DNA supercoiling suppresses real-time PCR: A new approach to the quantification of mitochondrial DNA damage and repair

Nucleic Acids Research

Volumn 35, Issue 4, 2007, Pages 1377-1388

  Chen, Jinsong ^a   Kadlubar, Fred F ^b   Chen, Junjian Z ^a  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROGEN PEROXIDE; MITOCHONDRIAL DNA; PLASMID DNA;

ACCURACY; ARTICLE; CANCER CELL; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DNA DAMAGE; DNA DENATURATION; DNA REPAIR; DNA SEQUENCE; DNA STRAND BREAKAGE; DNA SUPERCOILING; HUMAN; HUMAN CELL; IN VITRO STUDY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROSTATE CANCER; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SENSITIVITY ANALYSIS; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

CELL LINE, TUMOR; DNA DAMAGE; DNA REPAIR; DNA, MITOCHONDRIAL; DNA, NEOPLASM; DNA, SUPERHELICAL; FERROUS COMPOUNDS; HEAT; HUMANS; MALE; NUCLEIC ACID DENATURATION; PLASMIDS; POLYMERASE CHAIN REACTION; PROSTATIC NEOPLASMS;

EID: 34047130220     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm010     Document Type: Article

References (58)

1. Wallace,D.C. (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: A dawn for evolutionary medicine. Annu. Rev. Genet., 39, 359-407.
2. Polyak,K., Li,Y., Zhu,H., Lengauer,C., Willson,J.K., Markowitz,S.D., Trush,M.A., Kinzler,K.W. and Vogelstein,B. (1998) Somatic mutations of the mitochondrial genome in human colorectal tumours. Nat. Genet., 20, 291-293.
3. Penta,J.S., Johnson,F.M., Wachsman,J.T. and Copeland,W.C. (2001) Mitochondrial DNA in human malignancy. Mutat. Res., 488, 119-133.
4. Chen,J.Z. and Kadlubar,F.F. (2004) Mitochondrial mutagenesis and oxidative stress in human prostate cancer. J. Environ. Sci. Health C. Environ., 22, 1-12.
5. Anderson,S., Bankier,A.T., Barrell,B.G., de Bruijn,M.H., Coulson,A.R., Drouin,J., Eperon,I.C., Nierlich,D.P., Roe,B.A. et al. (1981) Sequence and organization of the human mitochondrial genome. Nature, 290, 457-465.
6. Clayton,D.A. (2000) Transcription and replication of mitochondrial DNA. Hum. Reprod., 15 (Suppl. 2) 11-17.
7. Turrens,J.F. and Boveris,A. (1980) Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem. J., 191, 421-427.
8. Richter,C. (1995) Oxidative damage to mitochondrial DNA and its relationship to aging. Int. J. Biochem. Cell Biol., 27, 647-653.
9. Toyokuni,S., Okamoto,K., Yodoi,J. and Hiai,H. (1995) Persistent oxidative stress in cancer. FEBS Lett., 358, 1-3.
10. Herrmann,P.C., Gillespie,J.W., Charboneau,L., Bichsel,V.E., Paweletz,C.P., Calvert,V.S., Kohn,E.C., Emmert-Buck,M.R., Liotta,L.A. et al. (2003) Mitochondrial proteome: Altered cytochrome c oxidase subunit levels in prostate cancer. Proteomics, 3, 1801-1810.
11. Fliss,M.S., Usadel,H., Caballero,O.L., Wu,L., Buta,M.R., Eleff,S.M., Jen,J. and Sidransky,D. (2000) Facile detection of mitochondrial DNA mutations in tumors and bodily fluids. Science, 287, 2017-2019.
12. Parrella,P., Xiao,Y., Fliss,M., Sanchez-Cespedes,M., Mazzarelli,P., Rinaldi,M., Nicol,T., Gabrielson,E., Cuomo,C. et al. (2001) Detection of mitochondrial DNA mutations in primary breast cancer and fine-needle aspirates. Cancer Res., 61, 7623-7626.
