A truncated form of DNA topoisomerase IIβ associates with the mtDNA genome in mammalian mitochondria

European Journal of Biochemistry

Volumn 270, Issue 20, 2003, Pages 4173-4186

  Low, Robert L ^a   Orton, Shayla ^a   Friedman, David B ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Mitochondrial DNA; Mitochondrial DNA topoisomerase; mtDNA replication; Type II DNA topoisomerase

Indexed keywords

ADENOSINE TRIPHOSPHATE; DNA; DNA TOPOISOMERASE (ATP HYDROLYSING); DNA TOPOISOMERASE INHIBITOR; ENZYME; ETOPOSIDE; MAGNESIUM; MITOCHONDRIAL DNA; POLYCLONAL ANTIBODY; PROTEIN;

ARTICLE; CELL ACTIVITY; CELL NUCLEUS; CHEMICAL REACTION; ENZYME ACTIVITY; ENZYME SUBUNIT; GENOME; IN VITRO STUDY; INHIBITION KINETICS; KINETOPLAST; MAMMAL; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; RELAXATION TRAINING;

AMINO ACID SEQUENCE; ANIMALS; CATTLE; DNA TOPOISOMERASES, TYPE II; DNA, MITOCHONDRIAL; DNA-BINDING PROTEINS; MASS SPECTROMETRY; MITOCHONDRIA; MOLECULAR SEQUENCE DATA;

BOVINAE; EUKARYOTA; MAMMALIA; PROTOZOA;

EID: 0142088886     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03814.x     Document Type: Article

References (69)

