Nature 362, 709 - 715 (22 April 1993); doi:10.1038/362709a0

Instability and decay of the primary structure of DNA

Tomas Lindahl

Imperial Cancer Research Fund, Clare Hall Laboratories, South Mimms. Hertfordshire EN6 3LD. UK.

Although DNA is the carrier of genetic information, it has limited chemical stability. Hydrolysis, oxidation and nonenzymatic methylation of DNA occur at significant ratesin vivo, and are counteracted by specific DNA repair processes. The spontaneous decay of DNA is likely to be a major factor in mutagenesis, carcinogenesis and ageing, and also sets limits for the recovery of DNA fragments from fossils.

References

1.	Ahern, T. J. & Klibanov, A. M. Science 228, 1280−1284 (1985). | PubMed | ISI | ChemPort |
2.	Kossiakoff, A. A. Science 240, 191−194 (1988). | PubMed | ChemPort |
3.	Lindahl, T. J. biol. Chem. 242, 1970−1973 (1967). | PubMed | ISI | ChemPort |
4.	Pace, N. R. Cell 65, 531−533 (1991). | Article | PubMed | ISI | ChemPort |
5.	Lindahl, T. & Nyberg, B. Biochemistry 11, 3610−3618 (1972) | Article | PubMed | ISI | ChemPort |
6.	Lindahl, T. & Karlström, O. Biochemistry 12, 5151−5154 (1973). | PubMed | ISI | ChemPort |
7.	Loeb, L. A. & Preston, B. D. A. Rev. Genet. 20, 201−230 (1986). | ChemPort |
8.	Lindahl, T. & Andersson, A. Biochemistry 11, 3618−3623 (1972). | Article | PubMed | ISI | ChemPort |
9.	Shapiro, R. in Chromosome Damage and Repair (eds Seeberg, E. & Kleppe, K.) 3−18 (Plenum, New York, 1981). | ChemPort |
10.	Doetsch, P. W. & Cunningham, R. P. Mutat. Res. 236, 173−201 (1990). | PubMed | ChemPort |
11.	Dianov, G., Price, A. & Lindahl, T. Molec. cell. Biol. 12, 1605−1612 (1992). | PubMed | ChemPort |
12.	Lindahl, T. & Nyberg, B. Biochemistry 13, 3405−3410 (1974) | Article | PubMed | ISI | ChemPort |
13.	Lindahl, T. Prog. Nucleic Acid Res. molec. Biol. 22, 135−192 (1979). | ChemPort |
14.	Ehrlich, M., Zhang, X-Y. & Inamdar, N. M. Mutat. Res. 238, 277−286 (1990). | PubMed | ChemPort |
15.	Frederico, L. A., Kunkel, T. A. & Shaw, B. R. Biochemistry 29, 2532−2537 (1990). | PubMed | ISI | ChemPort |
16.	Kricker, M. C. & Drake, J. W. J. Bact. 172, 3037−3039 (1990) | PubMed | ChemPort |
17.	Duncan, B. K., & Miller, J. H. Nature 287, 560−561 (1980). | Article | PubMed | ISI | ChemPort |
18.	Chen, J.-D. & Lacks, S. A. J. Bact. 173, 283−290 (1991). | PubMed | ChemPort |
19.	Impellizzeri, K. J., Anderson, B. & Burgers, P. M. J. J. Bact. 173, 6807−6810 (1991). | PubMed | ChemPort |
20.	Cooper, D. N. & Youssoufian, H. Hum. Genet. 78, 151−155 (1988). | Article | PubMed | ISI | ChemPort |
21.	Rideout, W. M. III, Coetzee, G. A., Olumi, A. F. & Jones, P. A. Science 249, 1288−1290 (1990). | PubMed | ISI | ChemPort |
22.	Selker, E. U. A. Rev. Genet 24, 579−613 (1990). | ChemPort |
23.	Shen, J.-C., Rideout, W. M. III, & Jones, P. A. Cell 71, 1073−1080 (1992). | PubMed | ISI | ChemPort |
24.	Perutz, M. F. J. molec. Biol. 213, 203−206 (1990). | PubMed | ChemPort |
