Heart tissue of harlequin (hq)/Big Blue® mice has elevated reactive oxygen species without significant impact on the frequency and nature of point mutations in nuclear DNA

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 691, Issue 1-2, 2010, Pages 64-71

  Crabbe, Rory A ^a   Hill, Kathleen A ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Apoptosis inducing factor; CII mutations; Mitochondrial dysfunction; Mutation detection; Paraquat; Reactive oxygen species; Transgenic mouse

Indexed keywords

APOPTOSIS INDUCING FACTOR; CELL NUCLEUS DNA; MITOCHONDRIAL DNA; PARAQUAT; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; HEART DISEASE; HETEROZYGOTE; MALE; MOUSE; MUTANT; MUTATION RATE; NONHUMAN; OXIDATIVE STRESS; POINT MUTATION; PRIORITY JOURNAL;

AGING, PREMATURE; ANIMALS; APOPTOSIS INDUCING FACTOR; CELL NUCLEUS; DISEASE MODELS, ANIMAL; MICE; MICE, MUTANT STRAINS; MYOCARDIUM; POINT MUTATION; REACTIVE OXYGEN SPECIES;

MUS; MUS MUSCULUS;

EID: 77956175629     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2010.06.001     Document Type: Article

References (54)

1. Dolle M.E., Snyder W.K., Gossen J.A., Lohman P.H., Vijg J. Distinct spectra of somatic mutations accumulated with age in mouse heart and small intestine. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:8403-8408.
2. Ono T., Ikehata H., Nakamura S., Saito Y., Hosoi Y., Takai Y., Yamada S., Onodera J., Yamamoto K. Age-associated increase of spontaneous mutant frequency and molecular nature of mutation in newborn and old lacZ-transgenic mouse. Mutat. Res. 2000, 447:165-177.
3. Marin-Garcia J., Pi Y., Goldenthal M.J. Mitochondrial-nuclear cross-talk in the aging and failing heart. Cardiovasc. Drugs Ther. 2006, 20:477-491.
4. Dai D.F., Rabinovitch P.S. Cardiac aging in mice and humans: the role of mitochondrial oxidative stress. Trends Cardiovasc. Med. 2009, 19:213-220.
5. Fosslien E. Review: mitochondrial medicine-cardiomyopathy caused by defective oxidative phosphorylation. Ann. Clin. Lab. Sci. 2003, 33:371-395.
6. Chinnery P.F., Samuels D.C., Elson J., Turnbull D.M. Accumulation of mitochondrial DNA mutations in ageing, cancer, and mitochondrial disease: is there a common mechanism?. Lancet 2002, 360:1323-1325.
7. Elson J.L., Samuels D.C., Turnbull D.M., Chinnery P.F. Random intracellular drift explains the clonal expansion of mitochondrial DNA mutations with age. Am. J. Hum. Genet. 2001, 68:802-806.
8. Klein J.A., Longo-Guess C.M., Rossmann M.P., Seburn K.L., Hurd R.E., Frankel W.N., Bronson R.T., Ackerman S.L. The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature 2002, 419:367-374.
9. van Empel V.P., Bertrand A.T., van der Nagel R., Kostin S., Doevendans P.A., Crijns H.J., de Wit E., Sluiter W., Ackerman S.L., De Windt L.J. Downregulation of apoptosis-inducing factor in harlequin mutant mice sensitizes the myocardium to oxidative stress-related cell death and pressure overload-induced decompensation. Circ. Res. 2005, 96:e92-e101.
10. van Empel V.P., Bertrand A.T., van Oort R.J., van der Nagel R., Engelen M., van Rijen H.V., Doevendans P.A., Crijns H.J., Ackerman S.L., Sluiter W., De Windt L.J. EUK-8, a superoxide dismutase and catalase mimetic, reduces cardiac oxidative stress and ameliorates pressure overload-induced heart failure in the harlequin mouse mutant. J. Am. Coll. Cardiol. 2006, 48:824-832.
11. Stringer J.R., Larson J.S., Fischer J.M., Stringer S.L. Increased mutation in mice genetically predisposed to oxidative damage in the brain. Mutat. Res. 2004, 556:127-134.
12. Van Osch F.S., Piliguian M., Hill K.A. Spontaneous mutation frequency is elevated in skin of harlequin (hq)/Big Blue mice. Mutagenesis 2010, 25:235-242.
13. de Haan J.B., Bladier C., Griffiths P., Kelner M., O'Shea R.D., Cheung N.S., Bronson R.T., Silvestro M.J., Wild S., Zheng S.S., Beart P.M., Hertzog P.J., Kola I. Mice with a homozygous null mutation for the most abundant glutathione peroxidase, Gpx1, show increased susceptibility to the oxidative stress-inducing agents paraquat and hydrogen peroxide. J. Biol. Chem. 1998, 273:22528-22536.