1. Clayton, D.A. (1991) Replication and transcription of vertebrate mitochondrial DNA. Ann. Rev. Cell Biol. 7, 453-478.
2. Chomyn, A., Mariottini, P., Cleeter, M.W., Ragan, C.I., Matsuno-Yagi, A., Hatefi, Y., Doolittle, R.F. & Attardi, G. (1985) Six unidentified reading frames of human mitochondrial DNA encode components of the respiratory-chain NADH dehydrogenase. Nature 314, 592-597.
3. Farr, C.L., Yang, Y. & Kaguni, L.S. (1999) Functional interactions of mitochondrial DNA polymerase and single-stranded DNA-binding protein: template-primer DNA binding and initiation and elongation of DNA strand synthesis. J. Biol. Chem. 274, 14779-14785.
4. Carrodeguas, J.A., Kobayashi, R., Lim, S.E., Copeland, W.C. & Bogenhagen, D.E. (1999) The accessory subunit of Xenopus laevis mitochondrial DNA polymerase gamma increases processivity of the catalytic subunit of human DNA polymerase gamma and is related to class II aminoacyl-tRNA synthetases. Mol. Cell Biol. 19, 4039-4046.
5. Graziewicz, M.A., Day, B.J. & Copeland, W.C. (2002) The mitochondrial DNA polymerase as a target of oxidative damage. Nucleic Acids Res. 30, 2817-2824.
6. Johnson, A.A., Tsai, Y.C., Graves, S.W. & Johnson, K.A. (2000) Human mitochondrial DNA polymerase holoenzyme: reconstitution and characterization. Biochemistry 39, 1702-1708.
7. Wang, J.C. (1996) DNA topoisomerases. Annu. Rev. Biochem. 65, 635-692.
8. Brown, P.O. & Cozzarelli, N.R. (1979) A sign inversion mechanism for enzymatic supercoiling of DNA. Science 206, 1081-1083.
9. Liu, L.F., Liu, C-C. & Alberts, B.M. (1980) Type II DNA topoisomerases: enzymes that can unknot a topologically knotted DNA molecule via a reversible double-strand break. Cell 19, 697-707.
10. Watt, P.M. & Hickson, I.D. (1994) Structure and function of type II DNA topoisomerases. Biochem. J. 303, 681-695.
11. Austin, C.A. & Marsh, K.L. (1998) Eukaryotic DNA topoisomerase II beta. Bioessays 20, 215-226.
12. Chen, A.Y. & Liu, L.F. (1994) DNA topoisomerases: essential enzymes and lethal target. Annu. Rev. Pharmacol. Toxicol. 34, 191-218.
13. Zhang, H., Barceló, J.M. Lee, B., Kohlhagen, G., Zimonjic, D.B., Popescu, N.C. & Pommier, Y. (2001) Human mitochondrial topoisomerase I. Proc. Natl Acad. Sci. USA 98, 10608-10613.
14. Brun, G., Vannier, P., Scovassi, I. & Callen, J.C. (1981) DNA topoisomerase I from mitochondria of Xenopus laevis oocytes. Eur. J. Biochem. 118, 407-415.
15. Fairfield, F.R., Bauer, W.R. & Simpson, M.V. (1985) Studies on mitochondrial type I topoisomerase and on its function. Biochim. Biophys. Acta 824, 45-57.
16. Lin, J.H. & Castora, F.J. (1995) Response of purified mitochondrial DNA topoisomerase I from bovine liver to camptothecin and m-AMSA. Arch. Biochem. Biophys. 324, 293-299.
17. Lazarus, G.M., Henrich, J.P., Kelly, W.G., Schmitz, S.A. & Castora, F.J. (1987) DNA topoisomerase I from calf thymus mitochondria is associated with a DNA binding, inner membrane protein. Biochemistry 26, 6195-6203.
18. Tua, A., Wang, J., Kulpa, V. & Wernette, C.M. (1997) Mitochondrial DNA topoisomerase I of Saccharomyces cerevisiae. Biochemie 19, 341-350.
19. Kosovsky, M.J. & Soslau, G. (1991) Mitochondrial DNA topoisomerase I from human platelets. Biochim. Biophys. Acta 1078, 56-62.
20. Wang, Y., Lyu, Y.L. & Wang, J.C. (2002) Dual localization of human DNA topoisomerase IIIα to mitochondria and nucleus. Proc. Natl Acad. Sci. USA 99, 12114-12119.
21. Melendy, T. & Ray, D.S. (1989) Novobiocin affinity purification of a mitochondrial type II topoisomerase from the trypanosomatid Crithidia fasciculate. J. Biol. Chem. 264, 1870-1876.
22. Shapiro, T.A. & Englund, P.A. (1995) The structure and replication of kinetoplast DNA. Annu. Rev. Microbiol. 49, 117-143.
23. Melendy, T., Sheline, C. & Ray, D.S. (1988) Localization of a type II DNA topoisomerase to two sites at the periphery of the kinetoplast DNA of Crithidia fasciculate. Cell 55, 1083-1088.
24. Shapiro, T.A., Klein, V.A. & Englund, P.T. (1989) Drug-promoted cleavage of kinetoplast DNA minicircles: evidence for type II topoisomerase activity in trypanosome mitochondria. J. Biol. Chem. 264, 4173-4178.
