Cancer chemoprevention by the antioxidant tempol in Atm-deficient mice

Human Molecular Genetics

Volumn 13, Issue 16, 2004, Pages 1793-1802

  Schubert, Ralf ^a,b   Erker, Laura ^a,b   Barlow, Carrolee ^c,e   Yakushiji, Hiroyuki ^a,b,f   Larson, Denise ^c   Russo, Angelo ^d   Mitchell, James B ^d   Wynshaw Boris, Anthony ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e MERCK RESEARCH LABORATORIES   (United States)

^f Taku Hospital   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; ANTIOXIDANT; ATM PROTEIN; NITROXIDE DERIVATIVE; REACTIVE OXYGEN METABOLITE; TEMPOL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; ATAXIA TELANGIECTASIA; CANCER; CANCER PREVENTION; CANCER SUSCEPTIBILITY; CHEMOPROPHYLAXIS; CONTINUOUS INFUSION; CONTROLLED STUDY; FEMALE; FOOD INTAKE; LIFESPAN; MALE; MEMBRANE POTENTIAL; METABOLIC RATE; MITOCHONDRIAL MEMBRANE; MOUSE; MOUSE MUTANT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEFICIENCY; THYMUS LYMPHOMA; TISSUE INJURY; WEANING; WEIGHT GAIN;

ANIMALS; ANTIOXIDANTS; ATAXIA TELANGIECTASIA; BLOTTING, WESTERN; CHEMOPREVENTION; CYCLIC N-OXIDES; FORMAZANS; LONGEVITY; LYMPHOMA; MEMBRANE POTENTIALS; MICE; MICE, MUTANT STRAINS; MITOCHONDRIA; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SPIN LABELS; TETRAZOLIUM SALTS; THYMUS NEOPLASMS; WEIGHT GAIN;

ATAXIA; ATAXIA TELANGIECTASIA;

EID: 4444349506     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddh189     Document Type: Article

References (61)

