Transgene expression of Drosophila melanogaster nucleoside kinase reverses mitochondrial thymidine kinase 2 deficiency

Journal of Biological Chemistry

Volumn 288, Issue 7, 2013, Pages 5072-5079

  Krishnan, Shuba ^a   Zhou, Xiaoshan ^a   Paredes, João A ^a   Kuiper, Raoul V ^a   Curbo, Sophie ^a   Karlsson, Anna ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA MELANOGASTER; MITOCHONDRIAL DNA (MTDNA); THYMIDINE KINASE; TRANSGENE EXPRESSION;

MITOCHONDRIA; NUCLEIC ACIDS; NUCLEOTIDES; TISSUE;

ENZYMES;

MITOCHONDRIAL DNA; NUCLEOSIDE KINASE; PHOSPHOTRANSFERASE; THYMIDINE KINASE; THYMIDINE KINASE 2; THYMIDINE PHOSPHATE; THYMIDINE TRIPHOSPHATE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME DEFICIENCY; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; GENE DOSAGE; GENE EXPRESSION; GENE THERAPY; MITOCHONDRIAL DNA DEPLETION; MITOCHONDRIAL THYMIDINE KINASE 2 DEFICIENCY; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE DISTRIBUTION; TRANSGENE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DNA, MITOCHONDRIAL; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENOTYPE; MICE; MICE, TRANSGENIC; MITOCHONDRIA; NUCLEOTIDES; PHOSPHOTRANSFERASES; POINT MUTATION; THYMIDINE KINASE; TRANSGENES;

EID: 84874056352     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.437152     Document Type: Article

References (38)

