Disruption of skeletal muscle mitochondrial network genes and miRNAs in amyotrophic lateral sclerosis

Neurobiology of Disease

Volumn 49, Issue 1, 2013, Pages 107-117

  Russell, Aaron P ^a   Wada, Shogo ^b   Vergani, Lodovica ^c   Hock, M Benjamin ^d   Lamon, Séverine ^a   Léger, Bertrand ^e   Ushida, Takashi ^b   Cartoni, Romain ^e,h   Wadley, Glenn D ^a   Hespel, Peter ^f   Kralli, Anastasia ^d   Soraru, Gianni ^c   Angelini, Corrado ^c,g   Akimoto, Takayuki ^b  

^a DEAKIN UNIVERSITY   (Australia)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF PADOVA   (Italy)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e SUVA   (Switzerland)

^f UNIVERSITY OF LEUVEN   (Belgium)

^g IRCCS SAN CAMILLO HOSPITAL   (Italy)

^h HARVARD MEDICAL SCHOOL   (United States)

Author keywords

ALS (amyotrophic lateral sclerosis); MicroRNA; Mitofusin; Peroxiome proliferator activator receptor co activator 1; Skeletal muscle

Indexed keywords

CITRATE SYNTHASE; CYTOCHROME C OXIDASE; ESTROGEN RELATED RECEPTOR ALPHA; MICRORNA; MICRORNA 206; MICRORNA 23A; MICRORNA 29B; MICRORNA 455; MITOFUSIN 1; MITOFUSIN 2; NUCLEAR RESPIRATORY FACTOR 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; UNCLASSIFIED DRUG; COPPER ZINC SUPEROXIDE DISMUTASE; MESSENGER RNA; MIRN23 MICRORNA, HUMAN; SUPEROXIDE DISMUTASE;

ADULT; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL TISSUE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOCHROME C OXIDASE SUBUNIT IV GENE; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; ESTROGEN RELATED RECEPTOR ALPHA GENE; FEMALE; GENE; GENE DISRUPTION; GENE EXPRESSION REGULATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MALE; MITOFUSIN 1 GENE; MITOFUSIN 2 GENE; MOUSE; MUSCLE REGENERATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; NUCLEAR RESPIRATORY FACTOR 1 GENE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1 ALPHA GENE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1 BETA GENE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE MITOCHONDRIAL NETWORK GENE; TRANSGENIC MOUSE; AGED; ANIMAL; DISEASE MODEL; GENETICS; METABOLISM; MIDDLE AGED; MITOCHONDRION; MUTATION; SKELETAL MUSCLE; YOUNG ADULT;

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE, TRANSGENIC; MICRORNAS; MIDDLE AGED; MITOCHONDRIA; MUSCLE FIBERS, SKELETAL; MUTATION; RNA, MESSENGER; SUPEROXIDE DISMUTASE; YOUNG ADULT;

EID: 84866491615     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.08.015     Document Type: Article

References (73)

