Mitochondrial dysfunction in the skeletal muscle of a mouse model of Rett syndrome (RTT): Implications for the disease phenotype

Mitochondrion

Volumn 15, Issue 1, 2014, Pages 10-17

  Gold, W A ^a,b   Williamson, S L ^a   Kaur, S ^a   Hargreaves, I P ^c   Land, J M ^c   Pelka, G J ^d   Tam, P P L ^d,e   Christodoulou, J ^a,b,e  

^a CHILDREN S HOSPITAL AT WESTMEAD   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d CHILDREN'S MEDICAL RESEARCH INSTITUTE   (Australia)

^e UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Mitochondria; Oxidative stress; PGC 1 ; Reactive oxygen species; Respiratory chain; Rett syndrome; Skeletal muscle

Indexed keywords

CYTOCHROME C OXIDASE; CYTOCHROME C OXIDASE 1; FREE RADICAL; GENOMIC DNA; GLUTATHIONE; METHYL CPG BINDING PROTEIN 2; MITOCHONDRIAL DNA; SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DETERIORATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; ENZYME ASSAY; FEMALE; GENE EXPRESSION; HINDLIMB; IMMUNOBLOTTING; MALE; MECP2 GENE; MICROARRAY ANALYSIS; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; RESPIRATORY CHAIN; RETT SYNDROME; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; ANIMAL; DISEASE MODEL; ENZYMOLOGY; HUMAN; METABOLISM; MITOCHONDRION; PATHOPHYSIOLOGY; PHYSIOLOGY; TOXICITY;

ANIMALS; DISEASE MODELS, ANIMAL; ELECTRON TRANSPORT COMPLEX II; ELECTRON TRANSPORT COMPLEX III; ELECTRON TRANSPORT COMPLEX IV; FREE RADICALS; GLUTATHIONE; HUMANS; MICE; MITOCHONDRIA; MUSCLE, SKELETAL; OXIDATIVE STRESS; RETT SYNDROME;

EID: 84897440230     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2014.02.012     Document Type: Article

References (58)

