A Drosophila model of mitochondrial DNA replication: Proteins, genes and regulation

IUBMB Life

Volumn 57, Issue 8, 2005, Pages 555-561

  Garesse, Rafael ^a   Kaguni, Laurie S ^b  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b Michigan State University   (United States)

Author keywords

Drosophila; Mitochondrial DNA replication

Indexed keywords

AMINO ACID TRANSFER RNA LIGASE; DNA DIRECTED DNA POLYMERASE GAMMA; EXONUCLEASE; HELICASE; HOLOENZYME; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; POLYPEPTIDE; RIBOSOME RNA; RNA POLYMERASE II; TRANSFER RNA;

5' UNTRANSLATED REGION; AGING; APOPTOSIS; BIOGENESIS; DEVELOPMENTAL DISORDER; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA REPLICATION; DNA TRANSCRIPTION; DROSOPHILA; GENE EXPRESSION REGULATION; HOMEOSTASIS; MITOCHONDRIAL DNA DISORDER; NONHUMAN; OPEN READING FRAME; OXIDATIVE PHOSPHORYLATION; PATHOPHYSIOLOGY; REVIEW; RNA INTERFERENCE;

ANIMALS; DNA REPLICATION; DNA, MITOCHONDRIAL; DROSOPHILA; GENE EXPRESSION REGULATION; GENE ORDER; MITOCHONDRIAL DISEASES; MITOCHONDRIAL PROTEINS;

ANIMALIA;

EID: 25144455938     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1080/15216540500215572     Document Type: Review

References (42)