13. Chen,J.Z., Gokden,N., Greene,G.F., Mukunyadzi,P. and Kadlubar,F.F. (2002) Extensive somatic mitochondrial mutations in primary prostate cancer using laser capture microdissection. Cancer Res., 62, 6470-6474.
14. Richter,C., Park,J.W. and Ames,B.N. (1988) Normal oxidative damage to the mitochondrial and nuclear DNA is extensive. Proc. Natl. Acad. Sci. USA, 85, 6465-6467.
15. Mecocci,P., MacGarvey,U., Kaufman,A.E., Koontz,D., Schoffner,J.M., Wallace,D.C. and Beal,M.F. (1993) Oxidative damage to mitochondrial DNA shows marked age-dependent increases in human brain. Ann. Neurol., 34, 609-616.
16. Hayakawa,M., Ogawa,T., Sugiyama,S., Tanaka,M. and Ozawa,T. (1991) Massive conversion of guanine to 8-hydroxy-guanosine in mouse liver mitochondrial DNA by administration of azidothymidine. Biochem. Biophys. Res. Commun., 176, 87-93.
17. Ames,B.N., Shigenaga,M.K. and Hagen,T.M. (1993) Oxidants antioxidants and the degenerative diseases of aging. Proc. Natl. Acad. Sci. USA, 90, 7915-7922.
18. Yakes,F.M. and Van Houten,B. (1997) Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc. Natl. Acad. Sci. USA, 94, 514-519.
19. Santos,J.H., Hunakova,L., Chen,Y., Bortner,C. and Van Houten,B. (2003) Cell sorting experiments link persistent mitochondrial DNA damage with loss of mitochondrial membrane potential and apoptotic cell death. J. Biol. Chem., 278, 1728-1734.
20. Radloff,R., Bauer,W. and Vinograd,J. (1967) A dye-buoyant-density method for the detection and isolation of closed circular duplex DNA: The closed circular DNA in HeLa cells. Proc. Natl. Acad. Sci. USA, 57, 1514-1521.
21. Robberson,D.L. and Clayton,D.A. (1972) Replication of mitochondrial DNA in mouse L cells and their thymidine kinasederivatives: Displacement replication on a covalently-closed circular template. Proc. Natl. Acad. Sci. USA, 69, 3810-3814.
22. Bogenhagen,D. and Clayton,D.A. (1978) Mechanism of mitochondrial DNA replication in mouse L-cells: Introduction of superhelical turns into newly replicated molecules. J. Mol. Biol., 119, 69-81.
23. Clayton,D.A. (1982) Replication of animal mitochondrial DNA. Cell, 28, 693-705.
24. Singh,G., Hauswirth,W.W., Ross,W.E. and Neims,A.H. (1985) A method for assessing damage to mitochondrial DNA caused by radiation and epichlorohydrin. Mol. Pharmacol., 27, 167-170.
25. Lim,L.O. and Neims,A.H. (1987) Mitochondrial DNA damage by bleomycin. Biochem. Pharmacol., 36, 2769-2774.
26. Hruszkewycz,A.M. (1988) Evidence for mitochondrial DNA damage by lipid peroxidation. Biochem. Biophys. Res. Commun., 153, 191-197.
27. Itoh,H., Shioda,T., Matsura,T., Koyama,S., Nakanishi,T., Kajiyama,G. and Kawasaki,T. (1994) Iron ion induces mitochondrial DNA damage in HTC rat hepatoma cell culture - role of antioxidants in mitochondrial DNA protection from oxidative stresses. Arch. Biochem. Biophys., 313, 120-125.
28. Yaffee,M., Walter,P., Richter,C. and Muller,M. (1996) Direct observation of iron-induced conformational changes of mitochondrial DNA by high-resolution field-emission in-lens scanning electron microscopy. Proc. Natl. Acad. Sci. USA, 93, 5341-5346.