25.	Karran, P. & Lindahl, T. Biochemistry 19, 6005−6011 (1980). | PubMed | ChemPort |
26.	Dianov, G. & Lindahl, T. Nucleic Acids Res. 19, 3829−3833 (1991). | PubMed | ISI | ChemPort |
27.	Hill-Perkins, M., Jones, M. D. & Karran, P. Mutat. Res. 162, 153−163 (1986). | PubMed | ChemPort |
28.	Wink, D. A. et al. Science 254, 1001−1003 (1991). | PubMed | ISI | ChemPort |
29.	Demple, B. A. Rev. Genet. 25, 315−337 (1991). | ChemPort |
30.	Kasai, H. & Nishimura, S. Nucleic Acids Res. 12, 2137−2145 (1984). | PubMed | ISI | ChemPort |
31.	Shibutani, S., Takeshita, M. & Grollman, A. Nature 349, 431−434 (1991). | Article | PubMed | ISI | ChemPort |
32.	Tchou, J. et al. Proc. natn. Acad. Sci. U.S.A. 88, 4690−4694 (1991). | ChemPort |
33.	Aruoma, O. I., Halliwell, B. & Dizdaroglu, M. J. biol. Chem. 264, 13024−13028 (1989). | PubMed | ChemPort |
34.	Michaels, M. L., Cruz, C., Grollman, A. P. & Miller, J. H. Proc. natn. Acad. Sci. U.S.A. 89, 7022−7025 (1992) | ChemPort |
35.	Maki, H. & Sekiguchi, M. Nature 355, 273−275 (1992). | Article | PubMed | ISI | ChemPort |
36.	Fraga, C. G., Shigenaga, M. K., Park, J.-W., Degan, P. & Ames, B. N. Proc. natn. Acad. Sci. U.S.A. 87, 4533−4537 (1990). | ChemPort |
37.	Wallace, S. S. Envir. molec. Mutag. 12, 431−477 (1988). | ChemPort |
38.	Breimer, L. H. Molec. Carcinog. 3, 188−197 (1990). | ChemPort |
39.	Kuo, C.-F. et al. Science 258, 434−440 (1992). | PubMed | ISI | ChemPort |
40.	Wagner, J. R., Hu, C.-C. & Ames, B. N. Proc natn. Acad. Sci. U.S.A. 89, 3380−3384 (1992). | ChemPort |
41.	Dirksen, M. L., Blakely, W. F., Holwitt, E. & Dizdaroglu, M. Int. J. Radiat. Biol. 54, 195−204 (1988). | PubMed | ChemPort |
42.	Carmichael, P. L., Shé, M. N. & Phillips, D. H. Carcinogenesis 13, 1127−1135 (1992). | PubMed | ChemPort |
43.	Szatrowski, T. P. & Nathan, C. F. Cancer Res. 51, 794−798 (1991). | PubMed | ISI | ChemPort |
44.	Mouret, J. F., Odin, F., Polverelli, M. & Cadet, J. Chem. Res. Toxicol. 3, 102−110 (1990). | PubMed | ChemPort |
45.	Joenje, H. Mutat. Res. 219, 193−208 (1989). | Article | PubMed | ISI | ChemPort |
46.	Ljungman, M. & Hanawalt, P. C. Molec. Carcinog. 5, 264−269 (1992). | ChemPort |
47.	Richter, C., Park, J.-W. & Ames, B. N. Proc. natn. Acad. Sci. U.S.A. 85, 6465−6467 (1988). | ChemPort |
48.	Wallace, D. C. et al. Science 242, 1427−1430 (1988). | PubMed | ISI | ChemPort |
49.	Linnane, A. W., Marzuki, S., Ozawa, T. & Tanaka, M. Lancet i, 642−645 (1989). | Article |
50.	Lutz, W. K. Mutat. Res. 238, 287−295 (1990). | PubMed | ChemPort |
51.	Paik, W. K., Lee, H. W. & Kim, S. FEBS Lett. 58, 39−42 (1975). | PubMed | ChemPort |
52.	Rydberg, B. & Lindahl, T. EMBO J. 1, 211−216 (1982). | PubMed | ISI | ChemPort |
53.	Barrows, L. R. & Magee, P. N. Carcinogenesis 3, 349−351 (1982). | PubMed | ChemPort |
54.	Park, J.-W. & Ames, B. N. Proc. natn. Acad. Sci. U.S.A. 85, 7467−7470; 85, 9508 (1988). | ChemPort |
55.	Rebeck, G. W. & Samson, L. J. Bact. 173, 2068−2076 (1991). | PubMed | ChemPort |
