Respiratory chain deficiency in aged spinal motor neurons

Neurobiology of Aging

Volumn 35, Issue 10, 2014, Pages 2230-2238

  Rygiel, Karolina A ^a,b   Grady, John P ^b   Turnbull, Doug M ^a,b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Complex I; Mitochondria; Motor neuron; MtDNA; Sarcopenia; Spinal cord

Indexed keywords

MITOCHONDRIAL DNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

AGED; ARTICLE; AUTOPSY; CELL LOSS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA CONTENT; FEMALE; HUMAN; HUMAN TISSUE; LUMBAR SPINAL CORD; MALE; MITOCHONDRION; MOTONEURON; MOTOR NERVE; MOTOR UNIT; MUSCLE CELL; MUSCLE DENERVATION; MUSCLE MASS; NEUROMUSCULAR SYNAPSE; PRIORITY JOURNAL; RESPIRATORY CHAIN; SARCOPENIA; SKELETAL MUSCLE; SPINAL CORD MOTONEURON; VERY ELDERLY; AGING; CYTOLOGY; DEFICIENCY; METABOLISM; MITOCHONDRIAL DISEASES; PATHOLOGY; SPINAL CORD; ULTRASTRUCTURE;

AGED; AGED, 80 AND OVER; AGING; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT COMPLEX I; FEMALE; HUMANS; MALE; MITOCHONDRIAL DISEASES; MOTOR NEURONS; SARCOPENIA; SPINAL CORD;

EID: 84903820129     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.02.027     Document Type: Article

References (46)

