Mitochondrial oxidative stress in human hepatoma cells exposed to stavudine

Toxicology and Applied Pharmacology

Volumn 199, Issue 1, 2004, Pages 10-19

  Velsor, Leonard W ^a   Kovacevic, Miro ^a   Goldstein, Mark ^a   Leitner, Heather M ^b   Lewis, William ^c   Day, Brian J ^a,b  

^a NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aconitase; AIDS; HIV; Mitochondrial DNA; Nucleoside reverse transcriptase inhibitors

Indexed keywords

ANTIOXIDANT; BENZOIC ACID DERIVATIVE; LACTIC ACID; MANGANESE TETRAKIS(4 BENZOIC ACID)PORPHYRIN; MITOCHONDRIAL DNA; PORPHYRIN DERIVATIVE; PYRUVIC ACID; REACTIVE OXYGEN METABOLITE; STAVUDINE; UNCLASSIFIED DRUG;

ANTIOXIDANT ACTIVITY; ARTICLE; CATALYSIS; CELL DAMAGE; CELL FUNCTION; CELL STRAIN HEPG2; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORRELATION ANALYSIS; GENE AMPLIFICATION; HEPATOMA CELL; HUMAN; HUMAN CELL; LIVER DEVELOPMENT; LIVER MITOCHONDRION; MITOCHONDRIAL RESPIRATION; OXIDATIVE STRESS; STATISTICAL SIGNIFICANCE;

CARCINOMA, HEPATOCELLULAR; DNA REPLICATION; DNA, MITOCHONDRIAL; HUMANS; MITOCHONDRIA, LIVER; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE INHIBITORS; STAVUDINE; TUMOR CELLS, CULTURED;

HUMAN IMMUNODEFICIENCY VIRUS;

EID: 4143050352     PISSN: 0041008X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.taap.2004.03.005     Document Type: Article

References (46)

