Molecular control of neuromuscular junction development

Journal of Cachexia, Sarcopenia and Muscle

Volumn 3, Issue 1, 2012, Pages 13-23

  Ferraro, Elisabetta ^a   Molinari, Francesca ^a   Berghella, Libera ^a  

^a IRCCS SAN RAFFAELE PISANA   (Italy)

Author keywords

AChR transcription; Agrin MuSK pathway; Congenital myastenic syndromes; Neuromuscular junction; Postsynaptical differentiation; Sarcopenia

Indexed keywords

AGRIN; CHOLINERGIC RECEPTOR; COPPER ZINC SUPEROXIDE DISMUTASE; MYOCYTE ENHANCER FACTOR 2; NEU DIFFERENTIATION FACTOR; PROTEIN KINASE C; PROTEIN MUSK; RAPSYN; SOMATOMEDIN B; SOMATOMEDIN C; STRESS ACTIVATED PROTEIN KINASE; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG;

AUTOPHOSPHORYLATION; CELL MATURATION; DOWN REGULATION; ENZYME ACTIVATION; HUMAN; MUSCLE ACTION POTENTIAL; MUSCLE ATROPHY; MYASTHENIA; NEUROMUSCULAR SYNAPSE; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUALITY OF LIFE; REVIEW; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS; TRANSCRIPTION REGULATION; UPREGULATION;

EID: 84866533624     PISSN: 21905991     EISSN: 21906009     Source Type: Journal    
DOI: 10.1007/s13539-011-0041-7     Document Type: Review

References (115)

