In vitro supplementation with deoxynucleoside monophosphates rescues mitochondrial DNA depletion

Molecular Genetics and Metabolism

Volumn 107, Issue 1-2, 2012, Pages 95-103

  Bulst, Stefanie ^a,b   Holinski Feder, Elke ^a   Payne, Brendan ^c   Abicht, Angela ^a,b   Krause, Sabine ^b   Lochmüller, Hanns ^c   Chinnery, Patrick F ^c   Walter, Maggie C ^b   Horvath, Rita ^a,c  

^a Medical Genetic Center   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

In vitro supplementation; Mitochondrial disease; Mitochondrial DNA depletion

Indexed keywords

ABACAVIR; CYTOCHROME C OXIDASE; DEOXYNUCLEOSIDE PHOSPHATE; DIDANOSINE; MITOCHONDRIAL DNA; MYOD PROTEIN; NUCLEOSIDE; STAVUDINE; UNCLASSIFIED DRUG;

ARTICLE; CELL TRANSDIFFERENTIATION; CONTROLLED STUDY; DNA CONTENT; FIBROBLAST; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; MITOCHONDRIAL DNA DEPLETION SYNDROME; MYOTUBE; PHENOTYPE; PRIORITY JOURNAL; SUPPLEMENTATION;

CELL LINE; CELL TRANSDIFFERENTIATION; DEOXYRIBONUCLEOTIDES; DNA, MITOCHONDRIAL; GENE DOSAGE; HUMANS; MITOCHONDRIA; MUSCLE FIBERS, SKELETAL; MUTATION; MYOBLASTS; REVERSE TRANSCRIPTASE INHIBITORS;

EID: 84866180900     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2012.04.022     Document Type: Article

References (50)

