Dramatic extension of tumor latency and correction of neurobehavioral phenotype in Atm-mutant mice with a nitroxide antioxidant

Free Radical Biology and Medicine

Volumn 41, Issue 6, 2006, Pages 992-1000

  Gueven, Nuri ^a   Luff, John ^a   Peng, Cheng ^a   Hosokawa, Kazuyuki ^b   Bottle, Steven E ^b   Lavin, Martin F ^a,c  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Ataxia telangiectasia; Leukemia; Lymphoma; Neurodegeneration; Nitroxide; Oxidative stress

Indexed keywords

ANTIOXIDANT; ATM PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; ATAXIA TELANGIECTASIA; BRAIN PROTECTION; CANCER INHIBITION; COGNITIVE DEFECT; CONTROLLED STUDY; DRUG MECHANISM; GENE MUTATION; GENETIC PREDISPOSITION; HUMAN; HUMAN CELL; MOUSE; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; THERAPY EFFECT; THYMUS LYMPHOMA; TREATMENT OUTCOME; TUMOR GROWTH;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; ATAXIA TELANGIECTASIA; BEHAVIOR, ANIMAL; CELL CYCLE PROTEINS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; GENOTYPE; HUMANS; INDOLES; LYMPHOMA; LYMPHOMA, LYMPHOBLASTIC; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MOTOR ACTIVITY; MUTATION; POLYMERASE CHAIN REACTION; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

ATAXIA TELANGIECTASIA;

EID: 33747371969     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2006.06.018     Document Type: Article

References (38)