1. Aagaard P., Suetta C., et al. Role of the nervous system in sarcopenia and muscle atrophy with aging: strength training as a countermeasure. Scand. J. Med. Sci. Sports 2010, 20:49-64.
2. Aiken J., Bua E., et al. Mitochondrial DNA deletion mutations and sarcopenia. Ann. N. Y Acad. Sci. 2002, 959:412-423.
3. Andersen J.L. Muscle fibre type adaptation in the elderly human muscle. Scand. J. Med. Sci. Sports 2003, 13:40-47.
4. Borthwick G.M., Johnson M.A., et al. Mitochondrial enzyme activity in amyotrophic lateral sclerosis: implications for the role of mitochondria in neuronal cell death. Ann. Neurol. 1999, 46:787-790.
5. Brown W.F., Strong M.J., et al. Methods for estimating numbers of motor units in biceps-brachialis muscles and losses of motor units with aging. Muscle Nerve 1988, 11:423-432.
6. Caccia M.R., Harris J.B., et al. Morphology and physiology of skeletal muscle in aging rodents. Muscle Nerve 1979, 2:202-212.
7. Campbell M.J., McComas A.J., et al. Physiological changes in ageing muscles. J.Neurol. Neurosurg. Psychiatry 1973, 36:174-182.
8. Chai R.J., Vukovic J., et al. Striking denervation of neuromuscular junctions without lumbar motoneuron loss in geriatric mouse muscle. PLoS One 2011, 6:e28090.
9. Comi G.P., Bordoni A., et al. Cytochrome c oxidase subunit I microdeletion in a patient with motor neuron disease. Ann. Neurol. 1998, 43:110-116.
10. Dave K.R., Bradley W.G., et al. Early mitochondrial dysfunction occurs in motor cortex and spinal cord at the onset of disease in the Wobbler mouse. Exp. Neurol. 2003, 182:412-420.
11. Delbono O. Neural control of aging skeletal muscle. Aging Cell 2003, 2:21-29.
12. Doherty T.J., Brown W.F. The estimated numbers and relative sizes of thenar motor units as selected by multiple point stimulation in young and older adults. Muscle Nerve 1993, 16:355-366.
13. Ekstrand M., Larsson N.G. Breeding and genotyping of Tfam conditional knockout mice. Methods Mol. Biol. 2002, 197:391-400.
14. Fassone E., Rahman S. Complex I deficiency: clinical features, biochemistry and molecular genetics. J.Med. Genet. 2012, 49:578-590.
15. Fielding R.A., Vellas B., et al. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J.Am. Med. Dir. Assoc. 2011, 12:249-256.
16. Frontera W.R., Hughes V.A., et al. Aging of skeletal muscle: a 12-yr longitudinal study. J.Appl. Physiol. 2000, 88:1321-1326.
17. Greaves L.C., Turnbull D.M. Mitochondrial DNA mutations and ageing. Biochim. Biophys. Acta 2009, 1790:1015-1020.
18. Hakonen A.H., Goffart S., et al. 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.
19. Harish G., Venkateshappa C., et al. Mitochondrial function in human brains is affected by pre- and post mortem factors. Neuropathol. Appl. Neurobiol. 2013, 39:298-315.
20. Jung C., Higgins C.M., et al. Aquantitative histochemical assay for activities of mitochondrial electron transport chain complexes in mouse spinal cord sections. J.Neurosci. Methods 2002, 114:165-172.
21. Kawamura Y., Okazaki H., et al. Lumbar motoneurons of man: I) number and diameter histogram of alpha and gamma axons of ventral root. J.Neuropathol. Exp. Neurol. 1977, 36:853-860.
22. Kirby D.M., Crawford M., et al. Respiratory chain complex I deficiency: an underdiagnosed energy generation disorder. Neurology 1999, 52:1255-1264.
23. Krishnan K.J., Bender A., et al. Amultiplex real-time PCR method to detect and quantify mitochondrial DNA deletions in individual cells. Anal. Biochem. 2007, 370:127-129.
24. Kruse S.E., Watt W.C., et al. Mice with mitochondrial complex I deficiency develop a fatal encephalomyopathy. Cell Metab 2008, 7:312-320.
25. Landfield P.W., Thibault O., et al. Mechanisms of neuronal death in brain aging and Alzheimer's disease: role of endocrine-mediated calcium dyshomeostasis. J.Neurobiol. 1992, 23:1247-1260.
26. Larsson L. Motor units: remodeling in aged animals. J.Gerontol. A Biol. Sci. Med. Sci. 1995, 50 Spec No:91-95.
27. Lax N.Z., Hepplewhite P.D., et al. Cerebellar ataxia in patients with mitochondrial DNA disease: a molecular clinicopathological study. J.Neuropathol. Exp. Neurol. 2012, 71:148-161.
28. Lexell J. Evidence for nervous system degeneration with advancing age. J.Nutr. 1997, 127(5 Suppl):1011S-1013S.
29. Lexell J., Downham D.Y. The occurrence of fibre-type grouping in healthy human muscle: a quantitative study of cross-sections of whole vastus lateralis from men between 15 and 83 years. Acta Neuropathol. 1991, 81:377-381.
30. Lexell J., Taylor C.C. Variability in muscle fibre areas in whole human quadriceps muscle: effects of increasing age. J.Anat. 1991, 174:239-249.
31. McKiernan S.H., Colman R., et al. Longitudinal analysis of early stage sarcopenia in aging rhesus monkeys. Exp. Gerontol. 2009, 44:170-176.
32. McNeil C.J., Doherty T.J., et al. Motor unit number estimates in the tibialis anterior muscle of young, old, and very old men. Muscle Nerve 2005, 31:461-467.
33. Murphy J.L., Blakely E.L., et al. Resistance training in patients with single, large-scale deletions of mitochondrial DNA. Brain 2008, 131:2832-2840.
34. Old S.L., Johnson M.A. Methods of microphotometric assay of succinate dehydrogenase and cytochrome c oxidase activities for use on human skeletal muscle. Histochem. J. 1989, 21:545-555.
35. Pagliarini D.J., Calvo S.E., et al. Amitochondrial protein compendium elucidates complex I disease biology. Cell 2008, 134:112-123.
36. Quintana A., Kruse S.E., et al. Complex I deficiency due to loss of Ndufs4 in the brain results in progressive encephalopathy resembling Leigh syndrome. Proc. Natl. Acad. Sci. U S A 2010, 107:10996-11001.
37. Rowan S.L., Rygiel K., et al. Denervation causes fiber atrophy and myosin heavy chain co-expression in senescent skeletal muscle. PLoS One 2012, 7:e29082.
38. Silva J.P., Larsson N.G. Manipulation of mitochondrial DNA gene expression in the mouse. Biochim. Biophys. Acta 2002, 1555:106-110.
39. Smeitink J.A., van den Heuvel L.W., et al. Cell biological consequences of mitochondrial NADH: ubiquinone oxidoreductase deficiency. Curr. Neurovasc Res. 2004, 1:29-40.
40. Stalberg E., Fawcett P.R. Macro EMG in healthy subjects of different ages. J.Neurol. Neurosurg. Psychiatry 1982, 45:870-878.
41. Tomlinson B.E., Irving D. The numbers of limb motor neurons in the human lumbosacral cord throughout life. J.Neurol. Sci. 1977, 34:213-219.
42. Urbanchek M.G., Picken E.B., et al. Specific force deficit in skeletal muscles of old rats is partially explained by the existence of denervated muscle fibers. J.Gerontol. A Biol. Sci. Med. Sci. 2001, 56:B191-B197.
43. Valdez G., Tapia J.C., et al. Attenuation of age-related changes in mouse neuromuscular synapses by caloric restriction and exercise. Proc. Natl. Acad. Sci. U S A 2010, 107:14863-14868.
44. von Haehling S., Morley J.E., et al. An overview of sarcopenia: facts and numbers on prevalence and clinical impact. J.Cachexia Sarcopenia Muscle 2010, 1:129-133.
45. Wang Z.M., Zheng Z., et al. Extension and magnitude of denervation in skeletal muscle from ageing mice. J.Physiol. 2005, 565(Pt 3):757-764.
46. Wiedemann F.R., Manfredi G., et al. Mitochondrial DNA and respiratory chain function in spinal cords of ALS patients. J.Neurochem. 2002, 80:616-625.