1. Amir R.E., Van den Veyver I.B., et al. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 1999, 23(2):185-188.
2. Belichenko P.V., Wright E.E., et al. Widespread changes in dendritic and axonal morphology in Mecp2-mutant mouse models of Rett syndrome: evidence for disruption of neuronal networks. J. Comp. Neurol. 2009, 514(3):240-258.
3. Bindoff L.A., Birch-Machin M.A., et al. Respiratory chain abnormalities in skeletal muscle from patients with Parkinson's disease. J. Neurol. Sci. 1991, 104(2):203-208.
4. Bindoli A., Rigobello M.P. Principles in redox signaling: from chemistry to functional significance. Antioxid. Redox Signal. 2013, 18(13):1557-1593.
5. Bruno C., Martinuzzi A., et al. A stop-codon mutation in the human mtDNA cytochrome c oxidase I gene disrupts the functional structure of complex IV. Am. J. Hum. Genet. 1999, 65(3):611-620.
6. Ciammola A., Sassone J., et al. Low anaerobic threshold and increased skeletal muscle lactate production in subjects with Huntington's disease. Mov. Disord. 2011, 26(1):130-137.
7. Ciccoli L., De Felice C., et al. Morphological changes and oxidative damage in Rett syndrome erythrocytes. Biochim. Biophys. Acta 2012, 1820(4):511-520.
8. Coker S.B., Melnyk A.R. Rett syndrome and mitochondrial enzyme deficiencies. J. Child Neurol. 1991, 6(2):164-166.
9. Comi G.P., Bordoni A., et al. Cytochrome c oxidase subunit I microdeletion in a patient with motor neuron disease. Ann. Neurol. 1998, 43(1):110-116.
10. Cornford M.E., Philippart M., et al. Neuropathology of Rett syndrome: case report with neuronal and mitochondrial abnormalities in the brain. J. Child Neurol. 1994, 9(4):424-431.
11. De Felice C., Ciccoli L., et al. Systemic oxidative stress in classic Rett syndrome. Free Radic. Biol. Med. 2009, 47(4):440-448.
12. De Felice C., Signorini C., et al. F2-dihomo-isoprostanes as potential early biomarkers of lipid oxidative damage in Rett syndrome. J. Lipid Res. 2011, 52(12):2287-2297.
13. Dotti M.T., Manneschi L., et al. Mitochondrial dysfunction in Rett syndrome. An ultrastructural and biochemical study. Brain Dev. 1993, 15(2):103-106.
14. Duncan A.J., Heales S.J., et al. Determination of coenzyme Q10 status in blood mononuclear cells, skeletal muscle, and plasma by HPLC with di-propoxy-coenzyme Q10 as an internal standard. Clin. Chem. 2005, 51(12):2380-2382.
15. Eeg-Olofsson O., al-Zuhair A.G., Teebi A.S., al-Essa M.M. Abnormal mitochondria in the Rett syndrome. Brain Dev. 1988, 10(4):260-262.
16. Finck B.N., Kelly D.P. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J. Clin. Invest. 2006, 116(3):615-622.
17. Formichi P., Battisti C., et al. Vitamin E serum levels in Rett syndrome. J. Neurol. Sci. 1998, 156(2):227-230.
18. Geng T., Li P., et al. PGC-1alpha plays a functional role in exercise-induced mitochondrial biogenesis and angiogenesis but not fiber-type transformation in mouse skeletal muscle. Am. J. Physiol. Cell Physiol. 2010, 298(3):C572-C579.
19. Gibson J.H., Slobedman B., et al. Downstream targets of methyl CpG binding protein 2 and their abnormal expression in the frontal cortex of the human Rett syndrome brain. BMC Neurosci. 2010, 11:53.
20. Griffith O.W., Mulcahy R.T. The enzymes of glutathione synthesis: gamma-glutamylcysteine synthetase. Adv. Enzymol. Relat. Areas Mol. Biol. 1999, 73:209-267. (xii).
21. Grosser E., Hirt U., et al. Oxidative burden and mitochondrial dysfunction in a mouse model of Rett syndrome. Neurobiol. Dis. 2012, 48(1):102-114.
22. Hagberg B. Rett's syndrome: prevalence and impact on progressive severe mental retardation in girls. Acta Paediatr. Scand. 1985, 74(3):405-408.
23. Hargreaves I.P., Sheena Y., Land J.M., Heales S.J. Glutathione deficiency in patients with mitochondrial disease: implications for pathogenesis and treatment. J. Inherit. Metab. Dis. 2005, 28(1):81-88.
24. Hargreaves I.P., Duncan A.J., et al. Inhibition of mitochondrial complex IV leads to secondary loss complex II-III activity: implications for the pathogenesis and treatment of mitochondrial encephalomyopathies. Mitochondrion 2007, 7(4):284-287.
25. Hudson G., Carelli V., et al. X-inactivation patterns in females harboring mtDNA mutations that cause Leber hereditary optic neuropathy. Mol. Vis. 2007, 13:2339-2343.
26. Ikeda M., Takemura T., Hino S., Yoshioka K. Molecular cloning, expression, and chromosomal localization of a human tubulointerstitial nephritis antigen. Biochem. Biophys. Res. Commun. 2000, 268(1):225-230.
27. Jellinger K., Seitelberger F. Neuropathology of Rett syndrome. Am. J. Med. Genet. Suppl. 1986, 1:259-288.
