Deoxynucleoside stress exacerbates the phenotype of a mouse model of mitochondrial neurogastrointestinal encephalopathy

Brain

Volumn 137, Issue 5, 2014, Pages 1337-1349

  Garcia Diaz, Beatriz ^a   Garone, Caterina ^a,b   Barca, Emanuele ^a   Mojahed, Hamed ^a   Gutierrez, Purification ^a   Pizzorno, Giuseppe ^c   Tanji, Kurenai ^a   Arias Mendoza, Fernando ^a   Quinzii, Caterina M ^a   Hirano, Michio ^a  

^a Department of Medicine   (United States)

^b Universities of Bologna and Turin   (Italy)

^c DESERT RESEARCH INSTITUTE   (United States)

Author keywords

animal model; deoxynucleotide; deoxyuridine; mitochondrial DNA; MNGIE; thymidine

Indexed keywords

DEOXYRIBONUCLEOSIDE TRIPHOSPHATE; DEOXYURIDINE; MITOCHONDRIAL DNA; PYRIMIDINE NUCLEOSIDE; THYMIDINE; THYMIDINE PHOSPHORYLASE; URIDINE PHOSPHORYLASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; FEMALE; KNOCKOUT MOUSE; LEUKOENCEPHALOPATHY; MITOCHONDRIAL DNA DEPLETION; MNGIE SYNDROME; MOUSE; MUSCLE STRENGTH; MUTANT; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; RESPIRATORY CHAIN; SMALL INTESTINE; STRESS; WHITE MATTER;

ANIMAL MODEL; DEOXYNUCLEOTIDE; DEOXYURIDINE; MITOCHONDRIAL DNA; MNGIE; THYMIDINE;

AGE FACTORS; ANIMALS; BODY WEIGHT; BRAIN; DEOXYRIBONUCLEOSIDES; DISEASE MODELS, ANIMAL; INTESTINAL PSEUDO-OBSTRUCTION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIAL DISEASES; MITOCHONDRIAL ENCEPHALOMYOPATHIES; MOTOR ACTIVITY; MUSCLE STRENGTH; MUSCLE, SKELETAL; PSYCHOMOTOR DISORDERS; SUCCINATE DEHYDROGENASE; THYMIDINE; THYMIDINE PHOSPHORYLASE; URIDINE PHOSPHORYLASE;

EID: 84899819342     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awu068     Document Type: Article

References (46)

