The neuromuscular junction: Aging at the crossroad between nerves and muscle

Frontiers in Aging Neuroscience

Volumn 6, Issue AUG, 2014, Pages

  Gonzalez Freire, Marta ^a   de Cabo, Rafael ^a   Studenski, Stephanie A ^a   Ferrucci, Luigi ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Aging; Denervation; Motor unit; Neuromuscular junction; Sarcopenia

Indexed keywords

AGRIN; BIOLOGICAL MARKER; COPPER ZINC SUPEROXIDE DISMUTASE; NEUROTROPHIC FACTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SODIUM CHANNEL NAV1.5; SOMATOMEDIN C;

AGING; APOPTOSIS; CALORIC RESTRICTION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY YIELD; EXERCISE; HUMAN; INFLAMMATION; INNERVATION; MOTONEURON; MOTOR UNIT; MUSCLE ACTION POTENTIAL; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE CONTRACTION; NERVE ENDING; NERVE FIBER; NEUROMUSCULAR DISEASE; NEUROMUSCULAR JUNCTION DYSFUNCTION; NEUROMUSCULAR SYNAPSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN DEGRADATION; REVIEW; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY;

EID: 84906225383     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2014.00208     Document Type: Review

References (146)

1. Afilalo, J., Alexander, K. P., Mack, M. J., Maurer, M. S., Green, P., Allen, L. A., et al. (2014). Frailty assessment in the cardiovascular care of older adults. J. Am. Coll. Cardiol. 63, 747-762. doi: 10.1016/j.jacc.2013.09.070
2. Andersen, J. L. (2003). Muscle fibre type adaptation in the elderly human muscle. Scand. J. Med. Sci. Sports 13, 40-47. doi:10.1034/j.1600-0838.2003.00299.x
3. Anderson, R. M., and Weindruch, R. (2012). The caloric restriction paradigm: implications for healthy human aging. Am. J. Hum. Biol. 24, 101-106. doi:10.1002/ajhb.22243
4. Apel, P. J., Ma, J., Callahan, M., Northam, C. N., Alton, T. B., Sonntag, W. E., et al. (2010). Effect of locally delivered IGF-1 on nerve regeneration during aging: an experimental study in rats. Muscle Nerve 41, 335-341. doi:10.1002/mus.21485
5. Arnold, A. S., Gill, J., Christe, M., Ruiz, R., McGuirk, S., St-Pierre, J., et al. (2014). Morphological and functional remodelling of the neuromuscular junction by skeletal muscle PGC-1alpha. Nat Commun 5, 3569. doi:10.1038/ncomms4569
6. Arrowsmith, J. E. (2007). The neuromuscular junction. Surgery (Oxford) 25, 105-111. doi:10.1016/j.mpsur.2007.02.001
7. Baines, H. L., Turnbull, D. M., and Greaves, L. C. (2014). Human stem cell aging: do mitochondrial DNA mutations have a causal role? Aging Cell 13, 201-205. doi:10.1111/acel.12199
8. Banker, B. Q., Kelly, S. S., and Robbins, N. (1983). Neuromuscular transmission and correlative morphology in young and old mice. J. Physiol. 339, 355-377.
9. Barrett, E. F., Barrett, J. N., and David, G. (2011). Mitochondria in motor nerve terminals: function in health and in mutant superoxide dismutase 1 mouse models of familial ALS. J. Bioenerg. Biomembr. 43, 581-586. doi:10.1007/s10863-011-9392-1
10. Belluardo, N., Westerblad, H., Mudo, G., Casabona, A., Bruton, J., Caniglia, G., et al. (2001). Neuromuscular junction disassembly and muscle fatigue in mice lacking neurotrophin 4. Mol. Cell. Neurosci. 18, 56-67. doi:10.1006/mcne.2001.1001
11. Bodine, S. C., Latres, E., Baumhueter, S., Lai, V. K., Nunez, L., Clarke, B. A., et al. (2001). Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294, 1704-1708. doi:10.1126/science.1065874
12. Bolliger, M. F., Zurlinden, A., Luscher, D., Butikofer, L., Shakhova, O., Francolini, M., et al. (2010). Specific proteolytic cleavage of agrin regulates maturation of the neuromuscular junction. J. Cell Sci. 123(Pt 22), 3944-3955. doi:10.1242/jcs.072090
13. Butikofer, L., Zurlinden, A., Bolliger, M. F., Kunz, B., and Sonderegger, P. (2011). Destabilization of the neuromuscular junction by proteolytic cleavage of agrin results in precocious sarcopenia. FASEB J. 25, 4378-4393. doi:10.1096/fj.11-191262
14. Chai, R. J., Vukovic, J., Dunlop, S., Grounds, M. D., and Shavlakadze, T. (2011). Striking denervation of neuromuscular junctions without lumbar motoneuron loss in geriatric mouse muscle. PLoS ONE 6:e28090. doi:10.1371/journal.pone.0028090