1. DiMauro, S., and Schon, E. A. (2003) Mitochondrial respiratory-chain diseases. New. Engl. J. Med. 348, 2656-2668.
2. Lowell, B. B., and Shulman, G. I. (2005) Mitochondrial dysfunction and type 2 diabetes. Science 307, 384-387.
3. Wilson, F. H., et al. (2004) A cluster of metabolic defects caused by mutation in a mitochondrial tRNA. Science 306, 1190-1194.
4. Timmis, J. N., Ayliffe, M. A., Huang, C. Y., and Martin, W. (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5, 123-135.
5. Garesse, R., and Vallejo, C. G. (2001) Animal mitochondrial biogenesis and function: a regulatory cross-talk between two genomes. Gene 263, 1-16.
6. Clayton, D.A. (2000) Vertebrate mitochondrial DNA-a circle of surprises. Exp. Cell Res. 255, 4-9.
7. Fish, J., Raule, N., and Attardi, G. (2004) Discovery of a major D-loop replication origin reveals two modes of human mtDNA synthesis. Science 306, 2098-2101.
8. Bogenhagen, D. F., and Clayton, D. A. (2003) The mitochondrial DNA replication bubble has not burst. Trends Biochem. Sci. 28, 357-360.
9. Holt, I. J., and Jacobs, H. T. (2003) Response: the mitochondrial DNA replication bubble has not burst. Trends Biochem. Sci. 28, 355-356.
10. Holt, I. J., Lorimer, H. E., and Jacobs, H. T. (2000) Coupled leading-and lagging-strand synthesis of mammalian mitochondrial DNA. Cell 100, 515-524.
11. Yang, M. Y., Bowmaker, M., Reyes, A., Vergani, L., Angeli, P., Gringeri, E., Jacobs, H. T., and Holt, I. J. (2002) Biased incorporation of ribonucleotides on the mitochondrial L-strand accounts for apparent strand-asymmetric DNA replication. Cell 111, 495-505.
12. Reyes, A., Yang, M., Bowmaker, M., and Holt, I. (2005) Bidirectional replication initiates at sites throughout the mitochondrial genome of birds. J. Biol. Chem. 280, 3242-3250.
13. Goddard, J. M., and Wolstenholme, D. R. (1978) Origin and direction of replication in mitochondrial DNA molecules from Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 75, 3886-3890.
14. Lewis, D. L., Farr, C. L., Farquhar, A. L., and Kaguni, L. S. (1994) Sequence, organization, and evolution of the A + T region of Drosophila melanogaster mitochondrial DNA. Mol. Biol. Evol. 11, 523-538.
15. Tsujino, F., Kosemura, A., Inohira, K., Hara, T., Otsuka, Y. F., Obara, M. K., and Matsuura, E. T. (2002) Evolution of the A + T-rich region of mitochondrial DNA in the melanogaster species subgroup of Drosophila. J. Mol. Evol. 55, 573-583.
16. Matsushima, Y., Garesse, R., and Kaguni, L. S. (2004) Drosophila mitochondrial transcription factor B2 regulates mitochondrial DNA copy number and transcription in schneider cells. J. Biol. Chem. 279, 26900-26905.
17. Matsushima, Y., Adán, C, Garesse, R., and Kaguni, L. S. (2005) Drosophila mitochondrial transcription factor B1 modulates mitochondrial translation but not transcription or DNA copy number in Schneider cells. J. Biol. Chem. 280, 16815-16820.
18. Kaguni, L. S. (2004) DNA polymerase g, the mitochondrial replicase. Annu. Rev. Biochem. 73, 293-320.
19. Wernette, C. M., and Kaguni, L. S. (1996) A mitochondrial DNA polymerase from embryos of Drosophila melanogaster. Purification, subunit structure, and partial characterization. J. Biol. Chem. 261, 14764-14770.
20. Olson, M. W., and Kaguni, L. S. (1992) 3′-5′ exonuclease in Drosophila mitochondrial DNA polymerase. Substrate specificity and functional coordination of nucleotide polymerization and mispair hydrolysis. J. Biol. Chem. 267, 23136-23142.
21. Kaguni, L. S., and Olson M. W. (1989) Mismatch-specific 3′-5′ exonuclease associated with the mitochondrial DNA polymerase from Drosophila embryos. Proc. Natl. Acad. Sci. USA 86, 6469-6473.
22. Lewis, D. L., Farr, C. L., Wang, Y., Lagina, A. T. III, and Kaguni, L. S. (1998) Catalytic subunit of mitochondrial DNA polymerase from Drosophila embryos: cloning, bacterial overexpression and biochemical characterization. J. Biol. Chem. 271, 23389-23394.
23. Fan, L., Sanschagrin, P. C., Kaguni, L. S., and Kuhn, L. A. (1999) The accessory subunit of mitochondrial DNA polymerase shares structural homology with aminoacyl-tRNA synthetases: Implications for a dual role as a primer recognition factor and processivity clamp. Proc. Natl. Acad. Sci. USA 96, 9527-9532.
24. Farr, C. L., Wang, Y., and 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.
25. Farr, C. L., Matsushima, Y., Lagina, A. T. III, Luo, N., and Kaguni, L. S. (2004) Physiological and biochemical defects in functional interactions of mitochondrial DNA polymerase and DNA-binding mutants of single-stranded DNA-binding protein. J. Biol. Chem. 279, 17047-17053.
26. Iyengar, B., Roote, J., and Campos, A. R. (1999) The tamas gene, identified as a mutation that disrupts larval behavior in drosophila melanogaster, codes for the mitochondrial DNA polymerase catalytic subunit (DNApol-gamma125). Genetics 153, 1809-1824.
27. Iyengar, B., Luo, N., Farr, C. L., Kaguni, L. S., and Campos, A. R. (2002) The accessory subunit of DNA polymerase gamma is essential for mitochondrial DNA maintenance and development in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 99, 4483-4488.
28. Maier, D., Farr, C. L., Poeck, B., Alahari, A., Vogel, M., Fisher, S., Kaguni, L. S., and Schneuwly, S. (2001). Mitochondrial single-stranded DNA-binding protein is required for mitochondrial DNA replication and development in Drosophila melanogaster. Mol. Biol. Cell 12, 821-830.
29. Lefai, E., Fernández-Moreno, M. A., Kaguni, L. S., and Garesse, R. (2000) The highly compact structure of the mitochondrial DNA polymerase genomic region of Drosophila melanogaster: functional and evolutionary implications. Insect Mol. Biol. 9, 315-322.
30. Ibba, M., and Soll, D. (2004) Aminoacyl-tRNAs: setting the limits of the genetic code. Genes Dev. 18, 731-738.
31. Lefai, E., Fernández-Moreno, M. A., Alahari, A., Kaguni, L. S., and Garesse, R. (2000) Differential regulation of the catalytic and accessory subunit genes of drosophila mitochondrial DNA polymerase. J. Biol. Chem. 275, 33123-33133.
32. Ruiz de Mena, I., Lefai, E., Garesse, R., and Kaguni, L.S. (2000) Regulation of mitochondrial single-stranded DNA-binding protein gene expression links nuclear and mitochondrial DNA replication in Drosophila. J. Biol. Chem. 275, 13628-13636.
33. Takata, K., Yoshida, H., Hirose, F., Yamaguchi, M., Kai, M., Oshige, M., Sakimoto, I., Koiwai, O., and Sakaguchi, K. (2001) Drosophila mitochondrial transcription factor A: characterization of its cDNA and expression pattern during development. Biochem. Biophys. Res. Commun. 287, 474-483.
34. Kelly, D. P., and Scarpulla, R. C. (2004) Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 18, 357-368.
35. Calzone, F. J., Hoog, C., Teplow, D. B., Cutting, A. E., Zeller, R. W., Britten, R. J., and Davidson, E. H. (1991) Gene regulatory factors of the sea urchin embryo. I. Purification by affinity chromatography and cloning of P3A2, a novel DNA-binding protein. Development 112, 335-350.
36. Sardiello, M., Tripoli, G., Romito, A., Minervini, C., Viggiano, L., Caggese, C., and Pesole, G. (2005) Energy biogenesis: one key for coordinating two genomes. Trends Genet. 21, 12-16.
37. Galloni, M. (2003) Bonsai, a ribosomal protein S15 homolog, involved in gut mitochondrial activity and systemic growth. Dev. Biol. 264, 482-494.
38. Fortini, M. E., and Bonini, N. M. (2000) Modeling human neurodegenerative diseases in Drosophila: on a wing and a prayer. Trends Genet. 16, 161-167.
39. Jacobs, H. T., Fernández-Ayala, D., Manjiry, S., Kemppainen, E., Toivonen, J. M., and O'Dell, K. M. (2004) Mitochondrial disease in flies. Biochim. Biophys. Acta 1659, 190-196.
40. Lefai, E., Calleja, M., Ruiz de Mena, I., Lagina, A. T. 3rd, Kaguni, L. S., and Garesse, R. (2000) Overexpression of the catalytic subunit of DNA polymerase gamma results in depletion of mitochondrial DNA in Drosophila melanogaster. Mol. Gen. Genet. 264, 37-46.
41. Trifunovic, A., Wrendenberg, A., Falkenberg, M., Spelbrink, J. N., Rovio, A. T., Bruder, C. E., Bohlooly, Y. M., Gidlof, S., Oldfors, A., Wibom, R., Tornell, J., Jacobs, H. T., and Larsson, N. G. (2004) Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429, 417-423.
42. Jacobs, H. T., (2003) The mitochondrial theory of aging: dead or alive? Aging Cell 2, 11-17.