1. Davies, K.J. (2000) Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life, 50, 279-289.
2. Beckman, K.B. and Ames, B.N. (1997) Oxidative decay of DNA. J. Biol. Chem., 272, 19633-19636.
3. Burdon, R.H. (1995) Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free Radic. Biol. Med., 18, 775-794.
4. Schmidt-Ullrich, R.K., Dent, P., Grant, S., Mikkelsen, R.B. and Valerie, K. (2000) Signal transduction and cellular radiation responses. Radiat. Res., 153, 245-257.
5. Pearce, A.K. and Humphrey, T.C. (2001) Integrating stress-response and cell-cycle checkpoint pathways. Trends Cell Biol., 11, 426-433.
6. Finkel, T. (2001) Reactive oxygen species and signal transduction. IUBMB Life, 52, 3-6.
7. Leroy, C., Mann, C. and Marsolier, M.C. (2001) Silent repair accounts for cell cycle specificity in the signaling of oxidative DNA lesions. EMBO J., 20, 2896-2906.
8. Sauer, H., Wartenberg, M. and Hescheler, J. (2001) Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell Physiol. Biochem., 11, 173-186.
9. Neumann, C.A., Krause, D.S., Carman, C., Das, S., Dubey, D., Abraham, J., Bronson, R.T., Fujiwara, Y., Orkin, S. and Van Etten, R. (2003) Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression. Nature, 424, 561-565.
10. Tamimi, R.M., Lagiou, P., Adami, H.O. and Trichopoulos, D. (2002) Prospects for chemoprevention of cancer. J. Intern. Med., 251, 286-300.
11. Savitsky, K., Bar-Shira, A., Gilad, S., Rotman, G., Ziv, Y., Vanagaite, L., Tagle, D.A., Smith, S., Uziel, T., Sfez, S. et al. (1995) A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science, 268, 1749-1753.
12. Keith, C.T. and Schreiber, S.L. (1995) PIK-related kinases: DNA repair, recombination, and cell cycle checkpoints. Science, 270, 50-51.
13. Kastan, M.B. and Lim, D.S. (2000) The many substrates and functions of ATM. Nat. Rev. Mol. Cell Biol., 1, 179-186.
14. Abraham, R.T. (2001) Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev., 15, 2177-2196.
15. Shiloh, Y. (1997) Ataxia-telangiectasia and the Nijmegen breakage syndrome: related disorders but genes apart. Annu. Rev. Genet., 31, 635-662.
16. Rotman, G. and Shiloh, Y. (1997) Ataxia-telangiectasia: is ATM a sensor of oxidative damage and stress? Bioessays, 19, 911-917.
17. Takao, N., Li, Y. and Yamamoto, K. (2000) Protective roles for ATM in cellular response to oxidative stress. FEBS Lett., 472, 133-136.
18. Formichi, P., Battisti, C., Tripodi, S.A., Tosi, P. and Federico, A. (2000) Apoptotic response and cell cycle transition in ataxia telangiectasia cells exposed to oxidative stress. Life Sci., 66, 1893-1903.
19. Barlow, C., Dennery, P.A., Shigenaga, M.K., Smith, M.A., Morrow, J.D., Roberts, L.J., II, Wynshaw-Boris, A. and Levine, R.L. (1999) Loss of the ataxia-telangiectasia gene product causes oxidative damage in target organs. Proc. Natl Acad. Sci. USA, 96, 9915-9919.
20. Kamsler, A., Daily, D., Hochman, A., Stern, N., Shiloh, Y., Rotman, G. and Barzilai, A. (2001) Increased oxidative stress in ataxia telangiectasia evidenced by alterations in redox state of brains from Atm-deficient mice. Cancer Res., 61, 1849-1854.
21. Quick, K.L. and Dugan, L.L. (2001) Superoxide stress identifies neurons at risk in a model of ataxia-telangiectasia. Ann. Neurol., 49, 627-635.
22. Stern, N., Hochman, A., Zemach, N., Weizman, N., Hammel, I., Shiloh, Y., Rotman, G. and Barzilai, A. (2002) Accumulation of DNA damage and reduced levels of nicotine adenine dinucleotide in the brains of Atm-deficient mice. J. Biol. Chem., 277, 602-608.
23. Krishna, M.C., Grahame, D.A., Samuni, A., Mitchell, J.B. and Russo, A. (1992) Oxoammonium cation intermediate in the nitroxide-catalyzed dismutation of superoxide. Proc. Natl Acad. Sci. USA, 89, 5537-5541.