28. Johnson K., Farley D., Hu S.I., Terkeltaub R. One of two chondrocyte-expressed isoforms of cartilage intermediate-layer protein functions as an insulin-like growth factor 1 antagonist. Arthritis Rheum. 2003, 48(5):1302-1314.
29. Kirby D.M., Thorburn D.R., Turnbull D.M., Taylor R.W. Biochemical assays of respiratory chain complex activity. Methods Cell Biol. 2007, 80:93-119.
30. Kobayashi M., Yamamoto M. Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species. Adv. Enzyme. Regul. 2006, 46:113-140.
31. Kriaucionis S., Paterson A., et al. Gene expression analysis exposes mitochondrial abnormalities in a mouse model of Rett syndrome. Mol. Cell. Biol. 2006, 26(13):5033-5042.
32. Laurvick C.L., de Klerk N., et al. Rett syndrome in Australia: a review of the epidemiology. J. Pediatr. 2006, 148(3):347-352.
33. Leick L., Lyngby S.S., Wojtaszewski J.F., Pilegaard H. PGC-1alpha is required for training-induced prevention of age-associated decline in mitochondrial enzymes in mouse skeletal muscle. Exp. Gerontol. 2010, 45(5):336-342.
34. Leoncini S., De Felice C., et al. Oxidative stress in Rett syndrome: natural history, genotype, and variants. Redox Rep. 2011, 16(4):145-153.
35. Lodi R., Schapira A.H., et al. Abnormal in vivo skeletal muscle energy metabolism in Huntington's disease and dentatorubropallidoluysian atrophy. Ann. Neurol. 2000, 48(1):72-76.
36. Neul J.L., Kaufmann W.E., et al. Rett syndrome: revised diagnostic criteria and nomenclature. Ann. Neurol. 2010, 68(6):944-950.
37. Pecorelli A., Ciccoli L., et al. Increased levels of 4HNE-protein plasma adducts in Rett syndrome. Clin. Biochem. 2011, 44(5-6):368-371.
38. Pelka G.J., Watson C.M., et al. Mecp2 deficiency is associated with learning and cognitive deficits and altered gene activity in the hippocampal region of mice. Brain 2006, 129(Pt 4):887-898.
39. Petersen K.F., Dufour S., et al. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N. Engl. J. Med. 2004, 350(7):664-671.
40. Puigserver P., Spiegelman B.M. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr. Rev. 2003, 24(1):78-90.
41. Puigserver P., Adelmant G., et al. Activation of PPARgamma coactivator-1 through transcription factor docking. Science 1999, 286(5443):1368-1371.
42. Rett A. On a unusual brain atrophy syndrome in hyperammonemia in childhood. Wien. Med. Wochenschr. 1966, 116(37):723-726.
43. Riederer P., Sofic E., et al. Transition metals, ferritin, glutathione, and ascorbic acid in parkinsonian brains. J. Neurochem. 1989, 52(2):515-520.
44. Ruch A., Kurczynski T.W., Velasco M.E. Mitochondrial alterations in Rett syndrome. Pediatr. Neurol. 1989, 5(5):320-323.
45. Saft C., Zange J., et al. Mitochondrial impairment in patients and asymptomatic mutation carriers of Huntington's disease. Mov. Disord. 2005, 20(6):674-679.
46. Schagger H. Respiratory chain supercomplexes of mitochondria and bacteria. Biochim. Biophys. Acta 2002, 1555(1-3):154-159.
47. Schlame M., Haldar D. Cardiolipin is synthesized on the matrix side of the inner membrane in rat liver mitochondria. J. Biol. Chem. 1993, 268(1):74-79.
48. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 2008, 3(6):1101-1108.
49. Sierra C., Vilaseca M.A., et al. Oxidative stress in Rett syndrome. Brain Dev. 2001, 23(Suppl. 1):S236-S239.
50. Signorini C., De Felice C., et al. F(4)-neuroprostanes mediate neurological severity in Rett syndrome. Clin. Chim. Acta 2011, 412(15-16):1399-1406.
51. Sofic E., Riederer P., Killian W., Rett A. Reduced concentrations of ascorbic acid and glutathione in a single case of Rett syndrome: a postmortem brain study. Brain Dev. 1987, 9(5):529-531.
52. St-Pierre J., Drori S., et al. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 2006, 127(2):397-408.
53. Ungvari Z., Sonntag W.E., et al. Mitochondrial protection by resveratrol. Exerc. Sport Sci. Rev. 2011, 39(3):128-132.
54. Valle I., Alvarez-Barrientos A., et al. PGC-1alpha regulates the mitochondrial antioxidant defense system in vascular endothelial cells. Cardiovasc. Res. 2005, 66(3):562-573.
55. Venditti P., Di Stefano L., Di Meo S. Mitochondrial metabolism of reactive oxygen species. Mitochondrion 2013, 13(2):71-82.
56. Wakai S., Kameda K., et al. Rett syndrome: findings suggesting axonopathy and mitochondrial abnormalities. Pediatr. Neurol. 1990, 6(5):339-343.
57. Wang Y.X., Lee C.H., et al. Peroxisome-proliferator-activated receptor delta activates fat metabolism to prevent obesity. Cell 2003, 113(2):159-170.
58. Wenz T., Rossi S.G., et al. Increased muscle PGC-1alpha expression protects from sarcopenia and metabolic disease during aging. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(48):20405-20410.