1. Moraes C.T., Shanske S., Tritschler H.-J., Aprille J.R., Andreetta F., Bonilla E., Schon E.A., DiMauro S. MtDNA depletion with variable tissue expression: a novel genetic abnormality in mitochondrial diseases. Am. J. Hum. Genet. 1991, 48:492-501.
2. Hirano M., Vu T.H. Defects of intergenomic communication: where do we stand?. Brain Pathol. 2000, 10:451-461.
3. Spinazzola A., Zeviani M. Disorders of nuclear-mitochondrial intergenomic signalling. Gene 2005, 354:162-168.
4. Sarzi E., Bourdon A., Chrétien D., Zarhrate M., Corcos J., Slama A., Cormier-Daire V., de Lonlay P., Munnich A., Rötig A. Mitochondrial DNA depletion is a prevalent cause of multiple respiratory chain deficiency in childhood. J. Pediatr. 2007, 150:531-534. (534.e1-6).
5. Rötig A., Poulton J. Genetic causes of mitochondrial DNA depletion in humans. Biochim. Biophys. Acta 2007, 12:1103-1108.
6. Spinazzola A., Invernizzi F., Carrara F., Lamantea E., Donati A., DiRocco M., Giordano I., Meznaric-Petrusa M., Baruffini E., Ferrero I., Zeviani M. Clinical and molecular features of mitochondrial DNA depletion syndrome. J. Inherit. Metab. Dis. 2009, 32:143-158.
7. Suomalainen A., Isohanni P. Mitochondrial DNA depletion syndromes - many genes, common mechanisms. Neuromuscul. Disord. 2010, 7:429-437.
8. Alberio S., Mineri R., Tiranti V., Zeviani M. Depletion of mtDNA: syndromes and genes. Mitochondrion 2007, 7:6-12.
9. Mandel H., Szargel R., Labay V., Elpeleg O., Saada A., Shalata A., Anbinder Y., Berkowitz D., Hartman C., Barak M., Eriksson S., Cohen N. The deoxyguanosine kinase gene is mutated in individuals with depleted hepatocerebral mitochondrial DNA. Nat. Genet. 2001, 29:337-341.
10. Naviaux R.K., Nguyen K.V. POLG mutations associated with Alpers' syndrome and mtDNA depletion. Ann. Neurol. 2004, 55:706-712.
11. Spinazzola A., Viscomi C., Fernandez-Vizarra E., Carrara F., D'Adamo P., Calvo S., Marsano R.M., Donnini C., Weiher H., Strisciuglio P., Parini R., Sarzi E., Chan A., DiMauro S., Rötig A., Gasparini P., Ferrero I., Mootha V.K., Tiranti V., Zeviani M. MPV17 encodes an inner mitochondrial membrane protein and is mutated in infantile hepatic mitochondrial DNA depletion. Nat. Genet. 2006, 38:570-575.
12. Hakonen A.H., Goffart S., Marjavaara S., Paetau A., Cooper H., Mattila K., Lampinen M., Sajantila A., Lönnqvist T., Spelbrink J.N., Suomalainen A. Infantile-onset spinocerebellar ataxia and mitochondrial recessive ataxia syndrome are associated with neuronal complex I defect and mtDNA depletion. Hum. Mol. Genet. 2008, 17:3822-3835.
13. Kaguni L.S. DNA polymerase gamma, the mitochondrial replicase. Annu. Rev. Biochem. 2004, 73:293-320.
14. Copeland W.C., Longley M.J. DNA polymerase gamma in mitochondrial DNA replication and repair. Sci. World J. 2003, 3:34-44.
15. Chinnery P.F., Zeviani M. 155th ENMC workshop: polymerase gamma and disorders of mitochondrial DNA synthesis, 21-23 September 2007, Naarden, The Netherlands. Neuromuscul. Disord. 2008, 18:259-267.
16. Nguyen K.V., Sharief F.S., Chan S.S.L., Copeland W.C., Naviaux R.K. Molecular diagnosis of Alpers syndrome. J. Hepatol. 2006, 45:108-116.
17. Tyynismaa H., Sun R., Ahola-Erkkilä S., Almusa H., Pöyhönen R., Korpela M., Honkaniemi J., Isohanni P., Paetau A., Wang L., Suomalainen A. Thymidine kinase 2 mutations in autosomal recessive progressive ophthalmoplegia with multiple mitochondrial DNA deletions. Hum. Mol. Genet. 2011, 21:66-75.
18. 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., Rahman S. Kearns-Sayre syndrome caused by defective R1/p53R2 assembly. J. Med. Genet. 2011, 48:610-617.
19. Fratter C., Raman P., Alston C.L., Blakely E.L., Craig K., Smith C., Evans J., Seller A., Czermin B., Hanna M.G., Poulton J., Brierley C., Staunton T.G., Turnpenny P.D., Schaefer A.M., Chinnery P.F., Horvath R., Turnbull D.M., Gorman G.S., Taylor R.W. RRM2B mutations are frequent in familial PEO with multiple mtDNA deletions. Neurology 2011, 76:2032-2034.
20. Bourdon A., Minai L., Serre V., Jais J.P., Sarzi E., Aubert S., Chretien D., de Lonlay P., Paquis-Flucklinger V., Arakawa H., Nakamura Y., Munnich A., Rötig A. Mutation of RRM2B, encoding p53-controlled ribonucleotide reductase (p53R2), causes severe mitochondrial DNA depletion. Nat. Genet. 2007, 39:776-780.
21. Bornstein B., Area E., Flanigan K.M., Ganesh J., Jayakar P., Swoboda K.J., Coku J., Naini A., Shanske S., Tanji K., Hirano M., DiMauro S. Mitochondrial DNA depletion syndrome due to mutations in the RRM2B gene. Neuromuscul. Disord. 2008, 18:453-459.
22. Tyynismaa H., Ylikallio E., Patel M., Molnar M.J., Haller R.G., Suomalainen A. A heterozygous truncating mutation in RRM2B causes autosomal-dominant progressive external ophthalmoplegia with multiple mtDNA deletions. Am. J. Hum. Genet. 2009, 85:290-295.
23. Copeland W.C. Inherited mitochondrial diseases of DNA replication. Annu. Rev. Med. 2008, 59:131-146.
24. Bulst S., Abicht A., Holinski-Feder E., Müller-Ziermann S., Koehler U., Thirion C., Walter M.C., Stewart J.D., Chinnery P.F., Lochmüller H., Horvath R. In vitro supplementation with dAMP/dGMP leads to partial restoration of mtDNA levels in mitochondrial depletion syndromes. Hum. Mol. Genet. 2009, 18:1590-1599.
25. Durham S.E., Bonilla E., Samuels D.C., DiMauro S., Chinnery P.F. Mitochondrial DNA copy number threshold in mtDNA depletion myopathy. Neurology 2005, 65:453-455.
26. Walker U.A., Setzer B., Venhoff N. Increased long-term mitochondrial toxicity in combinations of nucleoside analogue reverse-transcriptase inhibitors. AIDS 2002, 16:2165-2173.