14. Moody C.S., Hassan H.M. Mutagenicity of oxygen free radicals. Proc. Natl. Acad. Sci. U.S.A. 1982, 79:2855-2859.
15. Drew R., Gram T.E. Vehicle alteration of paraquat lethality in mice. Toxicol. Appl. Pharmacol. 1979, 48:479-487.
16. Hawksworth G.M., Bennett P.N., Davies D.S. Kinetics of paraquat elimination in the dog. Toxicol. Appl. Pharmacol. 1981, 57:139-145.
17. Cocheme H.M., Murphy M.P. Complex I is the major site of mitochondrial superoxide production by paraquat. J. Biol. Chem. 2008, 283:1786-1798.
18. Bus J.S., Gibson J.E. Paraquat: model for oxidant-initiated toxicity. Environ. Health Perspect. 1984, 55:37-46.
19. Fukushima T., Yamada K., Isobe A., Shiwaku K., Yamane Y. Mechanism of cytotoxicity of paraquat. I. NADH oxidation and paraquat radical formation via complex I. Exp. Toxicol. Pathol. 1993, 45:345-349.
20. Castello P.R., Drechsel D.A., Patel M. Mitochondria are a major source of paraquat-induced reactive oxygen species production in the brain. J. Biol. Chem. 2007, 282:14186-14193.
21. Ribas G., Surralles J., Carbonell E., Xamena N., Creus A., Marcos R. Genotoxic evaluation of the herbicide paraquat in cultured human lymphocytes. Teratog. Carcinog. Mutagen. 1997, 17:339-347.
22. Yin X.H., Li S.N., Zhang L., Zhu G.N., Zhuang H.S. Evaluation of DNA damage in Chinese toad (Bufo bufo gargarizans) after in vivo exposure to sublethal concentrations of four herbicides using the comet assay. Ecotoxicology 2008, 17:280-286.
23. D'Souza U.J., Zain A., Raju S. Genotoxic and cytotoxic effects in the bone marrow of rats exposed to a low dose of paraquat via the dermal route. Mutat. Res. 2005, 581:187-190.
24. Speit G., Haupter S., Hartmann A. Evaluation of the genotoxic properties of paraquat in V79 Chinese hamster cells. Mutat. Res. 1998, 412:187-193.
25. Jakubczak J.L., Merlino G., French J.E., Muller W.J., Paul B., Adhya S., Garges S. Analysis of genetic instability during mammary tumor progression using a novel selection-based assay for in vivo mutations in a bacteriophage lambda transgene target. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:9073-9078.
26. Lee D.H., Esworthy R.S., Chu C., Pfeifer G.P., Chu F.F. Mutation accumulation in the intestine and colon of mice deficient in two intracellular glutathione peroxidases. Cancer Res. 2006, 66:9845-9851.
27. Piegorsch W.W., Margolin B.H., Shelby M.D., Johnson A., French J.E., Tennant R.W., Tindall K.R. Study design and sample sizes for a lacI transgenic mouse mutation assay. Environ. Mol. Mutagen. 1995, 25:231-245.
28. Carter W.O., Narayanan P.K., Robinson J.P. Intracellular hydrogen peroxide and superoxide anion detection in endothelial cells. J. Leukoc. Biol. 1994, 55:253-258.
29. Burnaugh L., Sabeur K., Ball B.A. Generation of superoxide anion by equine spermatozoa as detected by dihydroethidium. Theriogenology 2007, 67:580-589.
30. Williams I.A., Allen D.G. The role of reactive oxygen species in the hearts of dystrophin-deficient mdx mice. Am. J. Physiol. Heart Circ. Physiol. 2007, 293:H1969-H1977.
31. Stratagene Big Blue Transgenic Mouse Mutagenesis Assay System: Instruction Manual, La Jolla, California, USA, 1992.
32. Stratagene λ Select-cII Mutation Detection System for Big Blue Rodents, La Jolla, California, USA, 2002.
33. Schwarz E., Scherer G., Hobom G., Kossel H. Nucleotide sequence of cro, cII and part of the O gene in phage lambda DNA. Nature 1978, 272:410-414.
34. Nishino H., Schaid D.J., Buettner V.L., Haavik J., Sommer S.S. Mutation frequencies but not mutant frequencies in Big Blue mice fit a Poisson distribution. Environ. Mol. Mutagen. 1996, 28:414-417.
35. Hill K.A., Buettner V.L., Halangoda A., Kunishige M., Moore S.R., Longmate J., Scaringe W.A., Sommer S.S. Spontaneous mutation in Big Blue mice from fetus to old age: tissue-specific time courses of mutation frequency but similar mutation types. Environ. Mol. Mutagen. 2004, 43:110-120.
36. Hill K.A., Halangoda A., Heinmoeller P.W., Gonzalez K., Chitaphan C., Longmate J., Scaringe W.A., Wang J.C., Sommer S.S. Tissue-specific time courses of spontaneous mutation frequency and deviations in mutation pattern are observed in middle to late adulthood in Big Blue mice. Environ. Mol. Mutagen. 2005, 45:442-454.