1. Attardi G., Ching E. Biogenesis of mitochondrial proteins in HeLa cells. Methods Enzymol. 56:1979;66-79
2. Barthelemy C., Ogier de Baulny H., Diaz J., Cheval M.A., Frachon P., Romero N., Goutieres F., Fardeau M., Lombes A. Late-onset mitochondrial DNA depletion: DNA copy number, multiple deletions, and compensation. Ann. Neurol. 49:2001;607-617
3. Bialkowska A., Bialkowski K., Gerschenson M., Diwan B.A., Jones A.B., Olivero O.A., Poirier M.C., Anderson L.M., Kasprzak K.S., Sipowicz M.A. Oxidative DNA damage in fetal tissues after transplacental exposure to 3′-azido-3′-deoxythymidine (AZT). Carcinogenesis. 21:2000;1059-1062
4. Birkus G., Hitchcock M.J., Cihlar T. Assessment of mitochondrial toxicity in human cells treated with tenofovir: comparison with other nucleoside reverse transcriptase inhibitors. Antimicrob. Agents Chemother. 46:2002;716-723
5. Choi J., Liu R.M., Kundu R.K., Sangiorgi F., Wu W., Maxson R., Forman H.J. Molecular mechanism of decreased glutathione content in human immunodeficiency virus type 1 Tat-transgenic mice. J. Biol. Chem. 275:2000;3693-3698
6. Cortopassi G., Wang E. Modelling the effects of age-related mtDNA mutation accumulation; complex I deficiency, superoxide and cell death. Biochim. Biophys. Acta. 1271:1995;171-176
7. Day B.J., Shawen S., Liochev S.I., Crapo J.D. A metalloporphyrin superoxide dismutase mimetic protects against paraquat-induced endothelial cell injury, in vitro. J. Pharmacol. Exp. Ther. 275:1995;1227-1232
8. De Clercq E. Strategies in the design of antiviral drugs. Nat. Rev., Drug Discov. 1:2002;13-25
9. de la Asuncion J.G., del Olmo M.L., Sastre J., Pallardo F.V., Vina J. Zidovudine (AZT) causes an oxidation of mitochondrial DNA in mouse liver. Hepatology. 29:1999;985-987
10. Flores S.C., Marecki J.C., Harper K.P., Bose S.K., Nelson S.K., McCord J.M. Tat protein of human immunodeficiency virus type 1 represses expression of manganese superoxide dismutase in HeLa cells. Proc. Natl. Acad. Sci. U.S.A. 90:1993;7632-7636
11. Fukushima T., Tawara T., Isobe A., Hojo N., Shiwaku K., Yamane Y. Radical formation site of cerebral complex I and Parkinson's disease. J. Neurosci. Res. 42:1995;385-390
12. Furman P.A., Fyfe J.A., St Clair M.H., Weinhold K., Rideout J.L., Freeman G.A., Lehrman S.N., Bolognesi D.P., Broder S., Mitsuya H., et al. Phosphorylation of 3′-azido-3′-deoxythymidine and selective interaction of the 5′-triphosphate with human immunodeficiency virus reverse transcriptase. Proc. Natl. Acad. Sci. U.S.A. 83:1986;8333-8337
13. Gardner P.R. Aconitase: sensitive target and measure of superoxide. Methods Enzymol. 349:2002;9-23
14. Gerschenson M., Nguyen V.T., St Claire M.C., Harbaugh S.W., Harbaugh J.W., Proia L.A., Poirier M.C. Chronic stavudine exposure induces hepatic mitochondrial toxicity in adult Erythrocebus patas monkeys. J. Hum. Virol. 4:2001;335-342
15. Graziewicz M.A., Day B.J., Copeland W.C. The mitochondrial DNA polymerase as a target of oxidative damage. Nucleic Acids Res. 30:2002;2817-2824
16. Lenzo N.P., Garas B.A., French M.A. Hepatic steatosis and lactic acidosis associated with stavudine treatment in an HIV patient: a case report. [comment] AIDS. 11:1997;1294-1296
17. Lewis W., Gonzalez B., Chomyn A., Papoian T. Zidovudine induces molecular, biochemical, and ultrastructural changes in rat skeletal muscle mitochondria. J. Clin. Invest. 89:1992;1354-1360
18. Lewis W., Simpson J.F., Meyer R.R. Cardiac mitochondrial DNA polymerase-gamma is inhibited competitively and noncompetitively by phosphorylated zidovudine. Circ. Res. 74:1994;344-348
19. Lewis W., Levine E.S., Griniuviene B., Tankersley K.O., Colacino J.M., Sommadossi J.P., Watanabe K.A., Perrino F.W. Fialuridine and its metabolites inhibit DNA polymerase gamma at sites of multiple adjacent analog incorporation, decrease mtDNA abundance, and cause mitochondrial structural defects in cultured hepatoblasts. Proc. Natl. Acad. Sci. U.S.A. 93:1996;3592-3597
20. Lewis W., Copeland W.C., Day B.J. Mitochondrial DNA depletion, oxidative stress, and mutation: mechanisms of dysfunction from nucleoside reverse transcriptase inhibitors. Lab. Invest. 81:2001;777-790
21. Li Q.Y., Pedersen C., Day B.J., Patel M. Dependence of excitotoxic neurodegeneration on mitochondrial aconitase inactivation. J. Neurochem. 78:2001;746-755
22. Lim S.E., Copeland W.C. Differential incorporation and removal of antiviral deoxynucleotides by human DNA polymerase gamma. J. Biol. Chem. 276:2001;23616-23623
23. Linnane A.W., Marzuki S., Ozawa T., Tanaka M. Mitochondrial DNA mutations as an important contributor to ageing and degenerative diseases. Lancet. 1:1989;642-645