15. Cheng, A., Morsch, M., Murata, Y., Ghazanfari, N., Reddel, S. W., and Phillips, W. D. (2013). Sequence of age-associated changes to the mouse neuromuscular junction and the protective effects of voluntary exercise. PLoS ONE 8:e67970. doi:10.1371/journal.pone.0067970
16. Chistiakov, D. A., Sobenin, I. A., Revin, V. V., Orekhov, A. N., and Bobryshev, Y. V. (2014). Mitochondrial Aging and Age-Related Dysfunction of Mitochondria. BioMed. Res. Int. 2014, 238463. doi:10.1155/2014/238463
17. Clark, D. J., and Fielding, R. A. (2012). Neuromuscular contributions to age-related weakness. J Gerontol A. Biol. Sci. Med. Sci. 67, 41-47. doi:10.1093/gerona/glr041
18. Clark, D. J., Pojednic, R. M., Reid, K. F., Patten, C., Pasha, E. P., Phillips, E. M., et al. (2013). Longitudinal decline of neuromuscular activation and power in healthy older adults. J. Gerontol. 68, 1419-1425. doi:10.1093/gerona/glt036
19. Conboy, I. M., and Rando, T. A. (2012). Heterochronic parabiosis for the study of the effects of aging on stem cells and their niches. Cell Cycle (Georgetown, Tex.) 11, 2260-2267. doi:10.4161/cc.20437
20. Degens, H. (2010). The role of systemic inflammation in age-related muscle weakness and wasting. Scand. J. Med. Sci. Sports 20, 28-38. doi:10.1111/j.1600-0838.2009.01018.x
21. Degens, H., and Alway, S. E. (2006). Control of muscle size during disuse, disease, and aging. Int. J. Sports Med. 27, 94-99. doi:10.1055/s-2005-837571
22. Delbono, O. (2000). Regulation of excitation contraction coupling by insulin-like growth factor-1 in aging skeletal muscle. J. Nutr. Health Aging 4, 162-164.
23. Delbono, O. (2003). Neural control of aging skeletal muscle. Aging Cell 2, 21-29. doi:10.1046/j.1474-9728.2003.00011.x
24. Delbono, O., O'Rourke, K. S., and Ettinger, W. H. (1995). Excitation-calcium release uncoupling in aged single human skeletal muscle fibers. J. Memb. Biol. 148, 211-222. doi:10.1007/BF00235039
25. Delbono, O., Renganathan, M., and Messi, M. L. (1997). Excitation-Ca2+ release-contraction coupling in single aged human skeletal muscle fiber. Muscle Nerve Suppl. 5, S88-S92. doi:10.1002/(SICI)1097-4598(1997)5+<88::AID-MUS21>3.0.CO;2-U
26. Derbre, F., Gomez-Cabrera, M. C., Nascimento, A. L., Sanchis-Gomar, F., Martinez-Bello, V. E., Tresguerres, J. A., et al. (2012). Age associated low mitochondrial biogenesis may be explained by lack of response of PGC-1alpha to exercise training. Age (Dordr) 34, 669-679. doi:10.1007/s11357-011-9264-y
27. Deschenes, M. R. (2011). Motor unit and neuromuscular junction remodeling with aging. Curr Aging Sci 4, 209-220. doi:10.2174/1874609811104030209
28. Deschenes, M. R., Roby, M. A., Eason, M. K., and Harris, M. B. (2010). Remodeling of the neuromuscular junction precedes sarcopenia related alterations in myofibers. Exp. Gerontol. 45, 389-393. doi:10.1016/j.exger.2010.03.007
29. Drey, M., Sieber, C. C., Bauer, J. M., Uter, W., Dahinden, P., Fariello, R. G., et al. (2013). C-terminal agrin fragment as a potential marker for sarcopenia caused by degeneration of the neuromuscular junction. Exp. Gerontol. 48, 76-80. doi:10.1016/j.exger.2012.05.021
30. Dupuis, L., Gonzalez de Aguilar, J.-L., Echaniz-Laguna, A., Eschbach, J., Rene, F., Oudart, H., et al. (2009). Muscle mitochondrial uncoupling dismantles neuromuscular junction and triggers distal degeneration of motor neurons. PLoS ONE 4:e5390. doi:10.1371/journal.pone.0005390
31. Dupuis, L., Oudart, H., Rene, F., Gonzalez de Aguilar, J. L., and Loeffler, J. P. (2004). Evidence for defective energy homeostasis in amyotrophic lateral sclerosis: benefit of a high-energy diet in a transgenic mouse model. Proc. Natl. Acad. Sci. U S A. 101, 11159-11164. doi:10.1073/pnas.0402026101
32. Dupuis, L., Pradat, P. F., Ludolph, A. C., and Loeffler, J. P. (2011). Energy metabolism in amyotrophic lateral sclerosis. Lancet Neurol. 10, 75-82. doi:10.1016/S1474-4422(10)70224-6
33. Fahim, M. A. (1997). Endurance exercise modulates neuromuscular junction of C57BL/6NNia aging mice. J. Appl. Physiol. 83, 59-66.
