Liver mtDNA content increases during development: A comparison of methods and the importance of age- and tissue-specific controls for the diagnosis of mtDNA depletion

Mitochondrion

Volumn 7, Issue 6, 2007, Pages 386-395

  Morten, Karl J ^a   Ashley, Neil ^a   Wijburg, Frits ^c   Hadzic, Nedim ^d   Parr, Jeremy ^b   Jayawant, Sandeep ^b   Adams, Susan ^a   Bindoff, Laurence ^e   Bakker, Henk D ^c   Mieli Vergani, Giorgina ^d   Zeviani, Massimo ^f   Poulton, Joanna ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^f DEPARTMENT OF NEUROSURGERY   (Italy)

Author keywords

Hepatocerebral syndrome; Mitochondrial DNA; Movement disorder; mtDNA depletion syndrome; PicoGreen

Indexed keywords

MITOCHONDRIAL DNA; TRANSFER RNA;

AGE DISTRIBUTION; ARTICLE; CASE REPORT; CELL NUCLEUS; CHILD; CHOREOATHETOSIS; CONTROLLED STUDY; CORPUS CALLOSUM AGENESIS; DEVELOPMENTAL DISORDER; DIAGNOSTIC VALUE; DIARRHEA; DNA CONTENT; DNA DETERMINATION; DNA ISOLATION; ENZYME DEFICIENCY; FAILURE TO THRIVE; FEEDING DISORDER; FIBROBLAST; FLUORESCENCE MICROSCOPY; GENE MUTATION; HEPATOMEGALY; HUMAN; HUMAN CELL; HUMAN TISSUE; INFANT; INTERMETHOD COMPARISON; LABORATORY TEST; LACTIC ACIDOSIS; LIVER BIOPSY; LIVER FAILURE; LIVER PARENCHYMA; MALE; MENTAL DEFICIENCY; MITOCHONDRIAL DNA DEPLETION; MITOCHONDRIAL DNA DEPLETION SYNDROME; MOTOR DYSFUNCTION; MUSCLE BIOPSY; MUSCLE HYPOTONIA; MUSCLE STRENGTH; MUTATIONAL ANALYSIS; PERINATAL PERIOD; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REFERENCE VALUE; RESPIRATORY CHAIN; STAINING; TISSUE SPECIFICITY; VOMITING;

AGE FACTORS; CHILD, PRESCHOOL; DNA, MITOCHONDRIAL; FATAL OUTCOME; FIBROBLASTS; HUMANS; IMMUNOBLOTTING; INFANT; LIVER; LIVER DISEASES; MALE; MITOCHONDRIAL DISEASES; ORGANIC CHEMICALS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 36048966317     PISSN: 15677249     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mito.2007.09.001     Document Type: Article

References (45)