27. Birkus G., Hitchcock M.J.M., Cihlar T. Assessment of mitochondrial toxicity in human cells treated with tenofovir: comparison with other nucleoside reverse transcriptase inhibitors. Antimicrob. Agents Chemother. 2002, 46:716-723.
28. Lund K.C., Peterson L.L., Wallace K.B. Absence of a universal mechanism of mitochondrial toxicity by nucleoside analogs. Antimicrob. Agents Chemother. 2007, 51:2531-2539.
29. Havenga M.J.E., Lemckert A.A.C., Ophorst O.J.A.E., van Meijer M., Germeraad W.T.V., Grimbergen J., van den Doel M.A., Vogels R., van Deutekom J., Janson A.A.M., de Bruijn J.D., Uytdehaag F., Quax P.H.A., Logtenberg T., Mehtali M., Bout A. Exploiting the nature diversity in adenovirus tropism for therapy and prevention of disease. J. Virol. 2002, 76:4612-4620.
30. Fischer J.C., Ruitenbeek W., Gabreels F.J., Janssen A.J., Renier W.O., Sengers R.C., Stadhouders A.M., ter Laak H.J., Trijbels J.M., Yeerkamp J.H. A mitochondrial encephalomyopathy: the first case with an established defect at the level of coenzyme. Q. Eur. J. Pediatr. 1986, 144:441-444.
31. Bent A.J., Haddara W., Prevec L., Graham F.L. An efficient and flexible system for construction of adenovirus vectors with insertions or deletions in early regions 1 and 3. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:8802-8806.
32. Robbins P.D., Tahara H., Ghivizzani S.C. Viral vectors for gene therapy. Trends Biotechnol. 1998, 16:35-40.
33. Huang S., Stupack D., Mathias P., Wang Y., Nemerow G. Growth arrest of Epstein-Barr virus immortalized B lymphocytes by adenovirus delivered ribozymes. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:8156-8161.
34. Bergelson J.M., Cunningham J.A., Droguett G., Kurt-Jones E.A., Krithivas A., Hong J.S., Horwitz M.S., Crowell R.L., Finberg R.W. Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science 1997, 275:1320-1323.
35. Marshall C.J., Lloyd A.C., Morris J.D., Paterson H., Price B., Hall A. Signal transduction by p21ras. Int. J. Cancer Suppl. 1998, 4:29-31.
36. Saada A. Fishing in the (deoxyribonucleotide) pool. Biochem. J. 2009, 422:e3-e6.
37. Mathews C.K., Song S. Maintaining precursor pools for mitochondrial DNA replication. FASEB J. 2007, 21:2294-2303.
38. Saada A. Mitochondrial deoxyribonucleotide pools in deoxyguanosine kinase deficiency. Mol. Genet. Metab. 2008, 95:169-173.
39. Eklund H., Uhlin U., Farnegardh M., Logan D.T., Nordlund P. Structure and function of the radical enzyme ribonucleotide reductase. Prog. Biophys. Mol. Biol. 2001, 77:177-268.
40. Tanaka H., Arakawa H., Yamaguchi T., Shiraishi K., Fukuda S., Matsui K., Takei Y., Nakamura Y. A ribonucleotide reductase gene involved in a 53-dependent cell-cycle checkpoint for DNA damage. Nature 2000, 404:42-49.
41. Pontarin G., Ferraro P., Hakansson P., Thelander L., Reichard P., Bianchi V. p53R2-dependent ribonucleotide reduction provides deoxyribonucleotides in quiescent human fibroblasts in the absence of induced DNA damage. J. Biol. Chem. 2007, 282:16820-16828.
42. Leanza L., Ferraro P., Reichard P., Bianchi V. Metabolic interrelations within guanine deoxynucleotide pools for mitochondrial and nuclear DNA maintenance. J. Biol. Chem. 2008, 283:16437-16445.
43. Wang L., Saada A., Eriksson S. Kinetic properties of mutant human thymidine kinase 2 suggest a mechanism for mitochondrial DNA depletion myopathy. J. Biol. Chem. 2003, 278:6963-6968.
44. Rylova S.N., Albertioni F., Flygh G., Eriksson S. Activity profiles of deoxynucleotide kinases and 5'-nucleotidases in cultured adipocytes and myoblastic cells: insights into mitochondrial toxicity of nucleoside analogs. Biochem. Pharmacol. 2005, 69:951-960.
45. Mazzon C., Rampazzo C., Scaini M.C., Gallinaro L., Karlsson A., Meier C., Balzarini J., Reichard P., Bianchi V. Cytosolic and mitochondrial deoxyribonucleotidases: activity with substrate analogs, inhibitors and implications for therapy. Biochem. Pharmacol. 2003, 66:471-479.
46. Ashley N., Adams S., Slama A., Zeviani M., Suomalainen A., Andreu A.L., Naviaux R.K., Poulton J. Defects in maintenance of mitochondrial DNA are associated with intramitochondrial nucleotide imbalances. Hum. Mol. Genet. 2007, 16:1400-1411.
47. Ray A.S., Basavapathruni A., Anderson K.S. Mechanistic studies to understand the progressive development of resistance in human immunodeficiency virus type 1 reverse transcriptase to abacavir. J. Biol. Chem. 2002, 43:40479-40490.
48. Saitoh A., Haas R.H., Naviaux R.K., Salva N.G., Wong J.K., Spector S.A. Impact of nucleoside reverse transcriptase inhibitors on mitochondrial DNA and RNA in human skeletal muscle cells. Antimicrob. Agents Chemother. 2008, 52:2825-2830.
49. Horvath R., Hudson G., Ferrari G., Fütterer N., Ahola S., Lamantea E., Prokisch H., Lochmüller H., McFarland R., Ramesh V., Klopstock T., Freisinger P., Salvi F., Mayr J.A., Santer R., Tesarova M., Zeman J., Udd B., Taylor R.W., Turnbull D., Hanna M., Fialho D., Suomalainen A., Zeviani M., Chinnery P.F. Phenotypic spectrum associated with mutations of the mitochondrial polymerase gamma gene. Brain 2006, 129:1674-1684.
50. Freisinger P., Fütterer N., Lankes E., Gempel K., Berger T.M., Spalinger J., Hoerbe A., Schwantes C., Lindner M., Santer R., Burdelski M., Schaefer H., Setzer B., Walker U.A., Horvath R. Hepatocerebral mitochondrial DNA depletion syndrome caused by deoxyguanosine kinase (DGUOK) mutations. Arch. Neurol. 2006, 63:1129-1134.