24. Samuni, A.M., DeGraff, W., Krishna, M.C. and Mitchell, J.B. (2002) Nitroxides as aritioxidants: tempol protects against EO9 cytotoxicity. Mol. Cell. Biochem., 234-235, 327-333.
25. Thiemermann, C. (2003) Membrane-permeable radical scavengers (tempol) for shock, ischemia-reperfusion injury, and inflammation. Crit. Care Med., 31, S76-S84.
26. Thiemermann, C., McDonald, M.C. and Cuzzocrea, S. (2001) The stable nitroxide, tempol, allenuates the effects of peroxynitrite and oxygen-derived free radicals. Crit. Care Med., 29, 223-224.
27. Hahn, S.M., Tochner, Z., Krishna, C.M., Glass, J., Wilson, L., Samuni, A., Sprague, M., Venzon, D., Glatstein, E., Mitchell, J.B. et al. (1992) Tempol, a stable free radical, is a novel murine radiation protector. Cancer Res., 52, 1750-1753.
28. Weiss, L., Stern, S., Reich, S. and Slavin, S. (1993) Effect of recombinant human manganese superoxide dismutase on radiosensitivity of murine B cell leukemia (BCL1) cells. Leuk. Lymphoma, 10, 477-481.
29. Samuni, A., Krishna, C.M., Riesz, P., Finkelstein, E. and Russo, A. (1988) A novel metal-free low molecular weight superoxide dismutase mimic. J. Biol. Chem., 263, 17921-17924.
30. Krishna, M.C., Samuni, A., Taira, J., Goldstein, S., Mitchell, J.B. and Russo, A. (1996) Stimulation by nitroxides of catalase-like activity of hemeproteins. Kinetics and mechanism. J. Biol. Chem., 271, 26018-26025.
31. Monti, E., Cova, D., Guido, E., Morelli, R. and Oliva, C. (1996) Protective effect of the nitroxide tempol against the cardiotoxicity of adriamycin. Free Radic. Biol. Med., 21, 463-470.
32. 2-induced injury. Lens Eye Toxic. Res., 9, 385-393.
33. Mitchell, J.B., Samuni, A., Krishna, M.C., DeGraff, W.G., Ahn, M.S., Samuni, U. and Russo, A. (1990) Biologically active metal-independent superoxide dismutase mimics. Biochemistry, 29, 2802-2807.
34. Rak, R., Chao, D.L., Pluta, R.M., Mitchell, J.B., Oldfield, E.H. and Watson, J.C. (2000) Neuroprotection by the stable nitroxide tempol during reperfusion in a rat model of transient focal ischemia. J. Neurosurg., 92, 646-651.
35. Samuni, A., Winkelsberg, D., Pinson, A., Hahn, S.M., Mitchell, J.B. and Russo, A. (1991) Nitroxide stable radicals protect beating cardiomyocytes against oxidative damage. J. Clin. Invest., 87, 1526-1530.
36. Mitchell, J.B., Xavier, S., DeLuca, A.M., Sowers, A.L., Cook, J.A., Krishna, M.C., Hahn, S.M. and Russo, A. (2003) A low molecular weight antioxidant decreases weight and lowers tumor incidence. Free Radic. Biol. Med., 34, 93-102.
37. Barlow, C., Hirotsune, S., Paylor, R., Liyanage, M., Eckhaus, M., Collins, F., Shiloh, Y., Crawley, J.N., Ried, T., Tagle, D. et al. (1996) Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell, 86, 159-171.
38. Liyanage, M., Weaver, Z., Barlow, C., Coleman, A., Pankratz, D.G., Anderson, S., Wynshaw-Boris, A. and Ried, T. (2000) Abnormal rearrangement within the alpha/delta T-cell receptor locus in lymphomas from Atm-deficient mice. Blood, 96, 1940-1946.
39. Burow, S. and Valet, G. (1987) Flow-cytometric characterization of stimulation, free radical formation, peroxidase activity and phagocytosis of human granulocytes with 2,7-dichlorofluorescein (DCF). Eur. J. Cell Biol., 43, 128-133.
40. Watanabe, S. (1998) In vivo fluorometric measurement of cerebral oxidative stress using 2′-7′-dichlorofluorescein (DCF). Keio J. Med., 47, 92-98.
41. Wang, H. and Joseph, J.A. (1999) Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic. Biol. Med., 27, 612-616.
42. Melov, S. (2002) Therapeutics against mitochondrial oxidative stress in animal models of aging. Ann. NY Acad. Sci., 959, 330-340.
43. Cossarizza, A., Baccarani-Contri, M., Kalashnikova, G. and Franceschi, C. (1993) A new method for the cytofluorimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5,5′,6,6′-tetrachloro-1,1′,3,3′ -tetraethyl-benzimidazolcarbocyanine iodide (JC-1). Biochem. Biophys. Res. Commun., 197, 40-45.