1. Anti M., Marra G., Rapaccini G.L., Rumi C., Bussa S., Fadda G., Vecchio F.M., Valenti A., Percesepe A., Pompili M., et al. DNA ploidy pattern in human chronic liver diseases and hepatic nodular lesions. Flow cytometric analysis on echo-guided needle liver biopsy. Cancer 73 (1994) 281-288
2. Antonicka H., Sasarman F., Kennaway N.G., and Shoubridge E.A. The molecular basis for tissue specificity of the oxidative phosphorylation deficiencies in patients with mutations in the mitochondrial translation factor EFG1. Hum. Mol. Genet. 15 (2006) 1835-1846
3. Ashley N., Harris D., and Poulton J. Detection of mitochondrial DNA depletion in living human cells using PicoGreen staining. Experimental Cell Research 303 (2004) 432-446
4. Bai R.K., Perng C.L., Hsu C.H., and Wong L.J. Quantitative PCR analysis of mitochondrial DNA content in patients with mitochondrial disease. Ann. NY Acad. Sci. 1011 (2004) 304-309
5. Barthelemy C., de Baulny H.O., and Lombes A. D-loop mutations in mitochondrial DNA: link with mitochondrial DNA depletion?. Hum. Genet. 110 (2002) 479-487
6. Barthelemy C., Ogier de Baulny H., Diaz J., Cheval M.A., Frachon P., Romero N., Goutieres F., Fardeau M., and Lombes A. Late-onset mitochondrial DNA depletion: DNA copy number, multiple deletions, and compensation. Ann. Neurol. 49 (2001) 607-617
7. Chabi B., Mousson de Camaret B., Duborjal H., Issartel J.P., and Stepien G. Quantification of mitochondrial DNA deletion, depletion, and overreplication: application to diagnosis. Clin. Chem. 49 (2003) 1309-1317
8. Chinnery P.F., and Dimauro S. Mitochondrial hepatopathies. J. Hepatol. 43 (2005) 207-209
9. Chiu R.W., Chan L.Y., Lam N.Y., Tsui N.B., Ng E.K., Rainer T.H., and Lo Y.M. Quantitative analysis of circulating mitochondrial DNA in plasma. Clin. Chem. 49 (2003) 719-726
10. DiMauro S., Nicholson J.F., Hayes A.P., Eastwood A.B., Papadimitriou A., Koenigsberger R., and DeVivo D.C. Benign infantile mitochondrial myopathy due to reversible cytochrome c oxidase deficiency. Ann. Neurol. 14 (1983) 226-234
11. Ducluzeau P.H., Lachaux A., Bouvier R., Duborjal H., Stepien G., Bozon D., and Mousson de Camaret B. Progressive reversion of clinical and molecular phenotype in a child with liver mitochondrial DNA depletion. J. Hepatol. 36 (2002) 698-703
12. Elpeleg O., Miller C., Hershkovitz E., Bitner-Glindzicz M., Bondi-Rubinstein G., Rahman S., Pagnamenta A., Eshhar S., and Saada A. Deficiency of the ADP-forming succinyl-CoA synthase activity is associated with encephalomyopathy and mitochondrial DNA depletion. Am. J. Hum. Genet. 76 (2005) 1081-1086
13. Epstein C.J., and Gatens E.A. Nuclear ploidy in mammalian parenchymal liver cells. Nature 214 (1967) 1050-1051
14. Ferrari G., Lamantea E., Donati A., Filosto M., Briem E., Carrara F., Parini R., Simonati A., Santer R., and Zeviani M. Infantile hepatocerebral syndromes associated with mutations in the mitochondrial DNA polymerase-gammaA. Brain 128 (2005) 723-731
15. Guidotti J.E., Bregerie O., Robert A., Debey P., Brechot C., and Desdouets C. Liver cell polyploidization: a pivotal role for binuclear hepatocytes. J. Biol. Chem. 278 (2003) 19095-19101
16. Hargreaves P., Rahman S., Guthrie P., Taanman J.W., Leonard J.V., Land J.M., and Heales S.J. Diagnostic value of succinate ubiquinone reductase activity in the identification of patients with mitochondrial DNA depletion. J. Inherit. Metab. Dis. 25 (2002) 7-16
17. Horvath R., Hudson G., Ferrari G., Futterer N., Ahola S., Lamantea E., Prokisch H., Lochmuller 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., and Chinnery P.F. Phenotypic spectrum associated with mutations of the mitochondrial polymerase gamma gene. Brain 129 (2006) 1674-1684
18. Iborra F.J., Kimura H., and Cook P.R. The functional organization of mitochondrial genomes in human cells. BMC Biol. 2 (2004) 9
19. Labarthe F., Dobbelaere D., Devisme L., De Muret A., Jardel C., Taanman J.W., Gottrand F., and Lombes A. Clinical, biochemical and morphological features of hepatocerebral syndrome with mitochondrial DNA depletion due to deoxyguanosine kinase deficiency. J. Hepatol. 43 (2005) 333-341
20. Legros F., Malka F., Frachon P., Lombes A., and Rojo M. Organization and dynamics of human mitochondrial DNA. J. Cell Sci. 117 (2004) 2653-2662
21. Macmillan C.J., and Shoubridge E.A. Mitochondrial DNA depletion: prevalence in a pediatric population referred for neurologic evaluation. Pediatr. Neurol. 14 (1996) 203-210
22. MacSween R., Burt A., Portmann B., Ishak K., Scheur P., and Anthony P. Pathology of the Liver (2002), Churchill Livingstone, London pp. 26ff
23. Magnusson J., Orth M., Lestienne P., and Taanman J.W. Replication of mitochondrial DNA occurs throughout the mitochondria of cultured human cells. Exp. Cell Res. 289 (2003) 133-142
24. 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. The deoxyguanosine kinase gene is mutated in individuals with depleted hepatocerebral mitochondrial DNA. Nat. Genet. 29 (2001) 337-341