29. Asin,J., Perez-Martos,A., Fernandez-Silva,P., Montoya,J. and Andreu,A.L. (2000) Iron(II) induces changes in the conformation of mammalian mitochondrial DNA resulting in a reduction of its transcriptional rate. FEBS Lett., 480, 161-164.
30. Walter,P.B., Knutson,M.D., Paler-Martinez,A., Lee,S., Xu,Y., Viteri,F.E. and Ames,B.N. (2002) Iron deficiency and iron excess damage mitochondria and mitochondrial DNA in rats. Proc. Natl. Acad. Sci. USA, 99, 2264-2269.
31. Santos,J.H., Mandavilli,B.S. and Van Houten,B. (2002) Measuring oxidative mtDNA damage and repair using quantitative PCR. Methods Mol. Biol., 197, 159-176.
32. Higuchi,R., Fockler,C., Dollinger,G. and Watson,R. (1993) Kinetic PCR analysis: Real-time monitoring of DNA amplification reactions. Biotechnology (NY), 11, 1026-1030.
33. Heid,C.A., Stevens,J., Livak,K.J. and Williams,P.M. (1996) Real time quantitative PCR. Genome Res., 6, 986-994.
34. Bustin,S.A. (2000) Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol., 25, 169-193.
35. Szuhai,K., Ouweland,J., Dirks,R., Lemaitre,M., Truffert,J., Janssen,G., Tanke,H., Holme,E., Maassen,J. et al. (2001) Simultaneous A8344G heteroplasmy and mitochondrial DNA copy number quantification in myoclonus epilepsy and ragged-red fibers (MERRF) syndrome by a multiplex molecular beacon based realtime fluorescence PCR. Nucleic Acids Res., 29, e13.
36. Gahan,M.E., Miller,F., Lewin,S.R., Cherry,C.L., Hoy,J.F., Mijch,A., Rosenfeldt,F. and Wesselingh,S.L. (2001) Quantification of mitochondrial DNA in peripheral blood mononuclear cells and subcutaneous fat using real-time polymerase chain reaction. J. Clin. Virol., 22, 241-247.
37. Cote,H.C., Brumme,Z.L., Craib,K.J., Alexander,C.S., Wynhoven,B., Ting,L., Wong,H., Harris,M., Harrigan,P.R. et al. (2002) Changes in mitochondrial DNA as a marker of nucleoside toxicity in HIV-infected patients. N. Engl. J. Med., 346, 811-820.
38. von Wurmb-Schwark,N., Higuchi,R., Fenech,A.P., Elfstroem,C., Meissner,C., Oehmichen,M. and Cortopassi,G.A. (2002) Quantification of human mitochondrial DNA in a real time PCR. Forensic Sci. Int., 126, 34-39.
39. Mambo,E., Gao,X., Cohen,Y., Guo,Z., Talalay,P. and Sidransky,D. (2003) Electrophile and oxidant damage of mitochondrial DNA leading to rapid evolution of homoplasmic mutations. Proc. Natl. Acad. Sci. USA, 100, 1838-1843.
40. Liu,C.S., Tsai,C.S., Kuo,C.L., Chen,H.W., Lii,C.K., Ma,Y.S. and Wei,Y.H. (2003) Oxidative stress-related alteration of the copy number of mitochondrial DNA in human leukocytes. Free Radic. Res., 37, 1307-1317.
41. Ayala-Torres,S., Chen,Y., Svoboda,T., Rosenblatt,J. and Van Houten,B. (2000) Analysis of gene-specific DNA damage and repair using quantitative polymerase chain reaction. Methods, 22, 135-147.
42. Svoboda,P. and Harms-Ringdahl,M. (2002) Kinetics of phosphatemediated oxidation of ferrous iron and formation of 8-oxo-2′-deoxyguanosine in solutions of free 2′-deoxyguanosine and calf thymus DNA. Biochim. Biophys. Acta., 1571, 45-54.
43. Djuric,Z., Potter,D.W., Taffe,B.G. and Strasburg,G.M. (2001) Comparison of iron-catalyzed DNA and lipid oxidation. J. Biochem. Mol. Toxicol., 15, 114-119.