44. Mossmann (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods, 65, 55-63.
45. Gariboldi, M.B., Lucchi, S., Caserini, C., Supino, R., Oliva, C. and Monti, E. (1998) Antiproliferative effect of the piperidine nitroxide TEMPOL on neoplastic and nonneoplastic mammalian cell lines. Free Radic. Biol. Med., 24, 913-923.
46. Monti, E., Supino, R., Colleoni, M., Costa, B., Ravizza, R. and Gariboldi, M.B. (2001) Nitroxide TEMPOL impairs mitochundrial function and induces apoptosis in HL60 cells. J. Cell. Biochem., 82, 271-276.
47. Singhal, A.B., Wang, X., Sumii, T., Mori, T. and Lo, E.H. (2002) Effects of normobaric hyperoxia in a rat model of focal cerebral ischemia-reperfusion. J. Cereb. Blood Flow Metab., 22, 861-868.
48. Berrigan, D., Perkins, S.N., Haines, D.C. and Hursting, S.D. (2002) Adult-onset calorie restriction and fasting delay spontaneous tumorigenesis in p53-deficient mice. Carcinogenesis, 23, 817-822.
49. Hursting, S.D., Perkins, S.N., Brown, C.C., Haines, D.C. and Phang, J.M. (1997) Calorie restriction induces a p53-independent delay of spontaneous carcinogenesis in p53-deficient and wild-type mice. Cancer Res., 57, 2843-2846.
50. Pugh, T.D., Oberley, T.D. and Weindruch, R. (1999) Dietary intervention at middle age: caloric restriction but not dehydroepiandrosterone sulfate increases lifespan and lifetime cancer incidence in mice. Cancer Res., 59, 1642-1648.
51. Yoshida, K., Inoue, T., Nojima, K., Hirabayashi, Y. and Sado, T. (1997) Calorie restriction reduces the incidence of myeloid leukemia induced by a single whole-body radiation in C3H/He mice. Proc. Natl Acad. Sci. USA, 94, 2615-2619.
52. Edwards, B.K., Howe, H.L., Ries, L.A., Thun, M.J., Rosenberg, H.M., Yancik, R., Wingo, P.A., Jemal, A. and Feigal, E.G. (2002) Annual report to the nation on the status of cancer, 1973-1999, featuring implications of age and aging on U.S. cancer burden. Cancer, 94, 2766-2792.
53. Krishnan, K., Campbell, S., Abdel-Rahman, F., Whaley, S. and Stone, W.L. (2003) Cancer chemoprevention drug targets. Curr. Drug Targets, 4, 45-54.
54. Schwartz, J.L., Antoniades, D.Z. and Zhao, S. (1993) Molecular and biochemical reprogramming of oncogenesis through the activity of prooxidants and antioxidants. Ann. NY Acad. Sci., 686, 262-278.
55. Reichenbach, J., Schubert, R., Schwan, C., Muller, K., Bohles, H.J. and Zielen, S. (1999) Anti-oxidative capacity in patients with ataxia telangiectasia. Clin. Exp. Immunol., 117, 535-539.
56. Browne, S.E., Roberts, L.J., 2nd, Dennery, P.A., Doctrow, S.R., Beal, M.F., Barlow, C. and Levine, R.L. (2004) Treatment with a catalytic antioxidant corrects the neurobehavioral defect in ataxia-telangiectasia mice. Free Radic. Biol. Med., 36, 938-942.
57. Doctrow, S.R., Huffman, K., Marcus, C.B., Tocco, G., Malfroy, E., Adinolfi, C.A., Kruk, H., Baker, K., Lazarowych, N., Mascarenhas, J. et al. (2002) Salen-manganese complexes as catalytic scavengers of hydrogen perioxide and cytoprotective agents: structure-activity relationship studies. J. Med. Chem., 45, 4549-4558.
58. Behrend, L., Henderson, G. and Zwacka, R.M. (2003) Reactive oxygen species in oncogenic transformation. Biochem. Soc. Trans., 31, 1441-1444.
59. Burdon, R.H. (1995) Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free. Radic. Biol. Med., 18, 775-794.
60. Slater, A.F., Stefan, C., Nobel, I., van den Dobbelsteen, D.J. and Orrenius, S. (1995) Signalling mechanisms and oxidative stress in apoptosis. Toxicol. Lett., 82-83, 149-153.
61. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular cloning: A Laboratory Manual., 2nd edn. Cold Spring Harbor Laboratory Press.