25. Ray, D.S., Hines, J.C. & Anderson, M. (1992) Kinetoplast-associated DNA topoisomerase in Crithidia fasciculate: crosslinking of mitochondrial topoisomerase II to both minicircles and maxicircles in cells treated with the topoisomerase inhibitor VP16. Nucleic Acids Res. 20, 3353-3356.
26. Wang, Z. & Englund, P.T. (2001) RNA interference of a trypanosome topoisomerase II causes progressive loss of mitochondrial DNA. EMBO J. 20, 4674-4683.
27. Komori, K., Kuroe, K., Yanagisawa, K. & Tanaka, Y. (1997) Cloning and characterization of the gene encoding a mitochondrially localized DNA topoisomerase II in Dictyostelium discoideum. Biochim. Biophys. Acta 1352, 63-72.
28. Chavalitshewinkoon-Petmitr, P., Worasing, R. & Wilairat, P. (2001) Partial purification of mitochondrial DNA topoisomerase II from Plasmodium falciparum and its sensitivity to inhibitors. Southeast Asian J. Trop. Med. Public Health 32, 733-738.
29. Castora, F.J., Lazarus, G.M. & Kunes, D. (1985) The presence of two mitochondrial DNA topoisomerases in human acute leukemia cells. Biochem. Biophys. Res. Commun. 130, 854-866.
30. Lin, J.-H. & Castora, F.J. (1991) DNA topoisomerase II from mammalian mitochondria is inhibited by the antitumor drugs, m-AMSA and VM-26. Biochem. Biophys. Res. Commun. 176, 690-697.
31. Lawrence, J.W., Claire, D.C., Weissig, V. & Rowe, T.C. (1996) Delayed cytotoxicity and cleavage of mitochondrial DNA in ciprofloxacin-treated mammalian cells. Mol. Pharmacol. 50, 1178-1188.
32. Mita, S., Rizzuto, R., Moraes, C.T., Shanske, S., Arnaudo, E., Fabrizi, G.M.; Koga, Y., DiMauro, S. & Shon, E.A. (1990) Recombination via flanking direct repeats is a major cause of large-scale deletions of human mitochondrial DNA. Nucleic Acids Res. 18, 561-567.
33. Blok, R.B., Thorburn, D.R., Thompson, G.N. & Dahl, H.-H.M. (1995) A topoisomerase II cleavage site is associated with a novel mitochondrial DNA deletion. Hum. Genet. 95, 75-81.
34. Nielsen-Preiss, S.M. & Low, R.L. (2000) Identification of a beta-like DNA polymerase activity in bovine heart mitochondria. Arch. Biochem. Biophysc. 374, 229-240.
35. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
36. Shevchenko, A., Wilm, M., Vorm, O. & Mann, M. (1996) Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858.
37. Schnaitman, C. & Greenawalt, J.W. (1968) Enzymatic properties of the inner and outer membranes of rat liver mitochondria. J. Cell Biol. 38, 158-175.
38. Tewey, K.M., Chen, G.L., Nelson, E.M. & Liu, L.F. (1984) Intercalate antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II. J. Biol. Chem. 259, 9182-9187.
39. Drake, F.H., Zimmerman, J.P., McCabe, F.L., Bartus, H.F., Per, S.R., Sullivan, D.M., Ross, W.E., Mattern, M.R., Johnson, R.K., Crooke, S.T. & Mirabelli, C.K. (1987) Purification of topoisomerase II from amsacrine-resistant P388 leukemia cells: evidence for two forms of the enzyme. J. Biol. Chem. 262, 16739-16747.
40. Drake, F.H., Hofman, G.A., Bartus, H.F., Mattern, M.R., Crooke, S.T. & Mirabelli, C.K. (1989) Biochemical and pharmacological properties of p170 and p180 forms of topoisomerase II. Biochemistry 28, 8154-8160.
41. Halligan, B.D., Edwards, K.A. & Liu, L.F. (1985) Purification and characterization of a type II DNA topoisomerase from bovine calf thymus. J. Biol. Chem. 260, 2475-2482.
42. Austin, C.A., Barot, H., Margerrison, E.E.C., Hayes, M.V. & Fisher, L.M. (1989) Biochemical and immunological characterization of mammalian DNA topoisomerase II. Biochem. Soc. Trans. 17, 528-529.
43. Beaufay, H. (1972) Lysosomes, pp. 1-45. Elsevier, North-Holland, New York.
44. Quaglino, D. & Ronchetti, I.P. (2001) Cell death in the rat thymus: a minireview. Apoptosis 6, 389-401.
45. Austin, C.A., Marsh, K.L., Wasserman, R.A., Willmore, E., Sayer, P.J., Wang, J.C. & Fisher, L.M. (1995) Expression, domain structure, and enzymatic properties of an active recombinant human DNA topoisomerase II beta. J. Biol. Chem. 270, 15739-15746.
46. Shiozaki, K. & Yanagida, M. (1992) Functional dissection of the phosphorylated termini of fission yeast DNA topoisomerase II. J. Cell. Biol. 119, 1023-1036.
47. Crenshaw, D.G. & Hsieh, T.-S. (1993) Function of the hydrophilic carboxyl terminus of type II DNA topoisomerase from Drosophila melanogaster. I. In vitro studies. J. Biol. Chem. 268, 21328-21334.