34. Ferrucci, L., Baroni, M., Ranchelli, A., Lauretani, F., Maggio, M., Mecocci, P., et al. (2014). Interaction between bone and muscle in older persons with mobility limitations. Curr. Pharm. Des. 20, 3178-3197. doi:10.2174/13816128113196660690
35. Ferrucci, L., Corsi, A., Lauretani, F., Bandinelli, S., Bartali, B., Taub, D. D., et al. (2005). The origins of age-related proinflammatory state. Blood 105, 2294-2299. doi:10.1182/blood-2004-07-2599
36. Ferrucci, L., de Cabo, R., Knuth, N. D., and Studenski, S. (2012). Of Greek heroes, wiggling worms, mighty mice, and old body builders. J Gerontol. A. Biol. Sci. Med. Sci. 67, 13-16. doi:10.1093/gerona/glr046
37. Ferrucci, L., Giallauria, F., and Schlessinger, D. (2008). Mapping the road to resilience: novel math for the study of frailty. Mech. Ageing Dev. 129, 677-679. doi:10.1016/j.mad.2008.09.007
38. Ferrucci, L., Harris, T. B., Guralnik, J. M., Tracy, R. P., Corti, M. C., Cohen, H. J., et al. (1999). Serum IL-6 level and the development of disability in older persons. J. Am. Geriatr. Soc. 47, 639-646.
39. Fontana, L., Partridge, L., and Longo, V. D. (2010). Extending healthy life span - from yeast to humans. Science 328, 321-326. doi:10.1126/science.1172539
40. Franceschi, C., Capri, M., Monti, D., Giunta, S., Olivieri, F., Sevini, F., et al. (2007). Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech Ageing Dev 128, 92-105. doi:10.1016/j.mad.2006.11.016
41. Franke, B., Gasch, A., Rodriguez, D., Chami, M., Khan, M. M., Rudolf, R., et al. (2014). Molecular basis for the fold organization and sarcomeric targeting of the muscle atrogin MuRF1. Open Biol. 4, 130172. doi:10.1098/rsob.130172
42. Furlow, J. D., Watson, M. L., Waddell, D. S., Neff, E. S., Baehr, L. M., Ross, A. P., et al. (2013). Altered gene expression patterns in muscle ring finger 1 null mice during denervation- and dexamethasone-induced muscle atrophy. Physiol. Genomics 45, 1168-1185. doi:10.1152/physiolgenomics.00022.2013
43. Garcia, M. L., Fernandez, A., and Solas, M. T. (2013). Mitochondria, motor neurons and aging. J. Neurol. Sci. 330, 18-26. doi:10.1016/j.jns.2013.03.019
44. Garcia-Valles, R., Gomez-Cabrera, M. C., Rodriguez-Manas, L., Garcia-Garcia, F. J., Diaz, A., Noguera, I., et al. (2013). Life-long spontaneous exercise does not prolong lifespan but improves health span in mice. Longev. Healthspan 2, 14. doi:10.1186/2046-2395-2-14
45. Gillette-Guyonnet, S., and Vellas, B. (2008). Caloric restriction and brain function. Curr. Opin. Clin. Nutr. Metab. Care 11, 686-692. doi:10.1097/MCO.0b013e328313968f
46. Glass, D., and Roubenoff, R. (2010). Recent advances in the biology and therapy of muscle wasting. Ann. N Y Acad. Sci. 1211, 25-36. doi:10.1111/j.1749-6632.2010.05809.x
47. Gomez-Pinilla, F. (2011). The combined effects of exercise and foods in preventing neurological and cognitive disorders. Prev. Med. 52(Suppl. 1), S75-S80. doi:10.1016/j.ypmed.2011.01.023
48. Gomez-Pinilla, F., Ying, Z., Roy, R. R., Molteni, R., and Edgerton, V. R. (2002). Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. J. Neurophysiol. 88, 2187-2195. doi:10.1152/jn.00152.2002
49. Gordon, T., Udina, E., Verge, V. M. K., and de Chaves, E. I. P. (2009). Brief electrical stimulation accelerates axon regeneration in the peripheral nervous system and promotes sensory axon regeneration in the central nervous system. Motor Control 13, 412-441.