1. Adhihetty P.J., et al. Effect of denervation on mitochondrially mediated apoptosis in skeletal muscle. J. Appl. Physiol. 2007, 102:1143-1151.
2. Bach D., et al. Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism. A novel regulatory mechanism altered in obesity. J. Biol. Chem. 2003, 278:17190-17197.
3. Bach D., et al. Expression of Mfn2, the Charcot-Marie-Tooth neuropathy type 2A gene, in human skeletal muscle: effects of type 2 diabetes, obesity, weight loss, and the regulatory role of tumor necrosis factor alpha and interleukin-6. Diabetes 2005, 54:2685-2693.
4. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
5. Bleazard W., et al. The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat. Cell Biol. 1999, 1:298-304.
6. Brault J.J., et al. Peroxisome proliferator-activated receptor gamma coactivator 1alpha or 1beta overexpression inhibits muscle protein degradation, induction of ubiquitin ligases, and disuse atrophy. J. Biol. Chem. 2010, 285:19460-19471.
7. Brooks B.R. El Escorial World Federation of Neurology criteria for the diagnosis of amyotrophic lateral sclerosis. Subcommittee on Motor Neuron Diseases/Amyotrophic Lateral Sclerosis of the World Federation of Neurology Research Group on Neuromuscular Diseases and the El Escorial "Clinical limits of amyotrophic lateral sclerosis" workshop contributors. J. Neurol. Sci. 1994, 124. (Suppl.).
8. Brooks K.J., et al. MRI detects early hindlimb muscle atrophy in Gly93Ala superoxide dismutase-1 (G93A SOD1) transgenic mice, an animal model of familial amyotrophic lateral sclerosis. NMR Biomed. 2004, 17:28-32.
9. Cartoni R., et al. Mitofusins 1/2 and ERRalpha expression are increased in human skeletal muscle after physical exercise. J. Physiol. 2005, 567:349-358.
10. Chen H., et al. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 2010, 141:280-289.
11. Clement A.M., et al. Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 2003, 302:113-117.
12. Crugnola V., et al. Mitochondrial respiratory chain dysfunction in muscle from patients with amyotrophic lateral sclerosis. Arch. Neurol. 2010, 67:849-854.
13. Da Cruz S., et al. Elevated PGC-1alpha activity sustains mitochondrial biogenesis and muscle function without extending survival in a mouse model of inherited ALS. Cell Metab. 2012, 15:778-786.
14. de Brito O.M., Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 2008, 456:605-610.
15. Derave W., et al. Skeletal muscle properties in a transgenic mouse model for amyotrophic lateral sclerosis: effects of creatine treatment. Neurobiol. Dis. 2003, 13:264-272.
16. Diseases of the lower motor neurone. Muscle biopsy. A practical approach 1985, Bailliere Tindall, London U.K. V. Dubowitz (Ed.).
17. Dupuis L., Echaniz-Laguna A. Skeletal muscle in motor neuron diseases: therapeutic target and delivery route for potential treatments. Curr. Drug Targets 2010, 11:1250-1261.
18. Dupuis L., et al. Up-regulation of mitochondrial uncoupling protein 3 reveals an early muscular metabolic defect in amyotrophic lateral sclerosis. FASEB J. 2003, 17:2091-2093.
19. Eisenberg I., et al. Distinctive patterns of microRNA expression in primary muscular disorders. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:17016-17021.
20. Finck B.N., Kelly D.P. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J. Clin. Invest. 2006, 116:615-622.
21. Frey D., et al. Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J. Neurosci. 2000, 20:2534-2542.
22. Gambardella S., et al. Overexpression of microRNA-206 in the skeletal muscle from myotonic dystrophy type 1 patients. J. Transl. Med. 2010, 8:48.
23. Gastaldi G., et al. Upregulation of peroxisome proliferator-activated receptor gamma coactivator gene (PGC1A) during weight loss is related to insulin sensitivity but not to energy expenditure. Diabetologia 2007, 50:2348-2355.
24. Gong Y.H., et al. Restricted expression of G86R Cu/Zn superoxide dismutase in astrocytes results in astrocytosis but does not cause motoneuron degeneration. J. Neurosci. 2000, 20:660-665.
25. Greco S., et al. Common micro-RNA signature in skeletal muscle damage and regeneration induced by Duchenne muscular dystrophy and acute ischemia. FASEB J. 2009, 23:3335-3346.
26. Guller I., Russell A.P. MicroRNAs in skeletal muscle: their role and regulation in development, disease and function. J. Physiol. 2011, 588:4075-4087.
27. Hamilton A.J., Baulcombe D.C. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 1999, 286:950-952.
28. Handschin C., Spiegelman B.M. Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr. Rev. 2006, 27:728-735.
29. Handschin C., et al. PGC-1alpha regulates the neuromuscular junction program and ameliorates Duchenne muscular dystrophy. Genes Dev. 2007, 21:770-783.
30. Holloszy J.O., Booth F.W. Biochemical adaptations to endurance exercise in muscle. Annu. Rev. Physiol. 1976, 38:273-291.
31. Kennel P.F., et al. Neuromuscular function impairment is not caused by motor neurone loss in FALS mice: an electromyographic study. Neuroreport 1996, 7:1427-1431.
32. Kong J., Xu Z. Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral sclerosis in mice expressing a mutant SOD1. J. Neurosci. 1998, 18:3241-3250.
33. Koshiba T., et al. Structural basis of mitochondrial tethering by mitofusin complexes. Science 2004, 305:858-862.
34. Leger B., et al. Human skeletal muscle atrophy in amyotrophic lateral sclerosis reveals a reduction in Akt and an increase in atrogin-1. FASEB J. 2006, 20:583-585.
35. Lelliott C.J., et al. Ablation of PGC-1beta results in defective mitochondrial activity, thermogenesis, hepatic function, and cardiac performance. PLoS Biol. 2006, 4:e369.
36. Liesa M., et al. Mitochondrial fusion is increased by the nuclear coactivator PGC-1beta. PLoS One 2008, 3:e3613.