1. Bridges, E. G., Jiang, Z., and Cheng, Y. C. (1999) Characterization of a dCTP transport activity reconstituted from human mitochondria. J. Biol. Chem. 274, 4620-4625
2. Ferraro, P., Nicolosi, L., Bernardi, P., Reichard, P., and Bianchi, V. (2006) Mitochondrial deoxynucleotide pool sizes in mouse liver and evidence for a transport mechanism for thymidine monophosphate. Proc. Natl. Acad. Sci. U.S.A. 103, 18586-18591
3. Anderson, D. D., and Quintero., C. M., and Stover, P. J. (2011) Identification of a de novo thymidylate biosynthesis pathway in mammalian mitochondria. Proc. Natl. Acad. Sci. U.S.A. 108, 15163-15168
4. Pontarin, G., Ferraro, P., Håkansson, P., Thelander, L., Reichard, P., and Bianchi, V. (2007) p53R2-dependent ribonucleotide reduction provides deoxyribonucleotides in quiescent human fibroblasts in the absence of induced DNA damage. J. Biol. Chem. 282, 16820-16828
5. Pontarin, G., Ferraro, P., Bee, L., Reichard, P., and Bianchi, V. (2012) Mammalian ribonucleotide reductase subunit p53R2 is required for mitochon-drial DNA replication and DNA repairin quiescent cells. Proc. Natl. Acad. Sci. U.S.A. 109, 13302-13307
6. Zhou, X., Johansson, M., Solaroli, N., Rozell, B., Grandien, A., and Karlsson, A. (2010) Hematopoiesis in the thymidine kinase 2 deficient mouse model of mitochondrial DNA depletion syndrome. J. Inherit. Metab. Dis. 33, 231-236
7. Zhou, X., Solaroli, N., Bjerke, M., Stewart, J. B., Rozell, B., Johansson, M., and Karlsson, A. (2008) Progressive loss of mitochondrial DNA in thymidine kinase 2-deficient mice. Hum. Mol. Genet. 17, 2329-2335
8. Mandel, H., Szargel, R., Labay, V., Elpeleg, O., Saada, A., Shalata, A., Anbinder, Y., Berkowitz, D., Hartman, C., Barak, M., Eriksson, S., and Cohen, N. (2001) The deoxyguanosine kinase gene is mutated in individuals with depleted hepatocerebral mitochondrial DNA. Nat. Genet. 29, 337-441
9. Correction Nat. Genet. 29, 491
10. Bourdon, A., Minai, L., Serre, V., Jais, J. P., Sarzi, E., Aubert, S., Chrétien, D., de Lonlay, P., Paquis-Flucklinger, V., Arakawa, H., Nakamura, Y., Munnich, A., and Rötig, A. (2007) Mutation of RRM2B, encoding p53-controlled ribonucleotide reductase (p53R2), causes severe mitochondrial DNA depletion. Nat. Genet. 39, 776-780
11. Suomalainen, A., and Isohanni, P. (2010) Mitochondrial DNA depletion syndromes - Many genes, common mechanisms. Neuromuscul. Disord. 20, 429-437
12. Saada, A., Shaag, A., Mandel, H., Nevo, Y., Eriksson, S., and Elpeleg, O. (2001) Mutant mitochondrial thymidine kinase in mitochondrial DNA depletion myopathy. Nat. Genet. 29, 342-344
13. Wang, L. (2010) Deoxynucleoside salvage enzymes and tissue specific mitochondrial DNA depletion. Nucleosides Nucleotides Nucleic Acids 29, 370-381
14. Meier, C., and Jessen., H. J., and Balzarini, J. (2008) Nucleoside diphosphate prodrugs. Nucleic Acids Symp. Ser. (Oxf.) 83-84
15. Mehellou, Y., Balzarini, J., and McGuigan, C. (2009) Aryloxy phosphora-midate triesters: atechnology for delivering monophosphorylated nucleosides and sugars into cells. Chemmedchem 4, 1779-1791
16. Johansson, M., van Rompay, A. R., Degrève, B., Balzarini, J., and Karlsson, A. (1999) Cloning and characterization of the multisubstrate deoxyribo-nucleoside kinase of Drosophila melanogaster. J. Biol. Chem. 274, 23814-23819
17. Munch-Petersen, B., Piskur, J., and Sondergaard, L. (1998) Four deoxy-nucleoside kinase activities from Drosophila melanogaster are contained within a single monomeric enzyme, a new multifunctional deoxynucleoside kinase. J. Biol. Chem. 273, 3926-3931
18. Solaroli, N., Johansson, M., Balzarini, J., and Karlsson, A. (2007) Enhanced toxicity of purine nucleoside analogs in cells expressing Drosophila melanogaster nucleoside kinase mutants. Gene Ther. 14, 86-92
19. Solaroli, N., Zheng, X., Johansson, M., Balzarini, J., and Karlsson, A. (2007) Mitochondrial expression of the Drosophila melanogaster multisubstrate deoxyribonucleoside kinase. Mol. Pharmacol. 72, 1593-1598