50. Gouspillou, G., and Hepple, R. T. (2013). Facts and controversies in our understanding of how caloric restriction impacts the mitochondrion. Exp. Gerontol. 48, 1075-1084. doi:10.1016/j.exger.2013.03.004
51. Gouspillou, G., Picard, M., Godin, R., Burelle, Y., and Hepple, R. T. (2013). Role of peroxisome proliferator-activated receptor gamma coactivator 1-alpha (PGC-1alpha) in denervation-induced atrophy in aged muscle: facts and hypotheses. Longev. Healthspan 2, 13. doi:10.1186/2046-2395-2-13
52. Gyorkos, A. M., McCullough, M. J., and Spitsbergen, J. M. (2014). Glial cell line-derived neurotrophic factor (GDNF) expression and NMJ plasticity in skeletal muscle following endurance exercise. Neuroscience 257, 111-118. doi:10.1016/j.neuroscience.2013.10.068
53. Handschin, C., Kobayashi, Y. M., Chin, S., Seale, P., Campbell, K. P., and Spiegelman, B. M. (2007). PGC-1alpha regulates the neuromuscular junction program and ameliorates Duchenne muscular dystrophy. Genes Dev. 21, 770-783. doi:10.1101/gad.1525107
54. Hettwer, S., Dahinden, P., Kucsera, S., Farina, C., Ahmed, S., Fariello, R., et al. (2013). Elevated levels of a C-terminal agrin fragment identifies a new subset of sarcopenia patients. Exp. Gerontol. 48, 69-75. doi:10.1016/j.exger.2012.03.002
55. Huang, E. J., and Reichardt, L. F. (2001). Neurotrophins: roles in neuronal development and function. Ann. Rev. Neurosci. 24, 677-736. doi:10.1146/annurev.neuro.24.1.677
56. Hurley, B. F., Hanson, E. D., and Sheaff, A. K. (2011). Strength training as a countermeasure to aging muscle and chronic disease. Sports Med. 41, 289-306. doi:10.2165/11585920-000000000-00000
57. Ibebunjo, C., Chick, J. M., Kendall, T., Eash, J. K., Li, C., Zhang, Y., et al. (2013). Genomic and proteomic profiling reveals reduced mitochondrial function and disruption of the neuromuscular junction driving rat sarcopenia. Mol. Cel. Biol. 33, 194-212. doi:10.1128/MCB.01036-12
58. Jang, Y. C., Liu, Y., Hayworth, C. R., Bhattacharya, A., Lustgarten, M. S., Muller, F. L., et al. (2012). Dietary restriction attenuates age-associated muscle atrophy by lowering oxidative stress in mice even in complete absence of CuZnSOD. Aging Cell 11, 770-782. doi:10.1111/j.1474-9726.2012.00843.x
59. Jang, Y. C., and Van Remmen, H. (2009). The mitochondrial theory of aging: insight from transgenic and knockout mouse models. Exp. Gerontol. 44, 256-260. doi:10.1016/j.exger.2008.12.006
60. Jang, Y. C., and Van Remmen, H. (2011). Age-associated alterations of the neuromuscular junction. Exp. Gerontol. 46, 193-198. doi:10.1016/j.exger.2010.08.029
61. Jiang, X., Tian, F., Du, Y., Copeland, N. G., Jenkins, N. A., Tessarollo, L., et al. (2008). BHLHB2 controls Bdnf promoter 4 activity and neuronal excitability. J. Neurosci. 28, 1118-1130. doi:10.1523/JNEUROSCI.2262-07.2008
62. Kallen, R. G., Sheng, Z. H., Yang, J., Chen, L. Q., Rogart, R. B., and Barchi, R. L. (1990). Primary structure and expression of a sodium channel characteristic of denervated and immature rat skeletal muscle. Neuron 4, 233-242. doi:10.1016/0896-6273(90)90098-Z
63. Kawabuchi, M., Tan, H., and Wang, S. (2011). Age affects reciprocal cellular interactions in neuromuscular synapses following peripheral nerve injury. Ageing Res. Rev. 10, 43-53. doi:10.1016/j.arr.2010.10.003
64. Kawabuchi, M., Zhou, C. J., Wang, S., Nakamura, K., Liu, W. T., and Hirata, K. (2001). The spatio temporal relationship among Schwann cells, axons and post-synaptic acetylcholine receptor regions during muscle reinnervation in aged rats. Anat. Rec. 264, 183-202. doi:10.1002/ar.1159
65. Khan, M. M., Strack, S., Wild, F., Hanashima, A., Gasch, A., Brohm, K., et al. (2014). Role of autophagy, SQSTM1, SH3GLB1, and TRIM63 in the turnover of nicotinic acetylcholine receptors. Autophagy 10, 123-136. doi:10.4161/auto.26841
66. Kim, H. A., Mindos, T., and Parkinson, D. B. (2013). Plastic fantastic: Schwann cells and repair of the peripheral nervous system. Stem Cells Transl. Med. 2, 553-557. doi:10.5966/sctm.2013-0011
67. Korkut, C., and Budnik, V. (2009). WNTs tune up the neuromuscular junction. Nat. Rev. Neurosci. 10, 627-634. doi:10.1038/nrn2681
68. Kraner, S. D., Novak, K. R., Wang, Q., Peng, J., and Rich, M. M. (2012). Altered sodium channel-protein associations in critical illness myopathy. Skelet. Muscle 2, 17. doi:10.1186/2044-5040-2-17
69. Kurokawa, K., Mimori, Y., Tanaka, E., Kohriyama, T., and Nakamura, S. (1999). Age-related change in peripheral nerve conduction: compound muscle action potential duration and dispersion. Gerontology 45, 168-173. doi:10.1159/000022081
70. Lecker, S. H., Jagoe, R. T., Gilbert, A., Gomes, M., Baracos, V., Bailey, J., et al. (2004). Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 18, 39-51.
71. Lexell, J. (1995). Human aging, muscle mass, and fiber type composition. J Gerontol. A. Biol. Sci. Med. Sci. 50 Spec No, 11-16.