37. Liu X., et al. MicroRNA-31 regulated by the extracellular regulated kinase is involved in vascular smooth muscle cell growth via large tumor suppressor homolog 2. J. Biol. Chem. 2011, 286:42371-42380.
38. Marcuzzo S., et al. Hind limb muscle atrophy precedes cerebral neuronal degeneration in G93A-SOD1 mouse model of amyotrophic lateral sclerosis: a longitudinal MRI study. Exp. Neurol. 2011, 231:30-37.
39. Mensink M., et al. Improved skeletal muscle oxidative enzyme activity and restoration of PGC-1 alpha and PPAR beta/delta gene expression upon rosiglitazone treatment in obese patients with type 2 diabetes mellitus. Int. J. Obes. (Lond) 2007, 31:1302-1310.
40. Menzies F.M., et al. Mitochondrial involvement in amyotrophic lateral sclerosis. Neurochem. Int. 2002, 40:543-551.
41. Mezzani A., et al. Reduced exercise capacity in early-stage amyotrophic lateral sclerosis: Role of skeletal muscle. Amyotroph. Lateral Scler. 2012, 13:87-94.
42. Mootha V.K., et al. Erralpha and Gabpa/b specify PGC-1alpha-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6570-6575.
43. Oishi Y., et al. Cellular adaptations in soleus muscle during recovery after hindlimb unloading. Acta Physiol (Oxf.) 2008, 192:381-395.
44. Panguluri S.K., et al. Genomic profiling of messenger RNAs and microRNAs reveals potential mechanisms of TWEAK-induced skeletal muscle wasting in mice. PLoS One 2010, 5:e8760.
45. Pasinelli P., Brown R.H. Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat. Rev. Neurosci. 2006, 7:710-723.
46. Perbellini R., et al. Dysregulation and cellular mislocalization of specific miRNAs in myotonic dystrophy type 1. Neuromuscul. Disord. 2011, 21:81-88.
47. Pramatarova A., et al. Neuron-specific expression of mutant superoxide dismutase 1 in transgenic mice does not lead to motor impairment. J. Neurosci. 2001, 21:3369-3374.
48. Puigserver P., et al. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 1998, 92:829-839.
49. Reinhart B.J., et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 403:901-906.
50. Rimbert V., et al. Muscle fat oxidative capacity is not impaired by age but by physical inactivity: association with insulin sensitivity. FASEB J. 2004, 18:737-739.
51. Romanello V., et al. Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J. 2010, 29:1774-1785.
52. Russell A., et al. Slow component of [V]O(2) kinetics: the effect of training status, fibre type, UCP3 mRNA and citrate synthase activity. Int. J. Obes. Relat. Metab. Disord. 2002, 26:157-164.
53. Russell A.P., et al. Endurance training in humans leads to fiber type-specific increases in levels of peroxisome proliferator-activated receptor-gamma coactivator-1 and peroxisome proliferator-activated receptor-alpha in skeletal muscle. Diabetes 2003, 52:2874-2881.
54. Russell A.P., et al. Regulation of metabolic transcriptional co-activators and transcription factors with acute exercise. FASEB J. 2005, 19:986-988.
55. Sandri M., et al. PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:16260-16265.
56. Schreiber S.N., et al. The transcriptional coactivator PGC-1 regulates the expression and activity of the orphan nuclear receptor estrogen-related receptor alpha (ERRalpha). J. Biol. Chem. 2003, 278:9013-9018.
57. Schreiber S.N., et al. The estrogen-related receptor alpha (ERRalpha) functions in PPARgamma coactivator 1alpha (PGC-1alpha)-induced mitochondrial biogenesis. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6472-6477.
58. Selsby J.T., et al. Rescue of dystrophic skeletal muscle by PGC-1alpha involves a fast to slow fiber type shift in the mdx mouse. PLoS One 2012, 7:e30063.
59. Sempere L.F., et al. Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 2004, 5:R13.
60. Short K.R., et al. Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity. Diabetes 2003, 52:1888-1896.
61. Small E.M., et al. Regulation of PI3-kinase/Akt signaling by muscle-enriched microRNA-486. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:4218-4223.
62. van Rooij E., et al. Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 2007, 316:575-579.
63. van Rooij E., et al. A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev. Cell 2009, 17:662-673.
64. Vielhaber S., et al. Mitochondrial DNA abnormalities in skeletal muscle of patients with sporadic amyotrophic lateral sclerosis. Brain 2000, 123:1339-1348.
65. Villena J.A., et al. Orphan nuclear receptor estrogen-related receptor alpha is essential for adaptive thermogenesis. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:1418-1423.
66. Wada S., et al. Translational suppression of atrophic regulators by miR-23a integrates resistance to skeletal muscle atrophy. J. Biol. Chem. 2011, 286:38456-38465.
67. Wallace M.A., et al. Striated muscle activator of Rho signalling (STARS) is a PGC-1α/ERRα target gene and is upregulated in human skeletal muscle following endurance exercise. J. Physiol. 2011, 15:2027-2039.
68. Wang H., et al. NF-kappaB-YY1-miR-29 regulatory circuitry in skeletal myogenesis and rhabdomyosarcoma. Cancer Cell 2008, 14:369-381.
69. Wiedemann F.R., et al. Impairment of mitochondrial function in skeletal muscle of patients with amyotrophic lateral sclerosis. J. Neurol. Sci. 1998, 156:65-72.
70. Williams A.H., et al. MicroRNA-206 delays ALS progression and promotes regeneration of neuromuscular synapses in mice. Science 2009, 326:1549-1554.
71. Wong M., Martin L.J. Skeletal muscle-restricted expression of human SOD1 causes motor neuron degeneration in transgenic mice. Hum. Mol. Genet. 2010, 19:2284-2302.
72. Wu Z., et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 1999, 98:115-124.
73. Zechner C., et al. Total skeletal muscle PGC-1 deficiency uncouples mitochondrial derangements from fiber type determination and insulin sensitivity. Cell Metab. 2010, 12:633-642.