48. Christensen, M.O., Larsen, M.K., Barthelmes, H.U., Hock, R., Andersen, C.L., Kjeldsen, E., Knudsen, B.R., Westergaard, O., Boege, F. & Mielke, C. (2002) Dynamics of human DNA topoisomerases IIα and IIα in living cells. J. Cell Biol. 157, 31-44.
49. Nishioka, K., Ohtsubo, T., Oda, H., Fujiwara, T., Kang, D., Sugimachi, K. & Nakabeppu, Y. (1999) Expression and differential intracellular localization of two major forms of human 8-oxoguanine DNA glycosylase encoded by alternatively spliced OGG1 mRNAs. Mol. Biol. Cell 10, 1637-1652.
50. Takao, M., Aburatani, H., Kobayashi, K. & Yasui, A. (1998) Mitochondrial targeting of human DNA glycosylases for repair of oxidative DNA damage. Nucleic Acids Res. 26, 2917-2922.
51. Lakshmipathy, U. & Campbell, C. (1999) The human DNA ligase III gene encodes nuclear and mitochondrial proteins. Mol. Cell Biol. 19, 3869-3876.
52. Coffey, G. & Campbell, C. (2000) An alternate form of Ku80 is required for DNA end-binding activity in mammalian mitochondria. Nucleic Acids Res. 28, 3793-3800.
53. Valgardsdottir, R., Brede, G., Eide, L.G., Frengen, E. & Prydz, H. (2001) Cloning and characterization of MDDX28, a putative DEAD-box helicase with mitochondrial and nuclear localization. J. Biol. Chem. 276, 32058-32063.
54. Casas, F., Daury, L., Grandemange, S., Busson, M., Seyer, P., Hatier, R., Carazo, A., Cabello, G. & Wrutniak-Cabello, C. (2003) Endocrine regulation of mitochondrial activity: involvement of truncated RXRα and c-Erb Aα1 proteins. FASEB J. 17, 426-436.
55. You, H.J., Swanson, R.L., Harrington, C., Corbett, A.H., Jinks-Robertson, S., Senturker, S., Wallace, S.S., Boiteux, S., Dizdaroglu, M. & Doetsch, P. (1999) Saccharomyces cerevisiae Ntg1p and Ntg2p: broad specificity N-glycosylases for the repair of oxidative DNA damage in the nucleus and mitochondria. Biochemistry 38, 11298-11306.
56. Lee, C.M., Sedman, J., Neupert, W. & Stuart, R.A. (1999) The DNA helicase, Hmi1p, is transported into mitochondria by a C-terminal cleavable targeting signal. J. Biol. Chem. 274, 20937-20942.
57. Folsch, H., Baume, B., Brunner, M., Neupert, W. & Stuart, R.A. (1998) C- to N-terminal translocation of preproteins into mitochondria. EMBO J. 17, 6508-6515.
58. Lang, A.J., Mirski, S.E.L. & Cummings, H.J., Yu Q., Gerlach, J.H. & Cole, S.P.C. (1998) Structural organization of the human TOP2A and TOP2B genes. Gene 21, 255-266.
59. Sng, J.-H., Heaton, V.J., Bell, M., Maini, P., Austin, C.A. & Fisher, L.M. (1999) Molecular cloning and characterization of the human topoisomerase IIα and IIβ genes: evidence for isoform evolution through gene duplication. Biochim. Biophys. Acta 1444, 395-406.
60. von Heijne, G. (1986) Mitochondrial targeting sequences may form amphiphilic helices. EMBO J. 5, 1335-1342.
61. Roise, D., Theiler, F., Horvath, S.J., Tomich, J.M., Richards, J.H., Allison, D.S. & Schatz, G. (1988) Amphiphilicity is essential for mitochondrial presequence function. EMBO J. 7, 649-653.
62. Claros, M.G. & Vincens, P. (1996) Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241, 779-786.
63. Peeter, N. & Small, I. (2001) Dual targeting to mitochondria and chloroplasts. Biochim. Biophys. Acta 1541, 54-63.
64. Zhou, N.E., Monera, O.D., Hodges, C.M. & Hodges, R.S. (1994) Alpha-helical propensities of amino acids in the hydrophobic face of an amphipathis alpha-helix. Protein Pept. Lett. 1, 114-119.
65. Hartmann, C. & Christen, P. (1991) Mitochondrial protein charge. Nature 352, 762-763.
66. Jaussi, R. (1995) Homologous nuclear-encoded mitochondrial and cytosolic isoproteins: a review of structure, biosynthesis, and genes. Eur. J. Biochem. 228, 551-561.
67. Holt, I.J., Lorimer, H.E. & Jacobs, H.T. (2000) Coupled leading-and lagging-strand synthesis of mammalian mitochondrial DNA. Cell 100, 515-524.
68. Yang, M.Y., Bowmaker, M., Reyes, A., Vergani, L., Angeli, P., Gringeri, E., Jacobs, H.T. & Holt, I.J. (2002) Biased incorporation of ribonucleotides on the mitochondrial 1-strand account for apparent strand-asymmetric DNA replication. Cell 111, 495-505.
69. Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.