72. Lexell, J. (1997). Evidence for nervous system degeneration with advancing age. J. Nutr. 127, 1011S-1013S.
73. Li, H., Kumar Sharma, L., Li, Y., Hu, P., Idowu, A., Liu, D., et al. (2013). Comparative bioenergetic study of neuronal and muscle mitochondria during aging. Free Rad. Biol. Med. 63, 30-40. doi:10.1016/j.freeradbiomed.2013.04.030
74. Li, L., Wu, W., Lin, L. F., Lei, M., Oppenheim, R. W., and Houenou, L. J. (1995). Rescue of adult mouse motoneurons from injury-induced cell death by glial cell line-derived neurotrophic factor. Proc. Natl. Acad. Sci.U S A 92, 9771-9775. doi:10.1073/pnas.92.21.9771
75. Li, Y., Lee, Y. I., and Thompson, W. J. (2011). Changes in aging mouse neuromuscular junctions are explained by degeneration and regeneration of muscle fiber segments at the synapse. J. Neurosci. 31, 14910-14919. doi:10.1523/JNEUROSCI.3590-11.2011
76. Liang, H., Ward, W. F., Jang, Y. C., Bhattacharya, A., Bokov, A. F., Li, Y., et al. (2011). PGC-1alpha protects neurons and alters disease progression in an amyotrophic lateral sclerosis mouse model. Muscle Nerve 44, 947-956. doi:10.1002/mus.22217
77. Lie, D. C., and Weis, J. (1998). GDNF expression is increased in denervated human skeletal muscle. Neurosci. Lett. 250, 87-90. doi:10.1016/S0304-3940(98)00434-0
78. Lin, L. F., Doherty, D. H., Lile, J. D., Bektesh, S., and Collins, F. (1993). GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 260, 1130-1132. doi:10.1126/science.8493557
79. Lin, M. T., and Beal, M. F. (2006). Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443, 787-795. doi:10.1038/nature05292
80. Lipsky, R. H., and Marini, A. M. (2007). Brain-derived neurotrophic factor in neuronal survival and behavior-related plasticity. Ann. NY Acad. Sci 1122, 130-143. doi:10.1196/annals.1403.009
81. Luff, A. R. (1998). Age-associated changes in the innervation of muscle fibers and changes in the mechanical properties of motor units. Ann. N. Y. Acad. Sci. 854, 92-101. doi:10.1111/j.1749-6632.1998.tb09895.x
82. Maggio, M., Ble, A., Ceda, G. P., and Metter, E. J. (2006). Decline in insulin-like growth factor-I levels across adult life span in two large population studies. J. Gerontol. A Biol. Sci. Med. Sci. 61, 182-183. doi:10.1093/gerona/61.2.182
83. Maggio, M., De Vita, F., Lauretani, F., Butto, V., Bondi, G., Cattabiani, C., et al. (2013). IGF-1, the cross road of the nutritional, inflammatory and hormonal pathways to frailty. Nutrients 5, 4184-4205. doi:10.3390/nu5104184
84. Manini, T. M., Hong, S. L., and Clark, B. C. (2013). Aging and muscle: a neuron's perspective. Curr. Opin. Clin. Nutr. Metab. Care 16, 21-26. doi:10.1097/MCO.0b013e32835b5880
85. Mayhew, M., Renganathan, M., and Delbono, O. (1998). Effectiveness of caloric restriction in preventing age-related changes in rat skeletal muscle. Biochem. Biophys. Res. Commun. 251, 95-99. doi:10.1006/bbrc.1998.9438
86. McCay, C. M., Crowell, M. F., and Maynard, L. A. (1935). The effect of retarded growth upon the length of life span and upon the ulti- mate body size. J. Nutr. 10, 63-79.
87. McCullough, M. J., Gyorkos, A. M., and Spitsbergen, J. M. (2013). Short-term exercise increases GDNF protein levels in the spinal cord of young and old rats. Neuroscience 240, 258-268. doi:10.1016/j.neuroscience.2013.02.063
88. McCullough, M. J., Peplinski, N. G., Kinnell, K. R., and Spitsbergen, J. M. (2011). Glial cell line-derived neurotrophic factor protein content in rat skeletal muscle is altered by increased physical activity in vivo and in vitro. Neuroscience 174, 234-244. doi:10.1016/j.neuroscience.2010.11.016
89. McKiernan, S. H., Bua, E., McGorray, J., and Aiken, J. (2004). Early-onset calorie restriction conserves fiber number in aging rat skeletal muscle. FASEB J. 18, 580-581.
90. Mercken, E. M., Carboneau, B. A., Krzysik-Walker, S. M., and de Cabo, R. (2012). Of mice and men: the benefits of caloric restriction, exercise, and mimetics. Ageing Res. Rev. 11, 390-398. doi:10.1016/j.arr.2011.11.005
91. Messi, M. L., and Delbono, O. (2003). Target-derived trophic effect on skeletal muscle innervation in senescent mice. J. Neurosci. 23, 1351-1359.