56.	Vaughan, P., Sedgwick, B., Hall, J., Gannon, J. & Lindahl, T. Carcinogenesis 12, 263−268 (1991). | PubMed | ISI | ChemPort |
57.	Kodama, M. & Saito, H. Cancer Lett. 10, 319−324 (1980). | PubMed | ChemPort |
58.	Bucala, R. P., Model, P. & Cerami, A. Proc. natn. Acad. Sci. U.S.A. 81, 105−109 (1984). | ChemPort |
59.	Lee, A. T. & Cerami, A. Proc. natn. Acad. Sci. U.S.A. 84, 8311−8314 (1987). | ChemPort |
60.	Setlow, P. J. Bact. 174, 2737−2741 (1992). | PubMed | ChemPort |
61.	Baross, J. A. & Deming, J. W. Nature 303, 423−426 (1983). | Article | ISI | ChemPort |
62.	Trent, J. D., Chastain, R. A. & Yayanos, A. A. Nature 307, 737−740 (1984). | Article | PubMed | ISI | ChemPort |
63.	Higuchi, R., Bowman, R., Friedberger, M., Ryder, O. A. & Wilson, A. C. Nature 312, 282−284 (1984). | Article | PubMed | ISI | ChemPort |
64.	Pääbo, S. Nature 314, 644−645 (1985). | Article | PubMed | ISI | ChemPort |
65.	Pääbo, S., Higuchi, R. G. & Wilson, A. C. J. biol. Chem. 264, 9709−9712 (1989). | PubMed | ISI | ChemPort |
66.	Hagelberg, E. & Clegg, J. B. Proc. R. Soc. B244, 45−50 (1991). | ChemPort |
67.	De Salle, R., Gatesy, J., Wheeler, W. & Grimaldi, D. Science 257, 1933−1936 (1992). | PubMed | ISI | ChemPort |
68.	Golenberg, E. M. et al. Nature 344, 656−658 (1990). | Article | PubMed | ISI | ChemPort |
69.	Sidow, A., Wilson, A. C. & Pääbo, S. Phil. Trans. R. Soc. B333, 429−433 (1991). | ChemPort |
70.	Smith, K. C. Mutat. Res. 277, 139−162 (1992). | PubMed | ChemPort |
71.	Schaaper, R. M. & Dunn, R. L. Genetics 129, 317−326 (1991) | PubMed | ISI | ChemPort |
72.	Oller, A. R. & Thilly, W. G. J. molec. Biol. 228, 813−826 (1992). | PubMed | ChemPort |
73.	Ramotar, D., Popoff, S. C., Gralla, E. B. & Demple, B. Molec. cell. Biol. 11, 4537−4544 (1991). | PubMed | ISI | ChemPort |
74.	Basu, A. K., Loechler, E. L., Leadon, S. A. & Essigmann, J. M. Proc. natn. Acad. Sci. U.S.A. 86, 7677−7681 (1989). | ChemPort |
75.	Klungland, A., Fairbairn, L., Watson, A. J., Margison, G. P. & Seeberg, E. EMBO J. 11, 4439−4444 (1992). | PubMed | ChemPort |
76.	Loeb, L. A. Cancer Res. 49, 5489−5496 (1989). | PubMed | ChemPort |
77.	Snowden, A., Kow, Y. W. & van Houten, B. Biochemistry 29, 7251−7259 (1990). | PubMed | ISI | ChemPort |
78.	Randerath, K., Leihr, J. G., Gladek, A. & Randerath, E. Mutat. Res. 219, 121−133 (1989). | PubMed | ChemPort |
79.	Cleaver, J. E. & Kraemer, K. H. in The Metabolic Basis of Inherited Disease 6th edn. (eds Scriver, C. R. et al.) 2949−2971 (McGraw-Hill, New York, 1989).
80.	Harley, C. B., Futcher, A. B. & Greider, C. W. Nature 345, 458−460 (1990). | Article | PubMed | ISI | ChemPort |
81.	McCarthy, T. V., Karran, P. & Lindahl, T. EMBO J. 3, 545−550 (1984). | PubMed | ISI | ChemPort |
82.	Lindahl, T. Nature 259, 64−66 (1976). | Article | PubMed | ISI | ChemPort |
83.	Saporito, S. M., Gedenk, M. & Cunningham, R. P. J. Bact. 171, 2542−2546 (1989). | PubMed | ChemPort |
84.	Satoh, M. S., Jones, C. J., Wood, R. D. & Lindahl, T. Proc. natn. Acad. Sci. U.S.A. (in the press).