041-5049
27. Li G., Nelsen C., and Hendrickson E.A. Ku86 is essential in human somatic cells. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 832-837
28. Lieber M.R., Ma Y., Pannicke U., and Schwarz K. Mechanism and regulation of human non-homologous DNA end-joining. Nat. Rev. Mol. Cell. Biol. 4 (2003) 712-720
29. Lorenzini A., Tresini M., Austad S.N., and Cristofalo V.J. Cellular replicative capacity correlates primarily with species body mass not longevity. Mech. Ageing Dev. 126 (2005) 1130-1133
30. Marangoni E., Le Romancer M., Foray N., Muller C., Douc-Rasy S., Vaganay S., Abdulkarim B., Barrois M., Calsou P., Bernier J., Salles B., and Bourhis J. Transfer of Ku86 RNA antisense decreases the radioresistance of human fibroblasts. Cancer Gene Ther. 7 (2000) 339-346
31. Martin G.M., Ogburn C.E., Colgin L.M., Gown A.M., Edland S.D., and Monnat Jr. R.J. Somatic mutations are frequent and increase with age in human kidney epithelial cells. Hum. Mol. Genet. 5 (1996) 215-221
32. Matheu A., Maraver A., Klatt P., Flores I., Garcia-Cao I., Borras C., Flores J.M., Vina J., Blasco M.A., and Serrano M. Delayed ageing through damage protection by the Arf/p53 pathway. Nature 448 (2007) 375-379
33. Mauldin S.K., Getts R.C., Liu W., and Stamato T.D. DNA-PK-dependent binding of DNA ends to plasmids containing nuclear matrix attachment region DNA sequences: evidence for assembly of a repair complex. Nucleic Acids Res. 30 (2002) 4075-4087
34. McKevitt T.P., Nasir L., Wallis C.V., and Argyle D.J. A cohort study of telomere and telomerase biology in cats. Am. J. Vet. Res. 64 (2003) 1496-1499
35. Morozov V.E., Falzon M., Anderson C.W., and Kuff E.L. DNA-dependent protein kinase is activated by nicks and larger single-stranded gaps. J. Biol. Chem. 269 (1994) 16684-16688
36. Murphy W.J., Eizirik E., O'Brien S.J., Madsen O., Scally M., Douady C.J., Teeling E., Ryder O.A., Stanhope M.J., de Jong W.W., and Springer M.S. Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294 (2001) 2348-2351
37. Nasir L., Devlin P., McKevitt T., Rutteman G., and Argyle D.J. Telomere lengths and telomerase activity in dog tissues: a potential model system to study human telomere and telomerase biology. Neoplasia 3 (2001) 351-359
38. Olive P.L., Banath J.P., and MacPhail H.S. Lack of a correlation between radiosensitivity and DNA double-strand break induction or rejoining in six human tumor cell lines. Cancer Res. 54 (1994) 3939-3946
39. Parrinello S., Samper E., Krtolica A., Goldstein J., Melov S., and Campisi J. Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat. Cell. Biol. 5 (2003) 741-747
40. Purvis A., and Rambaut A. Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Comput. Appl. Biosci. 11 (1995) 247-251
41. Rohme D. Evidence for a relationship between longevity of mammalian species and life spans of normal fibroblasts in vitro and erythrocytes in vivo. Proc. Natl. Acad. Sci. U.S.A. 78 (1981) 5009-5013
42. Ruis B.L., Fattah K.R., and Hendrickson E.A. The catalytic subunit of DNA-dependent protein kinase regulates proliferation, telomere length, and genomic stability in human somatic cells. Mol. Cell. Biol. 28 (2008) 6182-6195
43. Speakman J.R. Correlations between physiology and lifespan--two widely ignored problems with comparative studies. Aging Cell 4 (2005) 167-175
44. Stamato T., Guerriero S., and Denko N. Two methods for assaying DNA double-strand break repair in mammalian cells by asymmetric field inversion gel electrophoresis. Radiat. Res. 133 (1993) 60-66
45. Stamato T.D., and Denko N. Asymmetric field inversion gel electrophoresis: a new method for detecting DNA double-strand breaks in mammalian cells. Radiat. Res. 121 (1990) 196-205
46. Steinert S., White D.M., Zou Y., Shay J.W., and Wright W.E. Telomere biology and cellular aging in nonhuman primate cells. Exp. Cell. Res. 272 (2002) 146-152
47. Tuteja N., Tuteja R., Ochem A., Taneja P., Huang N.W., Simoncsits A., Susic S., Rahman K., Marusic L., Chen J., et al. Human DNA helicase II: a novel DNA unwinding enzyme identified as the Ku autoantigen. Embo J. 13 (1994) 4991-5001
48. Uegaki K., Adachi N., So S., Iiizumi S., and Koyama H. Heterozygous inactivation of human Ku70/Ku86 heterodimer does not affect cell growth, double-strand break repair, or genome integrity. DNA Repair (Amst.) 5 (2006) 303-311
49. Wang J., Chou C.H., Blankson J., Satoh M., Knuth M.W., Eisenberg R.A., Pisetsky D.S., and Reeves W.H. Murine monoclonal antibodies specific for conserved and non-conserved antigenic determinants of the human and murine Ku autoantigens. Mol. Biol. Rep. 18 (1993) 15-28
50. Wang Y., Ghosh G., and Hendrickson E.A. Ku86 represses lethal telomere deletion events in human somatic cells. Proc. Natl. Acad. Sci. U.S.A. 106 (2009) 12430-12435