92. Morel, J., Rannou, F., Talarmin, H., Giroux-Metges, M. A., Pennec, J. P., Dorange, G., et al. (2010). Sodium channel Na(V)1.5 expression is enhanced in cultured adult rat skeletal muscle fibers. J. Membr. Biol. 235, 109-119. doi:10.1007/s00232-010-9262-5
93. Muller, F. L., Song, W., Jang, Y. C., Liu, Y., Sabia, M., Richardson, A., et al. (2007). Denervation-induced skeletal muscle atrophy is associated with increased mitochondrial ROS production. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R1159-R1168. doi:10.1152/ajpregu.00767.2006
94. Mulligan, K. A., and Cheyette, B. N. R. (2012). Wnt signaling in vertebrate neural development and function. J. Neuroimmune Pharmacol. 7, 774-787. doi:10.1007/s11481-012-9404-x
95. Musaro, A., McCullagh, K., Paul, A., Houghton, L., Dobrowolny, G., Molinaro, M., et al. (2001). Localized IGF-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat. Genet. 27, 195-200. doi:10.1038/84839
96. Navarro, A., and Boveris, A. (2009). Brain mitochondrial dysfunction and oxidative damage in Parkinson's disease. J. Bioenerg. Biomembr 41, 517-521. doi:10.1007/s10863-009-9250-6
97. Nguyen, Q. T., Parsadanian, A. S., Snider, W. D., and Lichtman, J. W. (1998). Hyperinnervation of neuromuscular junctions caused by GDNF overexpression in muscle. Science 279, 1725-1729. doi:10.1126/science.279.5357.1725
98. Nishimune, H., Numata, T., Chen, J., Aoki, Y., Wang, Y., Starr, M. P., et al. (2012). Active zone protein Bassoon co-localizes with presynaptic calcium channel, modifies channel function, and recovers from aging related loss by exercise. PLoS ONE 7:e38029. doi:10.1371/journal.pone.0038029
99. Nishimune, H., Stanford, J. A., and Mori, Y. (2014). Role of exercise in maintaining the integrity of the neuromuscular junction. Muscle & Nerve 49, 315-324. doi:10.1002/mus.24095
100. Nordquist, J., Hoglund, A. S., Norman, H., Tang, X., Dworkin, B., and Larsson, L. (2007). Transcription factors in muscle atrophy caused by blocked neuromuscular transmission and muscle unloading in rats. Mol. Med. 13, 461-470. doi:10.2119/2006-00066
101. Okerlund, N. D., and Cheyette, B. N. (2011). Synaptic Wnt signaling; a contributor to major psychiatric disorders? J. Neurodev. Disord. 3, 162-174. doi:10.1007/s11689-011-9083-6
102. Payne, A. M., Zheng, Z., Messi, M. L., Milligan, C. E., Gonzalez, E., and Delbono, O. (2006). Motor neurone targeting of IGF-1 prevents specific force decline in ageing mouse muscle. J. Physiol. 570(Pt 2), 283-294. doi:10.1113/jphysiol.2005.100032
103. Peng, H. B., Yang, J. F., Dai, Z., Lee, C. W., Hung, H. W., Feng, Z. H., et al. (2003). Differential effects of neurotrophins and Schwann cell-derived signals on neuronal survival/growth and synaptogenesis. J. Neurosci. 23, 5050-5060.
104. Peterson, C. M., Johannsen, D. L., and Ravussin, E. (2012). Skeletal muscle mitochondria and aging: a review. J. Aging Res. 2012, 194821. doi:10.1155/2012/194821
105. Punga, A. R., and Ruegg, M. A. (2012). Signaling and aging at the neuromuscular synapse: lessons learnt from neuromuscular diseases. Curr. Opin. Pharmacol. 12, 340-346. doi:10.016/j.coph.2012.02.002
106. Rangaraju, S., Hankins, D., Madorsky, I., Madorsky, E., Lee, W. H., Carter, C. S., et al. (2009). Molecular architecture of myelinated peripheral nerves is supported by calorie restriction with aging. Aging Cell 8, 178-191. doi:10.1111/j.1474-9726.2009.00460.x
107. Rangaraju, S., and Notterpek, L. (2011). Autophagy aids membrane expansion by neuropathic Schwann cells. Autophagy 7, 238-239. doi:10.4161/auto.7.2.14278
108. Rannou, F., Pennec, J.-P., Morel, J., Gueret, G., Leschiera, R., Droguet, M., et al. (2011). Na v1.4 and Na v1.5 are modulated differently during muscle immobilization and contractile phenotype conversion. J. Appl. Physiol. 111, 495-507. doi:10.1152/japplphysiol.01136.2010
109. Reid, K. F., Doros, G., Clark, D. J., Patten, C., Carabello, R. J., Cloutier, G. J., et al. (2012). Muscle power failure in mobility-limited older adults: preserved single fiber function despite lower whole muscle size, quality and rate of neuromuscular activation. Eur J. Appl. Physiol. 112, 2289-2301. doi:10.1007/s00421-011-2200-0
110. Reid, K. F., Pasha, E., Doros, G., Clark, D. J., Patten, C., Phillips, E. M., et al. (2014). Longitudinal decline of lower extremity muscle power in healthy and mobility-limited older adults: influence of muscle mass, strength, composition, neuromuscular activation and single fiber contractile properties. Eur. J. Appl. Physiol. 114, 29-39. doi:10.1007/s00421-013-2728-2
111. Rocha, M. C., Pousinha, P. A., Correia, A. M., Sebastiao, A. M., and Ribeiro, J. A. (2013). Early changes of neuromuscular transmission in the SOD1(G93A) mice model of ALS start long before motor symptoms onset. PLoS ONE 8:e73846. doi:10.1371/journal.pone.0073846
112. Rosenheimer, J. L., and Smith, D. O. (1985). Differential changes in the end-plate architecture of functionally diverse muscles during aging. J. Neurophysiol. 53, 1567-1581.