25. Moraes C.T., Shanske S., Tritschler H.J., Aprille J.R., Andreetta F., Bonilla E., Schon E.A., and DiMauro S. mtDNA depletion with variable tissue expression: a novel genetic abnormality in mitochondrial diseases. Am. J. Hum. Genet. 48 (1991) 492-501
26. Moritz C., and Brown W.M. Tandem duplications in animal mitochondrial DNAs: variation in incidence and gene content among lizards. Proc. Natl. Acad. Sci. USA 84 (1987) 7183-7187
27. Morris A.A., Taanman J.W., Blake J., Cooper J.M., Lake B.D., Malone M., Love S., Clayton P.T., Leonard J.V., and Schapira A.H. Liver failure associated with mitochondrial DNA depletion. J. Hepatol. 28 (1998) 556-563
28. Naviaux R., Nyhan W., Barshop B., Poulton J., Markusic D., Karpinski N., and Haas R. Mitochondrial DNA polymerase gamma deficiency and mtDNA depletion in a child with Alpers' syndrome. Ann. Neurol. 45 (1999) 54-58
29. Naviaux R.K., and Nguyen K.V. POLG mutations associated with Alpers' syndrome and mitochondrial DNA depletion. Ann. Neurol. 55 (2004) 706-712
30. Nguyen K.V., Sharief F.S., Chan S.S., Copeland W.C., and Naviaux R.K. Molecular diagnosis of Alpers syndrome. J. Hepatol. 45 (2006) 108-116
31. Nishino I., Spinazzola A., and Hirano M. Thymidine phosphorylase gene mutations in MNGIE, a human mitochondrial disorder. Science 283 (1999) 689-692
32. Poulton J., Jayawant S., O'Rourke A., Morten K., Ashley N., Narasimhan M., and Fratter C. Mutations in the mitochondrial DNA gamma polymerase (POLG) may cause Alpers syndrome, mitochondrial DNA depletion and non-syndromic status epilepticus: implications for valproate therapy. Dev. Med. Child Neurol. (2007)
33. Poulton J., Sewry C., Potter C., Bourgeron T., Chretien D., Wijburg F., Morten K., and Brown G. Variation in mitochondrial DNA levels in muscle from normal controls. Is depletion of mitochondrial DNA in patients with mitochondrial myopathy a distinct clinical syndrome?. J. Inherit. Metab. Dis. 18 (1995) 4-20
34. Ricci E., Moraes C.T., Servidei S., Tonali P., Bonilla E., and Di Mauro S. Disorders associated with depletion of mitochondrial DNA. Brain Pathol. 2 (1992) 141-147
35. Roubertoux P.L., Sluyter F., Carlier M., Marcet B., Maarouf-Veray F., Cherif C., Marican C., Arrechi P., Godin F., Jamon M., Verrier B., and Cohen-Salmon C. Mitochondrial DNA modifies cognition in interaction with the nuclear genome and age in mice. Nat. Genet. 35 (2003) 65-69
36. Salviati L., Sacconi S., Mancuso M., Otaegui D., Camano P., Marina A., Rabinowitz S., Shiffman R., Thompson K., Wilson C.M., Feigenbaum A., Naini A.B., Hirano M., Bonilla E., DiMauro S., and Vu T.H. Mitochondrial DNA depletion and dGK gene mutations. Ann. Neurol. 52 (2002) 311-317
37. Sperl W., Sengers R.C., Trijbels J.M., Ruitenbeek W., Doesburg W.H., Smeitink J.A., Kollee L.A., and Boon J.M. Enzyme activities of the mitochondrial energy generating system in skeletal muscle tissue of preterm and fullterm neonates. Ann. Clin. Biochem. 29 (1992) 638-645
38. 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., Rotig A., Gasparini P., Ferrero I., Mootha V.K., Tiranti V., and Zeviani M. MPV17 encodes an inner mitochondrial membrane protein and is mutated in infantile hepatic mitochondrial DNA depletion. Nat. Genet. 38 (2006) 570-575
39. Spinazzola A., and Zeviani M. Disorders of nuclear-mitochondrial intergenomic signaling. Gene 354 (2005) 162-168
40. Taanman J.W., Bodnar A.G., Cooper J.M., Morris A.A., Clayton P.T., Leonard J.V., and Schapira A.H. Molecular mechanisms in mitochondrial DNA depletion syndrome. Hum. Mol. Genet. 6 (1997) 935-942
41. Vila M.R., Segovia-Silvestre T., Gamez J., Marina A., Naini A.B., Meseguer A., Lombes A., Bonilla E., DiMauro S., Hirano M., and Andreu A.L. Reversion of mtDNA depletion in a patient with TK2 deficiency. Neurology 60 (2003) 1203-1205
42. Vilarinho L., Chorao R., Cardoso M.L., Rocha H., Nogueira C., and Santorelli F.M. The ND1 T3308C mutation may be a mtDNA polymorphism. Report of two Portuguese patients. J. Inherit. Metab. Dis. 22 (1999) 90-91
43. Vu T.H., Sciacco M., Tanji K., Nichter C., Bonilla E., Chatkupt S., Maertens P., Shanske S., Mendell J., Koenigsberger M.R., Sharer L., Schon E.A., DiMauro S., and DeVivo D.C. Clinical manifestations of mitochondrial DNA depletion. Neurology 50 (1998) 1783-1790
44. Wang L., Limongelli A., Vila M.R., Carrara F., Zeviani M., and Eriksson S. Molecular insight into mitochondrial DNA depletion syndrome in two patients with novel mutations in the deoxyguanosine kinase and thymidine kinase 2 genes. Mol. Genet. Metab. 84 (2005) 75-82
45. Watmough N.J., Birch-Machin M.A., Bindoff L.A., Aynsley-Green A., Simpson K., Ragan C.I., Sherratt H.S., and Turnbull D.M. Tissue specific defect of complex I of the mitochondrial respiratory chain. Biochem. Biophys. Res. Commun. 160 (1989) 623-627