Synthesis of mitochondrial DNA precursors during myogenesis, an analysis in purified C2C12 myotubes

Journal of Biological Chemistry

Volumn 288, Issue 8, 2013, Pages 5624-5635

  Frangini, Miriam ^a   Franzolin, Elisa ^a   Chemello, Francesco ^a   Laveder, Paolo ^a   Romualdi, Chiara ^a   Bianchi, Vera ^a   Rampazzo, Chiara ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DNA PRECURSORS; DOWN-REGULATION; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL DNA; MYOGENESIS; MYOTUBES; SIRNA SILENCING; SYNTHETIC ENZYMES;

BIOCHEMISTRY; BIOLOGY;

NUCLEIC ACIDS;

DEOXYGUANOSINE KINASE; MITOCHONDRIAL DNA; THYMIDINE KINASE;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; DNA SYNTHESIS; ENZYME ACTIVITY; GENE SILENCING; MITOCHONDRIAL DNA DEPLETION; MITOCHONDRION; MOUSE; MUSCLE DEVELOPMENT; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; TISSUE DIFFERENTIATION;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CYTOSOL; DNA, MITOCHONDRIAL; GENE SILENCING; MICE; MITOCHONDRIA; MITOCHONDRIAL DISEASES; MODELS, BIOLOGICAL; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; NUCLEIC ACID HYBRIDIZATION; NUCLEOTIDES; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RIBONUCLEOTIDES; RNA, SMALL INTERFERING;

EID: 84874306753     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.441147     Document Type: Article

References (58)