113. Rosso, A. L., Studenski, S. A., Chen, W. G., Aizenstein, H. J., Alexander, N. B., Bennett, D. A., et al. (2013). Aging, the central nervous system, and mobility. J Gerontol. A. Biol. Sci. Med. Sci. 68, 1379-1386. doi:10.1093/gerona/glt089
114. Roubenoff, R. (2000). Sarcopenia and its implications for the elderly. Eur. J. Clin. Nutr. 54(Suppl. 3), S40-S47. doi:10.1038/sj.ejcn.1601024
115. Rowan, S. L., Rygiel, K., Purves-Smith, F. M., Solbak, N. M., Turnbull, D. M., and Hepple, R. T. (2012). Denervation causes fiber atrophy and myosin heavy chain co-expression in senescent skeletal muscle. PLoS ONE 7:e29082. doi:10.1371/journal.pone.0029082
116. Rudolf, R., Bogomolovas, J., Strack, S., Choi, K. R., Khan, M. M., Wagner, A., et al. (2013). Regulation of nicotinic acetylcholine receptor turnover by MuRF1 connects muscle activity to endo/lysosomal and atrophy pathways. Age (Dordr) 35, 1663-1674. doi:10.1007/s11357-012-9468-9
117. Russ, D. W., and Lanza, I. R. (2011). The impact of old age on skeletal muscle energetics: supply and demand. Curr. Aging Sci. 4, 234-247. doi:10.2174/1874609811104030234
118. Saheb-Al-Zamani, M., Yan, Y., Farber, S. J., Hunter, D. A., Newton, P., Wood, M. D., et al. (2013). Limited regeneration in long acellular nerve allografts is associated with increased Schwann cell senescence. Exp. Neurol. 247, 165-177. doi:10.1016/j.expneurol.2013.04.011
119. Saini, A., Faulkner, S., Al-Shanti, N., and Stewart, C. (2009). Powerful signals for weak muscles. Ageing Res. Rev. 8, 251-267. doi:10.1016/j.arr.2009.02.001
120. Saini, A., Nasser, A. S., and Stewart, C. E. (2007). Waste management - cytokines, growth factors and cachexia. Cytokine Growth Factor Rev. 17, 475-486. doi:10.1016/j.cytogfr.2006.09.006
121. Sakellariou, G. K., Davis, C. S., Shi, Y., Ivannikov, M. V., Zhang, Y., Vasilaki, A., et al. (2014). Neuron-specific expression of CuZnSOD prevents the loss of muscle mass and function that occurs in homozygous CuZnSOD-knockout mice. FASEB J. 28, 1666-1681. doi:10.1096/fj.13-240390
122. Sakellariou, G. K., Pye, D., Vasilaki, A., Zibrik, L., Palomero, J., Kabayo, T., et al. (2011). Role of superoxide-nitric oxide interactions in the accelerated age-related loss of muscle mass in mice lacking Cu,Zn superoxide dismutase. Aging Cell 10, 749-760. doi:10.1111/j.1474-9726.2011.00709.x
123. Schaefer, A. M., Sanes, J. R., and Lichtman, J. W. (2005). A compensatory subpopulation of motor neurons in a mouse model of amyotrophic lateral sclerosis. J. Comparat. Neurol. 490, 209-219. doi:10.1002/cne.20620
124. Seeburger, J. L., and Springer, J. E. (1993). Experimental rationale for the therapeutic use of neurotrophins in amyotrophic lateral sclerosis. Exp. Neurol. 124, 64-72. doi:10.1006/exnr.1993.1176
125. Shear, T. D., and Martyn, J. A. J. (2009). Physiology and biology of neuromuscular transmission in health and disease. J. Crit. Care 24, 5-10. doi:10.1016/j.jcrc.2008.08.002
126. Smith, D. O., and Rosenheimer, J. L. (1982). Decreased sprouting and degeneration of nerve terminals of active muscles in aged rats. J. Neurophysiol. 48, 100-109.