1. Sedgwick R.P., and Boder E. Ataxia-telangiectasia. In: Vianney De Jong J.M.B., and Liss A.R. (Eds). Hereditary neuropathies and spinocerebellar atrophies (1991) 347-423 New York
2. Lavin M.F., and Shiloh Y. The genetic defect in ataxia-telangiectasia. Annu. Rev. Immunol. 15 (1997) 177-202
3. Savitsky K., Bar-Shira A., Gilad S., Rotman G., Ziv Y., Vanagaite L., Tagle D.A., Smith S., Uziel T., Sfez S., et al. A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 268 (1995) 1749-1753
4. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev., Cancer 3 (2003) 155-168
5. Boder E. Ataxia-telangiectasia: an overview. Kroc Found. Ser. 19 (1985) 1-63
6. Taylor A.M., Metcalfe J.A., Thick J., and Mak Y.F. Leukemia and lymphoma in ataxia telangiectasia. Blood 87 (1996) 423-438
7. Lavin M.F., and Lederman H.M. Chromosomal breakage syndromes associated with immunodeficiency. In: Stiehm E.R., Ochs H.D., and Winkelstein J.A. (Eds). Immunologic disorders in infants & Children (2004), Elsevier Saunders, Philadelphia 580-604
8. Xu Y., Ashley T., Brainerd E.E., Bronson R.T., Meyn M.S., and Baltimore D. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 10 (1996) 2411-2422
9. Elson A., Wang Y., Daugherty C.J., Morton C.C., Zhou F., Campos-Torres J., and Leder P. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc. Natl. Acad. Sci. USA 93 (1996) 13084-13089
10. Borghesani P.R., Alt F.W., Bottaro A., Davidson L., Aksoy S., Rathbun G.A., Roberts T.M., Swat W., Segal R.A., and Gu Y. Abnormal development of Purkinje cells and lymphocytes in Atm mutant mice. Proc. Natl. Acad. Sci. USA 97 (2000) 3336-3341
11. Barlow C., Hirotsune S., Paylor R., Liyanage M., Eckhaus M., Collins F., Shiloh Y., Crawley J.N., Ried T., Tagle D., and Wynshaw-Boris A. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86 (1996) 159-171
12. Spring K., Cross S., Li C., Watters D., Ben-Senior L., Waring P., Ahangari F., Lu S.L., Chen P., Misko I., Paterson C., Kay G., Smorodinsky N.I., Shiloh Y., and Lavin M.F. Atm knock-in mice harboring an in-frame deletion corresponding to the human ATM 7636del9 common mutation exhibit a variant phenotype. Cancer Res. 61 (2001) 4561-4568
13. Browne S.E., Roberts II L.J., Dennery P.A., Doctrow S.R., Beal M.F., Barlow C., and Levine R.L. Treatment with a catalytic antioxidant corrects the neurobehavioral defect in ataxia-telangiectasia mice. Free Radic. Biol. Med. 36 (2004) 938-942
14. Mount H.T.J., Martel J.C., Fluit P., Wu Y., Gallo-Hendrikx E., Cosi C., and Marien M.R. Progressive sensorimotor impairment is not associated with reduced dopamine and high energy phosphate donors in a model of ataxia-telangiectasia. J. Neurochem. 88 (2004) 1449-1454
15. Barzilai A., Rotman G., and Shiloh Y. ATM deficiency and oxidative stress: a new dimension of defective response to DNA damage. DNA Repair (Amsterdam) 1 (2002) 23-25
16. Reichenbach J., Schubert R., Schindler D., Muller K., Bohles H., and Zielen S. Elevated oxidative stress in patients with ataxia telangiectasia. Antioxid. Redox Signal. 4 (2002) 465-469
17. Reichenbach J., Schubert R., Schwan C., Muller K., Bohles H.J., and Zielen S. Anti-oxidative capacity in patients with ataxia telangiectasia. Clin. Exp. Immunol. 117 (1999) 535-539
18. Barzilai A., and Yamamoto K. DNA damage responses to oxidative stress. DNA Repair 3 (2004) 1109-1115
19. Yi M., Rosin M.P., and Anderson C.K. Response of fibroblast cultures from ataxia-telangiectasia patients to oxidative stress. Cancer Lett. 54 (1990) 43-50
20. Barlow C., Dennery P.A., Shigenaga M.K., Smith M.A., Morrow J.D., Roberts II L.J., Wynshaw-Boris A., and Levine R.L. Loss of the ataxia-telangiectasia gene product causes oxidative damage in target organs. Proc. Natl. Acad. Sci. USA 96 (1999) 9915-9919
21. Watters D.J. Oxidative stress in ataxia telangiectasia. Redox Rep. 8 (2003) 23-29
22. Kamsler A., Daily D., Hochman A., Stern N., Shiloh Y., Rotman G., and Barzilai A. Increased oxidative stress in ataxia telangiectasia evidenced by alterations in redox state of brains from Atm-deficient mice. Cancer Res. 61 (2001) 1849-1854
23. Yang Y., and Herrup K. Loss of neuronal cell cycle control in ataxia-telangiectasia: a unified disease mechanism. J. Neurosci. 25 (2005) 2522-2529
24. Chen P., Peng C., Luff J., Spring K., Watters D., Bottle S., Furuya S., and Lavin M.F. Oxidative stress is responsible for deficient survival and dendritogenesis in purkinje neurons from ataxia-telangiectasia mutated mutant mice. J. Neurosci. 23 (2003) 11453-11460
25. Samuni A., Krishna C.M., Riesz P., Finkelstein E., and Russo A. A novel metal-free low molecular weight superoxide dismutase mimic. J. Biol. Chem. 263 (1988) 17921-17924
26. Krishna M.C., Grahame D.A., Samuni A., Mitchell J.B., and Russo A. Oxoammonium cation intermediate in the nitroxide-catalyzed dismutation of superoxide. Proc. Natl. Acad. Sci. USA 89 (1992) 5537-5541
27. Mitchell J.B., Samuni A., Krishna M.C., DeGraff W.G., Ahn M.S., Samuni U., and Russo A. Biologically active metal-independent superoxide dismutase mimics. Biochemistry 29 (1990) 2802-2807
28. Hahn S.M., Krishna C.M., Samuni A., DeGraff W., Cuscela D.O., Johnstone P., and Mitchell J.B. Potential use of nitroxides in radiation oncology. Cancer Res. 54 (1994) 2006s-2010s
29. Damiani E., Kalinska B., Canapa A., Canestrari S., Wozniak M., Olmo E., and Greci L. The effects of nitroxide radicals on oxidative DNA damage. Free Radic. Biol. Med. 28 (2000) 1257-1265
30. Bottle S., Gillies D., Highes D., Micallef A., Smirnov A., and Sutcliffe L. Synthesis, single X-ray crystal structure and W band (95GHz) EPR spectroscopy of a new anionic isoindoline aminoxyl: synthesis and characterisation of some derivatives. J. Chem. Soc. Perkin 27 (2000) 1285-1291
31. Gueven N., Fukao T., Luff J., Paterson C., Kay G., Kondo N., and Lavin M.F. Regulation of the Atm promoter in vivo. Genes Chromosomes Cancer 45 (2006) 61-71
32. MacMillan-Crow L.A., Crow J.P., Kerby J.D., Beckman J.S., and Thompson J.A. Nitration and inactivation of manganese superoxide dismutase in chronic rejection of human renal allografts. Proc. Natl. Acad. Sci. USA 93 (1996) 11853-11858
33. Suy S., Mitchel J.B., Samuni A., Mueller S., and Kasid U. Nitroxide Tempo, a small molecule, induces apoptosis in prostate carcinoma cells and suppresses tumour growth in athymic mice. Cancer 103 (2005) 1302-1313
34. Schubert R., Erker L., Barlow C., Yakushiji H., Larson D., Russo A., Mitchell J.B., and Wynshaw-Boris A. Cancer chemoprevention by the antioxidant Tempol in Atm-deficient mice. Hum Mol. Genet. 13 (2004) 1793-1802
35. Suy S., Mitchell J.B., Ehleiter D., Haimovitz-Friedman A., and Kasid U. Nitroxides tempol and tempo induce divergent signal transduction pathways in MDA-MB 231 breast cancer cells. J. Biol. Chem. 273 (1998) 17871-17878
36. Mitchell J.B., Xavier S., DeLuca A.M., Sowers A.L., Cook J.A., Krishna M.C., Hahn S.M., and Russo A. A low molecular weight antioxidant decreases weight and lowers tumor incidence. Free Radic. Biol. Med. 34 (2003) 93-102
37. Frappart P.O., Tong W.M., Demuth I., Radovanovic I., Herceg Z., Aguzzi A., Digweed M., and Wang Z.Q. An essential function for NBS1 in the prevention of ataxia and cerebellar defects. Nat. Med. 11 (2005) 538-544
38. Ziv S., Brenner O., Amariglio N., Smorodinsky N.I., Galron R., Carrion D.V., Zhang W., Sharma G.G., Pandita R.K., Agarwal M., et al. Impaired genomic stability and increased oxidative stress exacerbate different features of Ataxia-telangiectasia. Hum. Mol. Genet. 14 (2005) 2929-2943