1. Blazquez A, Martin MA, Lara MC, Marti R, Campos Y, Cabello A, et al. Increased muscle nucleoside levels associated with a novel frameshift mutation in the thymidine phosphorylase gene in a Spanish patient with MNGIE. Neuromuscul Disord 2005; 15: 775-8.
2. Bourdon A, Minai L, Serre V, Jais JP, Sarzi E, Aubert S, et al. Mutation of RRM2B, encoding p53-controlled ribonucleotide reductase (p53R2), causes severe mitochondrial DNA depletion. Nat Genet 2007; 39: 776-80.
3. De Vocht C, Ranquin A, Willaert R, Van Ginderachter JA, Vanhaecke T, Rogiers V, et al. Assessment of stability, toxicity and immunogenicity of new polymeric nanoreactors for use in enzyme replacement therapy of MNGIE. J Control Release 2009; 137: 246-54.
4. Desgranges C, Razaka G, Rabaud M, Bricaud H. Catabolism of thymidine in human blood platelets: purification and properties of thymidine phosphorylase. Biochim Biophys Acta 1981; 654: 211-8.
5. DiMauro S, Serveidei S, Zeviani M, DiRocco M, DeVivo DC, DiDonato S, et al. Cytochrome c oxidase deficiency in Leigh syndrome. Ann Neurol 1987; 22: 498-506.
6. Eimon PM, Chung SS, Lee CM, Weindruch R, Aiken JM. Age-associated mitochondrial DNA deletions in mouse skeletal muscle: comparison of different regions of the mitochondrial genome. Dev Genet 1996; 18: 107-13.
7. Ferraro P, Franzolin E, Pontarin G, Reichard P, Bianchi V. Quantitation of cellular deoxynucleoside triphosphates. Nucleic Acids Res 2010; 38: e85.
8. Ferraro P, Pontarin G, Crocco L, Fabris S, Reichard P, Bianchi V. Mitochondrial deoxynucleotide pools in quiescent fibroblasts: a possible model for mitochondrial neurogastrointestinal encephalomyopathy (MNGIE). J Biol Chem 2005; 280: 24472-80.
9. Garone C, Tadesse S, Hirano M. Clinical and genetic spectrum of mitochondrial neurogastrointestinal encephalomyopathy. Brain 2011; 134: 3326-32.
10. Giordano C, Sebastiani M, De Giorgio R, Travaglini C, Tancredi A, Valentino ML, et al. Gastrointestinal dysmotility in mitochondrial neurogastrointestinal encephalomyopathy is caused by mitochondrial DNA depletion. Am J Pathol 2008; 173: 1120-8.
11. Gonzalez-Vioque E, Torres-Torronteras J, Andreu AL, Marti R. Limited dCTP availability accounts for mitochondrial DNA depletion in mitochondrial neurogastrointestinal encephalomyopathy (MNGIE). PLoS Genet 2011; 7: e1002035.
12. Halter J, Schupbach WM, Casali C, Elhasid R, Fay K, Hammans S, et al. Allogeneic hematopoietic SCT as treatment option for patients with mitochondrial neurogastrointestinal encephalomyopathy (MNGIE): a consensus conference proposal for a standardized approach. Bone Marrow Transplant 2011; 46: 330-7.
13. Hirano M, Marti R, Casali C, Tadesse S, Uldrick T, Fine B, et al. Allogeneic stem cell transplantation corrects biochemical derangements in MNGIE. Neurology 2006; 67: 1458-60.
14. Hirano M, Martí R, Vilà MR, Nishigaki Y. MtDNA maintenance and stability genes: MNGIE and mtDNA depletion syndromes. In: Köhler C, Bauer MF, editors. Mitochondrial function and biogenetics. Berlin: Springer-Verlag; 2004. p. 177-200.
15. Hirano M, Silvestri G, Blake DM, Lombes A, Minetti C, Bonilla E, et al. Mitochondrial neurogastrointestinal encephalomyopathy (MNGIE): clinical, biochemical, and genetic features of an autosomal recessive mitochondrial disorder. Neurology 1994; 44: 721-7.
16. Johansson M. Identification of a novel human uridine phosphorylase. Biochem Biophys Res Commun 2003; 307: 41-6.
17. Koczor CA, Torres RA, Lewis W. The role of transporters in the toxicity of nucleoside and nucleotide analogs. Expert Opin Drug Metab Toxicol 2012; 8: 665-76.
18. la Marca G, Malvagia S, Casetta B, Pasquini E, Pela I, Hirano M, et al. Pre- and post-dialysis quantitative dosage of thymidine in urine and plasma of a MNGIE patient by using HPLC-ESI-MS/MS. J Mass Spectrom 2006; 41: 586-92.
19. Lara MC, Valentino ML, Torres-Torronteras J, Hirano M, Marti R. Mitochondrial neurogastrointestinal encephalomyopathy (MNGIE): biochemical features and therapeutic approaches. Biosci Rep 2007; 27: 151-63.
20. Levene M, Coleman DG, Kilpatrick HC, Fairbanks LD, Gangadharan B, Gasson C, et al. Preclinical toxicity evaluation of erythrocyteencapsulated thymidine phosphorylase in BALB/c mice and beagle dogs: an enzyme-replacement therapy for mitochondrial neurogastrointestinal encephalomyopathy. Toxicol Sci 2013; 131: 311-24.
21. Lopez LC, Akman HO, Garcia-Cazorla A, Dorado B, Marti R, Nishino I, et al. Unbalanced deoxynucleotide pools cause mitochondrial DNA instability in thymidine phosphorylase deficient mice. Hum Mol Genet 2009; 18: 714-22.
22. Mandel H, Szargel R, Labay V, Elpeleg O, Saada A, Shalata A, et al. The deoxyguanosine kinase gene is mutated in individuals with depleted hepatocerebral mitochondrial DNA. Nat Genet 2001; 29: 337-41.