37. Turker M.S., Gage B.M., Rose J.A., Elroy D., Ponomareva O.N., Stambrook P.J., Tischfield J.A. A novel signature mutation for oxidative damage resembles a mutational pattern found commonly in human cancers. Cancer Res. 1999, 59:1837-1839.
38. Takimoto E., Champion H.C., Li M., Ren S., Rodriguez E.R., Tavazzi B., Lazzarino G., Paolocci N., Gabrielson K.L., Wang Y., Kass D.A. Oxidant stress from nitric oxide synthase-3 uncoupling stimulates cardiac pathologic remodeling from chronic pressure load. J. Clin. Invest. 2005, 115:1221-1231.
39. Moens A.L., Takimoto E., Tocchetti C.G., Chakir K., Bedja D., Cormaci G., Ketner E.A., Majmudar M., Gabrielson K., Halushka M.K., Mitchell J.B., Biswal S., Channon K.M., Wolin M.S., Alp N.J., Paolocci N., Champion H.C., Kass D.A. Reversal of cardiac hypertrophy and fibrosis from pressure overload by tetrahydrobiopterin: efficacy of recoupling nitric oxide synthase as a therapeutic strategy. Circulation 2008, 117:2626-2636.
40. Franco A.A., Odom R.S., Rando T.A. Regulation of antioxidant enzyme gene expression in response to oxidative stress and during differentiation of mouse skeletal muscle. Free Radic. Biol. Med. 1999, 27:1122-1132.
41. Black A.T., Gray J.P., Shakarjian M.P., Laskin D.L., Heck D.E., Laskin J.D. Increased oxidative stress and antioxidant expression in mouse keratinocytes following exposure to paraquat. Toxicol. Appl. Pharmacol. 2008, 231:384-392.
42. Rakusan K., Heron M.I., Kolar F., Korecky B. Transplantation-induced atrophy of normal and hypertrophic rat hearts: effect on cardiac myocytes and capillaries. J. Mol. Cell. Cardiol. 1997, 29:1045-1054.
43. Cruz-Munoz W., Kalair W., Cosentino L., Heddle J.A. ENU induces mutations in the heart of lacZ transgenic mice. Mutat. Res. 2000, 469:23-34.
44. Goldstein M.A., Claycomb W.C., Schwartz A. DNA synthesis and mitosis in well-differentiated mammalian cardiocytes. Science 1974, 183:212-213.
45. Kunz J., Keim U., Fuhrmann I. Myocyte and fibroblast proliferation in rat myocardium in postnatal growth. Exp. Pathol. (Jena) 1972, 6:270-277.
46. Marino T.A., Haldar S., Williamson E.C., Beaverson K., Walter R.A., Marino D.R., Beatty C., Lipson K.E. Proliferating cell nuclear antigen in developing and adult rat cardiac muscle cells. Circ. Res. 1991, 69:1353-1360.
47. Nichols J.E., Simmons K.R. A quantitative histologic analysis of selected tissues in growing mice. Dev. Biol. 1970, 23:113-127.
48. Vahsen N., Cande C., Briere J.J., Benit P., Joza N., Larochette N., Mastroberardino P.G., Pequignot M.O., Casares N., Lazar V., Feraud O., Debili N., Wissing S., Engelhardt S., Madeo F., Piacentini M., Penninger J.M., Schagger H., Rustin P., Kroemer G. AIF deficiency compromises oxidative phosphorylation. EMBO J. 2004, 23:4679-4689.
49. Shane B.S., Smith-Dunn D.L., de Boer J.G., Glickman B.W., Cunningham M.L. Mutant frequencies and mutation spectra of dimethylnitrosamine (DMN) at the lacI and cII loci in the livers of Big Blue transgenic mice. Mutat. Res. 2000, 452:197-210.
50. Prat F., Houk K., Foote S. Effect of guanine stacking on the oxidation of 8-oxoguanine in B-DNA. J. Am. Chem. Soc. 1998, 120:845-847.
51. Voigt J.M., Topal M.D. O6-methylguanine and A.C and G.T mismatches cause asymmetric structural defects in DNA that are affected by DNA sequence. Biochemistry 1990, 29:5012-5018.
52. Ceccotti S., Aquilina G., Macpherson P., Yamada M., Karran P., Bignami M. Processing of O6-methylguanine by mismatch correction in human cell extracts. Curr. Biol. 1996, 6:1528-1531.
53. Calviello G., Piccioni E., Boninsegna A., Tedesco B., Maggiano N., Serini S., Wolf F.I., Palozza P. DNA damage and apoptosis induction by the pesticide Mancozeb in rat cells: involvement of the oxidative mechanism. Toxicol. Appl. Pharmacol. 2006, 211:87-96.
54. Besaratinia A., Synold T.W., Xi B., Pfeifer G.P. G-to-T transversions and small tandem base deletions are the hallmark of mutations induced by ultraviolet a radiation in mammalian cells. Biochemistry 2004, 43:8169-8177.