127. Snow, L. M., McLoon, L. K., and Thompson, L. V. (2005). Adult and developmental myosin heavy chain isoforms in soleus muscle of aging Fischer Brown Norway rat. Anat. Rec. A. Discov. Mol. Cell. Evol. Biol. 286, 866-873. doi:10.1002/ar.a.20218
128. Springer, J. E., Seeburger, J. L., He, J., Gabrea, A., Blankenhorn, E. P., and Bergman, L. W. (1995). cDNA sequence and differential mRNA regulation of two forms of glial cell line-derived neurotrophic factor in Schwann cells and rat skeletal muscle. Exp. Neurol. 131, 47-52. doi:10.1016/0014-4886(95)90006-3
129. Stamatakou, E., and Salinas, P. C. (2013). Postsynaptic assembly: a role for Wnt signaling. Dev. Neurobiol. doi:10.1002/dneu.22138
130. Suetta, C., Frandsen, U., Jensen, L., Jensen, M. M., Jespersen, J. G., Hvid, L. G., et al. (2012). Aging affects the transcriptional regulation of human skeletal muscle disuse atrophy. PLoS ONE 7:e51238. doi:10.1371/journal.pone.0051238
131. Tevald, M. A., Foulis, S. A., Lanza, I. R., and Kent-Braun, J. A. (2010). Lower energy cost of skeletal muscle contractions in older humans. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, R729-R739. doi:10.1152/ajpregu.00713.2009
132. Valdez, G., Tapia, J. C., Kang, H., Clemenson, G. D., Gage, F. H., Lichtman, J. W., et al. (2010). Attenuation of age-related changes in mouse neuromuscular synapses by caloric restriction and exercise. Proc. Natl. Acad. Sci. U S A 107, 14863-14868. doi:10.1073/pnas.1002220107
133. Vergani, L., Di Giulio, A. M., Losa, M., Rossoni, G., Muller, E. E., and Gorio, A. (1998). Systemic administration of insulin-like growth factor decreases motor neuron cell death and promotes muscle reinnervation. J. Neurosci. Res. 54, 840-847. doi:10.1002/(SICI)1097-4547(19981215)54:6<840::AID-JNR12>3.3.CO;2-C
134. Verge, V. M., Gratto, K. A., Karchewski, L. A., and Richardson, P. M. (1996). Neurotrophins and nerve injury in the adult. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 351, doi:10.1098/rstb.1996.0038
135. Wang, Q., Hebert, S. L., Rich, M. M., and Kraner, S. D. (2011). Loss of synaptic vesicles from neuromuscular junctions in aged MRF4-null mice. Neuroreport 22, 185-189. doi:10.1097/WNR.0b013e328344493c
136. Wang, X., Engisch, K. L., Li, Y., Pinter, M. J., Cope, T. C., and Rich, M. M. (2004). Decreased synaptic activity shifts the calcium dependence of release at the mammalian neuromuscular junction in vivo. J. Neurosci. 24, 10687-10692. doi:10.1523/JNEUROSCI.2755-04.2004
137. Wang, Z. M., Zheng, Z., Messi, M. L., and Delbono, O. (2005). Extension and magnitude of denervation in skeletal muscle from ageing mice. J. Physiol. 565(Pt 3), 757-764. doi:10.1113/jphysiol.2005.087601
138. Weis, J., Kaussen, M., Calvo, S., and Buonanno, A. (2000). Denervation induces a rapid nuclear accumulation of MRF4 in mature myofibers. Dev. Dyn. 218, 438-451. doi:10.1002/1097-0177(200007)
139. Wenz, T., Rossi, S. G., Rotundo, R. L., Spiegelman, B. M., and Moraes, C. T. (2009). Increased muscle PGC-1alpha expression protects from sarcopenia and metabolic disease during aging. Proc. Natl. Acad. Sci. U S A. 106, 20405-20410. doi:10.1073/pnas.0911570106
140. Wilson, M. H., and Deschenes, M. R. (2005). The neuromuscular junction: anatomical features and adaptations to various forms of increased, or decreased neuromuscular activity. Int. J. Neurosci. 115, 803-828. doi:10.1080/00207450590882172
141. Witzemann, V., Chevessier, F., Pacifici, P. G., and Yampolsky, P. (2013). The neuromuscular junction: selective remodeling of synaptic regulators at the nerve/muscle interface. Mech. Dev. 130, 402-411. doi:10.1016/j.mod.2012.09.004
142. Yampolsky, P., Pacifici, P. G., and Witzemann, V. (2010). Differential muscle-driven synaptic remodeling in the neuromuscular junction after denervation. Eur. J. Neurosci. 31, 646-658. doi:10.1111/j.1460-9568.2010.07096.x
143. Young, K. A., and Caldwell, J. H. (2005). Modulation of skeletal and cardiac voltage-gated sodium channels by calmodulin. J. Physiol. 565(Pt 2), 349-370. doi:10.1113/jphysiol.2004.081422
144. Yuan, Q., Wu, W., So, K. F., Cheung, A. L., Prevette, D. M., and Oppenheim, R. W. (2000). Effects of neurotrophic factors on motoneuron survival following axonal injury in newborn rats. Neuroreport 11, 2237-2241. doi:10.1097/00001756-200007140-00035
145. Zhang, W., Behringer, R. R., and Olson, E. N. (1995). Inactivation of the myogenic bHLH gene MRF4 results in up-regulation of myogenin and rib anomalies. Genes Dev. 9, 1388-1399. doi:10.1101/gad.9.11.1388
146. Zheng, Z., Wang, Z. M., and Delbono, O. (2002). Insulin-like growth factor-1 increases skeletal muscle dihydropyridine receptor alpha1s transcriptional activity by acting on the camp-response element-binding protein element of the promoter region. J. Biol. Chem. 277, 50535-50542. doi:10.1074/jbc.M210526200