24. Melov S., Schneider J.A., Day B.J., Hinerfeld D., Coskun P., Mirra S.S., Crapo J.D., Wallace D.C. A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat. Genet. 18:1998;159-163
25. Milano J., Day B.J. A catalytic antioxidant metalloporphyrin blocks hydrogen peroxide-induced mitochondrial DNA damage. Nucleic Acids Res. 28:2000;968-973
26. Mokrzycki M.H., Harris C., May H., Laut J., Palmisano J. Lactic acidosis associated with stavudine administration: a report of five cases. Clin. Infect. Dis. 30:2000;198-200
27. Pan-Zhou X.R., Cui L., Zhou X.J., Sommadossi J.P., Darley-Usmar V.M. Differential effects of antiretroviral nucleoside analogs on mitochondrial function in HepG2 cells. Antimicrob. Agents Chemother. 44:2000;496-503
28. Patel M.N. Metalloporphyrins improve the survival of Sod2-deficient neurons. Aging Cell. 2:2003;219-222
29. Patel M., Day B.J. Metalloporphyrin class of therapeutic catalytic antioxidants. Trends Pharmacol. Sci. 20:1999;359-364
30. Patel M., Day B.J., Crapo J.D., Fridovich I., McNamara J.O. Requirement for superoxide in excitotoxic cell death. Neuron. 16:1996;345-355
31. Prakash O., Teng S., Ali M., Zhu X., Coleman R., Dabdoub R.A., Chambers R., Aw T.Y., Flores S.C., Joshi B.H. The human immunodeficiency virus type 1 Tat protein potentiates zidovudine-induced cellular toxicity in transgenic mice. Arch. Biochem. Biophys. 343:1997;173-180
32. Raidel S.M., Haase C., Jansen N.R., Russ R.B., Sutliff R.L., Velsor L.W., Day B.J., Hoit B.D., Samarel A.M., Lewis W. Targeted myocardial transgenic expression of HIV Tat causes cardiomyopathy and mitochondrial damage. Am. J. Physiol.: Heart Circ. Physiol. 282:2002;H1672-H1678
33. Richter C. Oxidative damage to mitochondrial DNA and its relationship to ageing. Int. J. Biochem. Cell Biol. 27:1995;647-653
34. Robinson B.H. Use of fibroblast and lymphoblast cultures for detection of respiratory chain defects. Methods Enzymol. 264:1996;454-464
35. Roelofsen H., Vos T.A., Schippers I.J., Kuipers F., Koning H., Moshage H., Jansen P.L., Muller M. Increased levels of the multidrug resistance protein in lateral membranes of proliferating hepatocyte-derived cells. Gastroenterology. 112:1997;511-521
36. Schmidt E. Glutamate dehydrogenase. Bergmeyer H.U. Methods of Enzymatic Analysis. 1974;650-659 Academic Press, New York
37. Shigenaga M.K., Hagen T.M., Ames B.N. Oxidative damage and mitochondrial decay in aging. Proc. Natl. Acad. Sci. U.S.A. 91:1994;10771-10778
38. Skuta G., Fischer G.M., Janaky T., Kele Z., Szabo P., Tozser J., Sumegi B. Molecular mechanism of the short-term cardiotoxicity caused by 2′,3′-dideoxycytidine (ddC): modulation of reactive oxygen species levels and ADP-ribosylation reactions. Biochem. Pharmacol. 58:1999;1915-1925
39. Sohal R.S., Brunk U.T. Mitochondrial production of pro-oxidants and cellular senescence. Mutat. Res. 275:1992;295-304
40. Solas C., Li Y.F., Xie M.Y., Sommadossi J.P., Zhou X.J. Intracellular nucleotides of (-)-2′,3′-deoxy-3′-thiacytidine in peripheral blood mononuclear cells of a patient infected with human immunodeficiency virus. Antimicrob. Agents Chemother. 42:1998;2989-2995
41. Sutliff R.L., Dikalov S., Weiss D., Parker J., Raidel S., Racine A.K., Russ R., Haase C.P., Taylor W.R., Lewis W. Nucleoside reverse transcriptase inhibitors impair endothelium-dependent relaxation by increasing superoxide. Am. J. Physiol.: Heart Circ. Physiol. 283:2002;H2363-H2370
42. Szabados E., Fischer G.M., Toth K., Csete B., Nemeti B., Trombitas K., Habon T., Endrei D., Sumegi B. Role of reactive oxygen species and poly-ADP-ribose polymerase in the development of AZT-induced cardiomyopathy in rat. Free Radical Biol. Med. 26:1999;309-317
43. Taylor E.R., Hurrell F., Shannon R.J., Lin T.K., Hirst J., Murphy M.P. Reversible glutathionylation of complex I increases mitochondrial superoxide formation. J. Biol. Chem. 278:2003;19603-19610
44. Velsor L.W., van Heeckeren A., Day B.J. Antioxidant imbalance in the lungs of cystic fibrosis transmembrane conductance regulator protein mutant mice. Am. J. Physiol.: Lung Cell. Mol. Physiol. 281:2001;L31-L38
45. Walker U.A., Setzer B., Venhoff N. Increased long-term mitochondrial toxicity in combinations of nucleoside analogue reverse-transcriptase inhibitors. AIDS. 16:2002;2165-2173
46. Yamaguchi T., Katoh I., Kurata S. Azidothymidine causes functional and structural destruction of mitochondria, glutathione deficiency and HIV-1 promoter sensitization. Eur. J. Biochem. 269:2002;2782-2788