23. Marti R, Dorado B, Hirano M. Measurement of mitochondrial dNTP pools. Methods Mol Biol 2012; 837: 135-48.
24. Marti R, Nishigaki Y, Vilà MR, Hirano M. Alterations of nucleotide metabolism: a new mechanism for mitochondrial disorders. Clin Chem Lab Med 2003; 41: 845-51.
25. Marti R, Spinazzola A, Tadesse S, Nishino I, Nishigaki Y, Hirano M. Definitive diagnosis of mitochondrial neurogastrointestinal encephalomyopathy by biochemical assays. Clin Chem 2004; 50: 120-4.
26. Massaquoi SG, Hallett M. Ataxia and other cerebellar syndromes. In: Jankovic J, Tolosa E, editors. Parkinsons disease and movement disorders. Baltimore: Williams & Wilkins; 1998. p. 623-86.
27. Minuesa G, Volk C, Molina-Arcas M, Gorboulev V, Erkizia I, Arndt P, et al. Transport of lamivudine [(-)-beta-L-2,3-dideoxy-3-thiacytidine] and high-affinity interaction of nucleoside reverse transcriptase inhibitors with human organic cation transporters 1, 2, and 3. J Pharmacol Exp Ther 2009; 329: 252-61.
28. Nishigaki Y, Marti R, Copeland WC, Hirano M. Site-specific somatic mitochondrial DNA point mutations in patients with thymidine phosphorylase deficiency. J Clin Invest 2003; 111: 1913-21.
29. Nishigaki Y, Martí R, Hirano M. ND5 is a hot-spot for multiple atypical mitochondrial DNA deletions in mitochondrial neurogastrointestinal encephalomyopathy. Hum Mol Genet 2004; 13: 91-101.
30. Nishino I, Spinazzola A, Hirano M. Thymidine phosphorylase gene mutations in MNGIE, a human mitochondrial disorder. Science 1999; 283: 689-92.
31. Nishino I, Spinazzola A, Papadimitriou A, Hammans S, Steiner I, Hahn CD, et al. MNGIE: an autosomal recessive disorder due to thymidine phosphorylase mutations. Ann Neurol 2000; 47: 792-800.
32. Papadimitriou A, Comi GP, Hadjigeorgiou GM, Bordoni A, Sciacco M, Napoli L, et al. Partial depletion and multiple deletions of muscle mtDNA in familial MNGIE syndrome. Neurology 1998; 51: 1086-92.
33. Parkinson FE, Damaraju VL, Graham K, Yao SY, Baldwin SA, Cass CE, et al. Molecular biology of nucleoside transporters and their distributions and functions in the brain. Curr Top Med Chem 2011; 11: 948-72.
34. Pikó L, Hougham AJ, Bulpitt KJ. Studies of sequence heterogeneity of mitochondrial DNA from rat and mouse tissues: evidence for an increased frequency of deletions/additions with aging. Mech Ageing Dev 1988; 43: 279-93.
35. Pontarin G, Ferraro P, Valentino ML, Hirano M, Reichard P, Bianchi V. Mitochondrial DNA depletion and thymidine phosphate pool dynamics in a cellular model of mitochondrial neurogastrointestinal encephalomyopathy. J Biol Chem 2006; 281: 22720-8.
36. Quinzii CM, Garone C, Emmanuele V, Tadesse S, Krishna S, Dorado B, et al. Tissue-specific oxidative stress and loss of mitochondria in CoQdeficient Pdss2 mutant mice. FASEB J 2013; 27: 612-21.
37. Saada A, Shaag A, Mandel H, Nevo Y, Eriksson S, Elpeleg O. Mutant mitochondrial thymidine kinase in mitochondrial DNA depletion myopathy. Nat Genet 2001; 29: 342-4.
38. Schüpbach WM, Benoist J-F, Casali C, Elhasid R, Fay K, Hahn D, et al Allogeneic hematopoetic stem cell transplantation (HSCT) for mitochondrial neurogastrointestinal encephalomyopathy (MNGIE). Neurology 2009 73 332.
39. Song S, Wheeler LJ, Mathews CK. Deoxyribonucleotide pool imbalance stimulates deletions in HeLa cell mitochondrial DNA. J Biol Chem 2003; 278: 43893-6.
40. Spinazzola A, Marti R, Nishino I, Andreu A, Naini A, Tadesse S, et al. Altered thymidine metabolism due to defects of thymidine phosphorylase. J Biol Chem 2002; 277: 4128-33.
41. Spinazzola A, Viscomi C, Fernandez-Vizarra E, Carrara F, DAdamo P, Calvo S, et al. MPV17 encodes an inner mitochondrial membrane protein and is mutated in infantile hepatic mitochondrial DNA depletion. Nat Genet 2006; 38: 570-5.
42. Tanhauser SM, Laipis PJ. Multiple deletions are detectable in mitochondrial DNA of aging mice. J Biol Chem 1995; 270: 24769-75.
43. Tyynismaa H, Sembongi H, Bokori-Brown M, Granycome C, Ashley N, Poulton J, et al. Twinkle helicase is essential for mtDNA maintenance and regulates mtDNA copy number. Hum Mol Genet 2004; 13: 3219-27.
44. Valentino ML, Marti R, Tadesse S, Lopez LC, Manes JL, Lyzak J, et al. Thymidine and deoxyuridine accumulate in tissues of patients with mitochondrial neurogastrointestinal encephalomyopathy (MNGIE). FEBS Lett 2007; 581: 3410-4.
45. Yavuz H, Ozel A, Christensen M, Christensen E, Schwartz M, Elmaci M, et al. Treatment of mitochondrial neurogastrointestinal encephalomyopathy with dialysis. Arch Neurol 2007; 64: 435-8.
46. Young JD, Yao SY, Baldwin JM, Cass CE, Baldwin SA. The human concentrative and equilibrative nucleoside transporter families, SLC28 and SLC29. Mol Aspects Med 2013; 34: 529-47.