20. Zheng, X., Johansson, M., and Karlsson, A. (2001) Bystander effects of cancer cell lines transduced with the multisubstrate deoxyribonucleoside kinase of Drosophila melanogaster and synergistic enhancement by hydroxyurea. Mol. Pharmacol. 60, 262-266
21. Zheng, X., Johansson, M., and Karlsson, A. (2000) Retroviral transduction of cancer cell lines with the gene encoding Drosophila melanogaster multisubstrate deoxyribonucleoside kinase. J. Biol. Chem. 275, 39125-39129
22. Ferraro, P., Franzolin, E., Pontarin, G., Reichard, P., and Bianchi, V. (2010) Quantitation of cellular deoxynucleoside triphosphates. Nucleic Acids Res. 38, e85
23. Sherman, P. A., and Fyfe, J. A. (1989) Enzymatic assay for deoxyribo-nucleoside triphosphates using synthetic oligonucleotides as template primers. Anal. Biochem. 180, 222-226
24. Bertoli, A., Franco, M., Balzarini, J., Johansson, M., and Karlsson, A. (2005) Altered deoxyribonucleotide pools in T-lymphoblastoid cells expressing the multisubstrate nucleoside kinase of Drosophila melanogaster. FEBS J. 272, 3918-3928
25. Munch-Petersen, B., Knecht, W., Lenz, C., Søndergaard, L., and Piskur, J. (2000) Functional expression of a multisubstrate deoxyribonucleoside kinase from Drosophila melanogaster and its C-terminal deletion mutants. J. Biol. Chem. 275, 6673-6679
26. Eriksson, S., Arnér, E., Spasokoukotskaja, T., Wang, L., Karlsson, A., Brosjö, O., Gunvén, P., Julusson, G., and Liliemark, J. (1994) Properties and levels of deoxynucleoside kinases in normal and tumor cells; implications for chemotherapy. Adv. Enzyme Regul. 34, 13-25
27. Wang, L., and Eriksson, S. (2010) Tissue specific distribution of pyrimidine deoxynucleoside salvage enzymes shed light on the mechanism of mitochondrial DNA depletion. Nucleosides Nucleotides Nucleic Acids 29, 400-403
28. Babinet, C. (2000) Transgenic mice: an irreplaceable tool for the study of mammalian development and biology. J. Am. Soc. Nephrol. 11, S88-S94
29. Franzolin, E., Rampazzo, C., Pérez-Pérez, M.J., Hernández, A. I., Balzarini, J., and Bianchi, V. (2006) Bromovinyl-deoxyuridine: A selective substrate for mitochondrial thymidine kinase in cell extracts. Biochem. Biophys. Res. Commun. 344, 30-36
30. Wang, L., and Eriksson, S. (2008) 5-Bromovinyl 2'-deoxyuridine phosphorylation by mitochondrial and cytosolic thymidine kinase (TK2 and TK1) and its use in selective measurement of TK2 activity in crude extracts. Nucleosides Nucleotides Nucleic Acids 27, 858-862
31. m 5'-nucleotidase and 5'(3')-deoxyribonucleotidase in substrate cycles involved in nucleotide metabolism. J. Biol. Chem. 276, 6185-6190
32. Rampazzo, C, Fabris, S., Franzolin, E., Crovatto, K., Frangini, M., and Bianchi, V. (2007) Mitochondrial thymidine kinase and the enzymatic network regulating thymidine triphosphate pools in cultured human cells. J. Biol. Chem. 282, 34758-34769
33. Zegerman, P., and Diffley, J. F. X. (2009) DNA replication as a target of the DNA damage checkpoint. DNA Repair 8, 1077-1088
34. Kumar, D., Viberg, J., Nilsson, A. K., and Chabes, A. (2010) Highly mutagenic and severely imbalanced dNTP pools can escape detection by the S-phase checkpoint. Nucleic Acids Res. 38, 3975-3983
35. Valentino, M. L., Martí, R., Tadesse, S., López, L. C, Manes, J. L., Lyzak, J., Hahn, A., Carelli, V., and Hirano, M. (2007) Thymidine and deoxyuridine accumulate in tissues of patients with mitochondrial neurogastrointestinal encephalomyopathy (MNGIE). FEBSLett. 581, 3410-3414
36. López, L. C, Akman, H. O., García-Cazorla, A., Dorado, B., Martí, R., Nishino, I., Tadesse, S., Pizzorno, G., Shungu, D., Bonilla, E., Tanji, K., and Hirano, M. (2009) Unbalanced deoxynucleotide pools cause mitochondrial DNA instability in thymidine phosphorylase-deficient mice. Hum. Mol. Genet. 18, 714-722
37. González-Vioque, E., Torres-Torronteras, J., Andreu, A. L., and Martí, R. (2011) Limited dCTP availability accounts for mitochondrial DNA depletion in mitochondrial neurogastrointestinal encephalomyopathy (MNGIE). PLoS Genet. 7, e1002035
38. Gisch, N, Balzarini, J., and Meier, C. (2008) Studies on enzyme-cleavable dialkoxymethyl-cycloSaligenyl-2',3'-dideoxy-2',3'-didehydrothymidine monophosphates. J. Med. Chem. 51, 6752-6760