1. Moyes, C. D., Mathieu-Costello, O. A., Tsuchiya, N., Filburn, C., and Hansford, R. G. (1997) Mitochondrial biogenesis during cellular differentiation. Am. J. Physiol. 272, C1345-51
2. Kraft, C. S., LeMoine, C. M., Lyons, C. N., Michaud, D., Mueller, C. R., and Moyes, C. D. (2006) Control of mitochondrial biogenesis during myogenesis. Am. J. Physiol. Cell Physiol. 290, C1119-27
3. Spinazzola, A., Invernizzi, F., Carrara, F., Lamantea, E., Donati, A., Dirocco, M., Giordano, I., Meznaric-Petrusa, M., Baruffini, E., Ferrero, I., and Zeviani, M. (2009) Clinical and molecular features of mitochondrial DNA depletion syndromes. J. Inherit. Metab. Dis. 32, 143-158
4. Ylikallio, E., and Suomalainen, A. (2012) Mechanisms of mitochondrial diseases. Ann. Med. 44, 41-59
5. Nordlund, P., and Reichard, P. (2006) Ribonucleotide reductases. Annu. Rev. Biochem. 75, 681-706
6. Reichard, P. (1988) Interactions between deoxyribonucleotide and DNA synthesis. Annu. Rev. Biochem. 57, 349-374
7. Björklund, S., Skog, S., Tribukait, B., and Thelander, L. (1990) S-phasespecific expression of mammalian ribonucleotide reductase R1 and R2 subunit mRNAs. Biochemistry. 29, 5452-5458
8. Chabes, A. L., Björklund, S., and Thelander, L. (2004) S Phase-specific transcription of the mouse ribonucleotide reductase R2 gene requires both a proximal repressive E2F-binding site and an upstream promoter activating region. J. Biol. Chem. 279, 10796-10807
9. Kauffman, M. G., and Kelly, T. J. (1991) Cell cycle regulation of thymidine kinase: Residues near the carboxyl terminus are essential for the specific degradation of the enzyme at mitosis. Mol. Cell Biol. 11, 2538-2546
10. Chabes, A. L., Pfleger, C. M., Kirschner, M. W., and Thelander, L. (2003) Mouse ribonucleotide reductase R2 protein: A new target for anaphasepromoting complex-Cdh1-mediated proteolysis. Proc. Natl. Acad. Sci. U.S.A. 100, 3925-3929
11. Ke, P. Y., and Chang, Z. F. (2004) Mitotic degradation of human thymidine kinase 1 is dependent on the anaphase-promoting complex/cyclosome-CDH1-mediated pathway. Mol. Cell Biol. 24, 514-526
12. Hofer, A., Crona, M., Logan, D. T., and Sjöberg, B. M. (2012) DNA building blocks: Keeping control of manufacture. Crit. Rev. Biochem. Mol. Biol. 47, 50-63
13. Håkansson, P., Hofer, A., and Thelander, L. (2006) Regulation of mammalian ribonucleotide reduction and dNTP pools after DNA damage and in resting cells. J. Biol. Chem. 281, 7834-7841
14. 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
15. Tanaka, H., Arakawa, H., Yamaguchi, T., Shiraishi, K., Fukuda, S., Matsui, K., Takei, Y., and Nakamura, Y. (2000) A ribonucleotide reductase gene involved in a p53-dependent cell-cycle checkpoint for DNA damage. Nature 404, 42-49
16. Pontarin, G., Fijolek, A., Pizzo, P., Ferraro, P., Rampazzo, C., Pozzan, T., Thelander, L., Reichard, P. A., and Bianchi, V. (2008) Ribonucleotide reduction is a cytosolic process in mammalian cells independently of DNA damage. Proc. Natl. Acad. Sci. U.S.A. 105, 17801-17806
17. Pontarin, G., Ferraro, P., Bee, L., Reichard, P., and Bianchi, V. (2012a) Mammalian ribonucleotide reductase subunit p53R2 is required for mitochondrial DNA replication and DNA repair in quiescent cells. Proc. Natl. Acad. Sci. U.S.A. 109, 13302-13307
18. Pontarin, G., Ferraro, P., Reichard, P., and Bianchi, V. (2012) Out of Sphase: Shift of subunits for ribonucleotide reduction. Cell Cycle 11, 4099-4100
19. 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
20. Kimura, T., Takeda, S., Sagiya, Y., Gotoh, M., Nakamura, Y., and Arakawa, H. (2003) Impaired function of p53R2 in Rrm2b-null mice causes severe renal failure through attenuation of dNTP pools. Nat. Genet. 34, 440-445
21. Arnér, E. S., and Eriksson, S. (1995) Mammalian deoxyribonucleoside kinases. Pharmacol. Ther. 67, 155-186
22. 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
23. 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, 337-341
24. Toy, G., Austin, W. R., Liao, H. I., Cheng, D., Singh, A., Campbell, D. O., Ishikawa, T. O., Lehmann, L. W., Satyamurthy, N., Phelps, M. E., Herschman, H. R., Czernin, J., Witte, O. N., and Radu, C. G. (2010) Requirement for deoxycytidine kinase in T and B lymphocyte development. Proc. Natl. Acad. Sci. U.S.A. 107, 5551-5556
25. Pronicka, E., Weglewska-Jurkiewicz, A., Taybert, J., Pronicki, M., Szymanska-Debinska, T., Karkucinska-Wieckowska, A., Jakóbkiewicz-Banecka, J., Kowalski, P., Piekutowska-Abramczuk, D., Pajdowska, M., Socha, P., Sykut-Cegielska, J., and Wegrzyn, G. (2011) Post mortem identification of deoxyguanosine kinase (DGUOK) gene mutations combined with impaired glucose homeostasis and iron overload features in four infants with severe progressive liver failure. J. Appl. Genet. 52, 61-66
26. Barbieri, E., Battistelli, M., Casadei, L., Vallorani, L., Piccoli, G., Guescini, M., Gioacchini, A. M., Polidori, E., Zeppa, S., Ceccaroli, P., Stocchi, L., Stocchi, V., and Falcieri, E. (2011) Morphofunctional and Biochemical Approaches for Studying Mitochondrial Changes during Myoblasts Differentiation. J. Aging Res. 2011, 845379
27. Kislinger, T., Gramolini, A. O., Pan, Y., Rahman, K., MacLennan, D. H., and Emili, A. (2005) Proteome dynamics during C2C12 myoblast differentiation. Mol. Cell Proteomics 4, 887-901
28. Remels, A. H., Langen, R. C., Schrauwen, P., Schaart, G., Schols, A. M., and Gosker, H. R. (2010) Regulation of mitochondrial biogenesis during myogenesis. Mol. Cell Endocrinol. 315, 113-120