44. Pfaffl,M.W., Horgan,G.W. and Dempfle,L. (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res., 30, e36.
45. Pruss,G.J., Manes,S.H. and Drlica,K. (1982) Escherichia coli DNA topoisomerase I mutants: Increased supercoiling is corrected by mutations near gyrase genes. Cell, 31, 35-42.
46. Pruss,G.J. (1985) DNA topoisomerase I mutants: Increased heterogeneity in linking number and other replicon-dependent changes in DNA supercoiling. J. Mol. Biol., 185, 51-63.
47. Schneider,J.E., Browning,M.M. and Floyd,R.A. (1988) Ascorbate/iron mediation of hydroxyl free radical damage to PBR322 plasmid DNA. Free Radic. Biol. Med., 5, 287-295.
48. Rodriguez,H., Holmquist,G.P., D'Agostino,R. Jr., Keller,J. and Ackman,S.A. (1997) Metal ion-dependent hydrogen peroxide-induced DNA damage is more sequence specific than metal specific. Cancer Res., 57, 2394-2403.
49. Kozyavkin,S.A., Pushkin,A.V., Eiserling,F.A., Stetter,K.O., Lake,J.A. and Slesarev,A.I. (1996) DNA enzymology above 1008C. J. Biol. Chem., 270, 13593-13595.
50. LeDoux,S.P. and Wilson,G.L. (2001) Base excision repair of mitochondrial DNA damage in mammalian cells. Prog. Nucleic Acid Res. Mol. Biol., 68, 273-284.
51. Mandavilli,B.S., Santos,J.H. and Van Houten,B. (2002) Mitochondrial DNA repair and aging. Mutat. Res., 509, 127-151.
52. Driggers,W.J., Holmquist,G.P., LeDoux,S.P. and Wilson,G.L. (1997) Mapping frequencies of endogenous oxidative damage and the kinetic response to oxidative stress in a region of rat mtDNA. Nucleic Acids Res., 25, 4362-4369.
53. Harrison,J.F., Hollensworth,S.B., Spitz,D.R., Copeland,W.C., Wilson,G.L. and LeDoux,S.P. (2005) Oxidative stress-induced apoptosis in neurons correlates with mitochondrial DNA base excision repair pathway imbalance. Nucleic Acids Res., 33, 4660-4671.
54. Palapattu,G.S., Sutcliffe,S., Bastian,P.J., Platz,E.A., De Marzo,A.M., Isaacs,W.B. and Nelson,W.G. (2005) Prostate carcinogenesis and inflammation: Emerging insights. Carcinogenesis, 26, 1170-1181.
55. Chen,J.Z., Gokden,N., Greene,G.F., Green,G. and Kadlubar,F.F. (2003) Simultaneous generation of multiple mitochondrial DNA mutations in human prostate tumors suggests mitochondrial hypermutagenesis. Carcinogenesis, 24, 1481-1487.
56. Parr,R.L., Dakubo,G.D., Crandall,K.A., Maki,J., Reguly,B., Aguirre,A., Wittock,R., Robinson,K., Alexander,J.S. et al. (2006) Somatic mitochondrial DNA mutations in prostate cancer and normal appearing adjacent glands in comparison to age-matched prostate samples without malignant histology. J. Mol. Diagn., 8, 312-319.
57. Malins,D.C., Johnson,P.M., Barker,E.A., Polissar,N.L., Wheeler,T.M. and Anderson,K.M. (2003) Cancer-related changes in prostate DNA as men age and early identification of metastasis in primary prostate tumors. Proc. Natl. Acad. Sci. USA, 100, 5401-5406. Epub 2003 Apr 17.
58. Malins,D.C., Gilman,N.K., Green,V.M., Wheeler,T.M., Barker,E.A., Vinson,M.A., Sayeeduddin,M., Hellstrom,K.E. and Anderson,K.M. (2004) Metastatic cancer DNA phenotype identified in normal tissues surrounding metastasizing prostate carcinomas. Proc. Natl. Acad. Sci. USA, 101, 11428-11431. Epub 2004 Jul 27.