29. Tannu, N. S., Rao, V. K., Chaudhary, R. M., Giorgianni, F., Saeed, A. E., Gao, Y., and Raghow, R. (2004) Comparative proteomes of the proliferating C2C12 myoblasts and fully differentiated myotubes reveal the complexity of the skeletal muscle differentiation program. Mol. Cell Proteomics 3, 1065-1082
30. Akman, H. O., Dorado, B., López, L. C., García-Cazorla, A., Vilà, M. R., Tanabe, L. M., Dauer, W. T., Bonilla, E., Tanji, K., and Hirano, M. (2008) Thymidine kinase 2 (H126N) knockin mice show the essential role of balanced deoxynucleotide pools for mitochondrial DNA maintenance. Hum. Mol. Genet. 17, 2433-2440
31. Saada, A. (2004) Deoxyribonucleotides and disorders of mitochondrial DNA integrity. DNA Cell Biol. 23, 797-806
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. Stern-Straeter, J., Bonaterra, G. A., Hörmann, K., Kinscherf, R., and Goessler, U. R. (2009) Identification of valid reference genes during the differentiation of human myoblasts. BMC Mol. Biol. 10, 66
34. Pfaffl, M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45
35. Sharan, R., Maron-Katz, A., and Shamir, R. (2003) CLICK and EXPANDER: A system for clustering and visualizing gene expression data. Bioinformatics 19, 1787-1799
36. Saeed, A. I., Bhagabati, N. K., Braisted, J. C., Liang, W., Sharov, V., Howe, E. A., Li, J., Thiagarajan, M., White, J. A., and Quackenbush, J. (2006) TM4 microarray software suite. Methods Enzymol. 411, 134-193
37. Andreu, A. L., Martinez, R., Marti, R., and García-Arumí, E. (2009) Quan-tification of mitochondrial DNA copy number: Pre-analytical factors. Mitochondrion 9, 242-246
38. 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
39. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
40. Frangini, M., Rampazzo, C., Franzolin, E., Lara, M. C., Vilà, M. R., Martí, R., and Bianchi, V. (2009) Unchanged thymidine triphosphate pools and thymidine metabolism in two lines of thymidine kinase 2-mutated fibroblasts. FEBS J. 276, 1104-1113
41. Leanza, L., Ferraro, P., Reichard, P., and Bianchi, V. (2008) Metabolic interrelations within guanine deoxynucleotide pools for mitochondrial and nuclear DNA maintenance. J. Biol. Chem. 283, 16437-16445
42. Rylova, S. N., Mirzaee, S., Albertioni, F., and Eriksson, S. (2007) Expression of deoxynucleoside kinases and 5'-nucleotidases in mouse tissues: Implications for mitochondrial toxicity. Biochem. Pharmacol. 74, 169-175
43. Ferraro, P., Pontarin, G., Crocco, L., Fabris, S., Reichard, P., and Bianchi, V. (2005) Mitochondrial deoxynucleotide pools in quiescent fibroblasts: A possible model for mitochondrial neurogastrointestinal encephalomyopathy (MNGIE). J. Biol. Chem. 280, 24472-24480
44. Bianchi, V., and Fortunati, E. (1990) Cellular effects of an anionic surfactant detected in V79 fibroblasts by different cytotoxicity tests. Toxicol. In. Vitro. 4, 9-16
45. Sherman, P. A., and Fyfe, J. A. (1989) Enzymatic assay for deoxyribonucleoside triphosphates using synthetic oligonucleotides as template primers. Anal. Biochem. 180, 222-226
46. Ferraro, P., Franzolin, E., Pontarin, G., Reichard, P., and Bianchi, V. (2010) Quantitation of cellular deoxynucleoside triphosphates. Nucleic Acids Res. 38, e85
47. Engström, Y., and Rozell, B. (1988) Immunocytochemical evidence for the cytoplasmic localization and differential expression during the cell cycle of the M1 and M2 subunits of mammalian ribonucleotide reductase. EMBO J. 7, 1615-1620
48. Pitceathly, R. D., Fassone, E., Taanman, J. W., Sadowski, M., Fratter, C., Mudanohwo, E. E., Woodward, C. E., Sweeney, M. G., Holton, J. L., Hanna, M. G., and Rahman, S. (2011) Kearns-Sayre syndrome caused by defective R1/p53R2 assembly. J. Med. Genet. 48, 610-617
49. Wang, L., Hellman, U., and Eriksson, S. (1996) Cloning and expression of human mitochondrial deoxyguanosine kinase cDNA. FEBS Lett. 390, 39-43
50. Munch-Petersen, B., Cloos, L., Tyrsted, G., and Eriksson, S. (1991) Diverging substrate specificity of pure human thymidine kinases 1 and 2 against antiviral dideoxynucleosides. J. Biol. Chem. 266, 9032-9038
51. Pontarin, G., Ferraro, P., Rampazzo, C., Kollberg, G., Holme, E., Reichard, P., and Bianchi, V. (2011) Deoxyribonucleotide metabolism in cycling and resting human fibroblasts with a missense mutation in p53R2, a subunit of ribonucleotide reductase. J. Biol. Chem. 286, 11132-11140
52. Bianchi, V., Pontis, E., and Reichard, P. (1987) Regulation of pyrimidine deoxyribonucleotide metabolism by substrate cycles indCMPdeaminasedeficient V79 hamster cells. Mol. Cell Biol. 7, 4218-4224
53. Saada, A., Shaag, A., and Elpeleg, O. (2003) mtDNA depletion myopathy: Elucidation of the tissue specificity in the mitochondrial thymidine kinase (TK2) deficiency. Mol. Genet. Metab. 79, 1-5
54. Dorado, B., Area, E., Akman, H. O., and Hirano, M. (2011) Onset and organ specificity of Tk2 deficiency depends on Tk1 down-regulation and transcriptional compensation. Hum. Mol. Genet. 20, 155-164
55. 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
56. Hirano, M., Lagier-Tourenne, C., Valentino, M. L., Martí, R., and Nishigaki, Y. (2005) Thymidine phosphorylase mutations cause instability of mitochondrial DNA. Gene. 354, 152-156
57. Traut, T. W. (1994) Physiological concentrations of purines and pyrimidines. Mol. Cell Biochem. 140, 1-22
58. Goldstone, D. C., Ennis-Adeniran, V., Hedden, J. J., Groom, H. C., Rice, G. I., Christodoulou, E., Walker, P. A., Kelly, G., Haire, L. F., Yap, M. W., de Carvalho, L. P., Stoye, J. P., Crow, Y. J., Taylor, I. A., and Webb, M. (2011) HIV-1 restriction factor SAMHD1 is a deoxynucleoside triphosphate triphosphohydrolase. Nature 480, 379-382