1. Engel AG, Ohno K, Shen XM, Sine SM. Congenital myasthenic syndromes: multiple molecular targets at the neuromuscular junction. Ann N Y Acad Sci. 2003;998:138-60.
2. Hartzell HC, Fambrough DM. Acetycholine receptor production and incorporation into membranes of developing muscle fibers. Dev Biol. 1973;30:153-65.
3. Cohen SA, Fischbach GD. Clusters of acetylcholine receptors located at identified nerve-muscle synapses in vitro. Dev Biol. 1977;59:24-38.
4. Kummer TT, Misgeld T, Sanes JR. Assembly of the postsynaptic membrane at the neuromuscular junction: paradigm lost. Curr Opin Neurobiol. 2006;16:74-82.
5. Bevan S, Steinbach JH. The distribution of alpha-bungarotoxin binding sites of mammalian skeletal muscle developing in vivo. J Physiol. 1977;267:195-213.
6. Braithwaite AW, Harris AJ. Neural influence on acetylcholine receptor clusters in embryonic development of skeletal muscles. Nature. 1979;279:549-51.
7. Ziskind-Conhaim L, Bennett JI. The effects of electrical inactivity and denervation on the distribution of acetylcholine receptors in developing rat muscle. Dev Biol. 1982;90:185-97.
8. Yang X, Arber S, William C, Li L, Tanabe Y, Jessell TM, et al. Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron. 2001;30:399-410.
9. Lin W, Burgess RW, Dominguez B, Pfaff SL, Sanes JR, Lee KF. Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature. 2001;410:1057-64.
10. Yang X, Li W, Prescott ED, Burden SJ, Wang JC. DNA topoisomerase II beta and neural development. Science. 2000;287:131-4.
11. Anderson MJ, Cohen MW. Nerve-induced and spontaneous redistribution of acetylcholine receptors on cultured muscle cells. J Physiol. 1977;268:757-73.
12. Frank E, Fischbach GD. Early events in neuromuscular junction formation in vitro: induction of acetylcholine receptor clusters in the postsynaptic membrane and morphology of newly formed synapses. J Cell Biol. 1979;83:143-58.
13. Burden SJ. SnapShot: neuromuscular junction. Cell. 2011;144:826-6.
14. Wu H, Xiong WC, Mei L. To build a synapse: signaling pathways in neuromuscular junction assembly. Development. 2010;137:1017-33.
15. Young SH, Poo MM. Spontaneous release of transmitter from growth cones of embryonic neurones. Nature. 1983;305:634-7.
16. Burden S. Development of the neuromuscular junction in the chick embryo: the number, distribution, and stability of acetylcholine receptors. Dev Biol. 1977;57:317-29.
17. Merlie JP, Sanes JR. Concentration of acetylcholine receptor mRNA in synaptic regions of adult muscle fibres. Nature. 1985;317:66-8.
18. Fontaine B, Sassoon D, Buckingham M, Changeux JP. Detection of the nicotinic acetylcholine receptor alpha-subunit mRNA by in situ hybridization at neuromuscular junctions of 15-day-old chick striated muscles. EMBO J. 1988;7:603-9.
19. Simon AM, Hoppe P, Burden SJ. Spatial restriction of AChR gene expression to subsynaptic nuclei. Development. 1992;114:545-53.
20. McMahan UJ. The agrin hypothesis. Cold Spring Harb Symp Quant Biol. 1990;55:407-18.
21. Ruegg MA, Bixby JL. Agrin orchestrates synaptic differentiation at the vertebrate neuromuscular junction. Trends Neurosci. 1998;21:22-7.
22. Jones G, Meier T, Lichtsteiner M, Witzemann V, Sakmann B, Brenner HR. Induction by agrin of ectopic and functional postsynaptic-like membrane in innervated muscle. Proc Natl Acad Sci U S A. 1997;94:2654-9.
23. Herbst R, Burden SJ. The juxtamembrane region of MuSK has a critical role in agrin-mediated signaling. EMBO J. 2000;19:67-77 Erratum in: EMBO J 2000;19:1167.
24. Gautam M, Noakes PG, Moscoso L, Rupp F, Scheller RH, Merlie JP, et al. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell. 1996;85:525-35.
25. Jennings CG, Dyer SM, Burden SJ. Muscle-specific trkrelated receptor with a kringle domain defines a distinct class of receptor tyrosine kinases. Proc Natl Acad Sci U S A. 1993;90(7):2895-9.
26. Valenzuela DM, Stitt TN, DiStefano PS, Rojas E, Mattsson K, Compton DL, et al. Receptor tyrosine kinase specific for the skeletal muscle lineage: expression in embryonic muscle, at the neuromuscular junction, and after injury. Neuron. 1995;15:573-84.
27. DeChiara TM, Bowen DC, Valenzuela DM, Simmons MV, Poueymirou WT, Thomas S, et al. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell. 1996;85:501-12.
28. Mittaud P, Camilleri AA, Willmann R, Erb-Vögtli S, Burden SJ, Fuhrer C. A single pulse of agrin triggers a pathway that acts to cluster acetylcholine receptors. Mol Cell Biol. 2004;24:7841-54.
29. Kim N, Burden SJ. MuSK controls where motor axons grow and form synapses. Nature Neurosci. 2008;11:19-27.
30. Thang H, Veldman MB, Goldman D. Characterization of a muscle-specific enhancer in human MuSK promoter reveals the essential role of myogenin in controlling activity-dependent gene regulation. Proc Natl Acad Sci U S A. 2006;103:16977-82.
31. GlassDJ, Bowen DC, Stitt TN, Radziejewski C, Bruno J, Ryan TE, et al. Agrin acts via a MuSK receptor complex. Cell. 1996;85:513-23.
32. Glass DJ, Apel ED, Shah S, Bowen DC, DeChiara TM, Stitt TN, et al. Kinase domain of the muscle-specific receptor tyrosine kinase (MuSK) is sufficient for phosphorylation but not clustering of acetylcholine receptors: required role for the MuSK ectodomain? Proc Natl Acad Sci U S A. 1997;94:8848-53.
33. Weatherbee SD, Anderson KV, Niswander LA. LDL-receptorrelated protein 4 is crucial for formation of the neuromuscular junction. Development. 2006;133:4993-5000.
34. Kim N, Stiegler AL, Cameron TO, Hallock PT, Gomez AM, Huang JH, et al. Lrp4 is a receptor for agrin and forms a complex with MuSK. Cell. 2008;135:334-42.
35. Zhang B, Luo S, Wang Q, Suzuki T, Xiong WC, Mei L. LRP4 serves as a coreceptor of agrin. Neuron. 2008;60:285-97.
36. Kummer TT, Misged T, Sanes JR. Assembly of the postsynaptic membrane at the neuromuscular junction: paradigm lost. Curr Opin Neurobiol. 2006;16:74-82.
37. Okada K, Inoue A, Okada M, Murata Y, Kakuta S, Jigami T, et al. The muscle protein Dok-7 is essential for neuromuscular synaptogenesis. Science. 2006;312:1802-5.
38. Inoue A, Setoguchi K, Matsubara Y, Okada K, Sato N, Iwakura Y, et al. Dok-7 activates the muscle receptor kinase MuSK and shapes synapse formation. Sci Signal. 2009;2(59):ra7.
39. Bergamin E, Hallock PT, Burden SJ, Hubbard SR. The cytoplasmic adaptor protein Dok7 activates the receptor tyrosine kinase MuSK via dimerization. Mol Cell. 2010;39:100-9.
40. Hallock PT, Xu CF, Park TJ, Neubert TA, Curran T, Burden SJ. Dok-7 regulates neuromuscular synapse formation by recruiting Crk and Crk-L. Genes Dev. 2010;24:2451-61.
41. Burden SJ, DePalma RL, Hume RI, Akaaboune M. Identification of nicotinic acetylcholine receptor recycling and its role in maintaining receptor density at the neuromuscular junction in vivo. Cell. 1983;35:687-92.
42. GautamM, Mudd J, Copeland NG, Gilbert DJ, Jenkins NA, Merlie JP. Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature. 1995;377:232-6.
43. Strochlic L, Cartaud A, Cartaud J. The synaptic muscle-specific kinase (MuSK) complex: new partners, new functions. Bioassays. 2005;27:1129-35.
44. Falls DL. Neuregulins and the neuromuscular system: 10 years of answers and questions. J Neurocytol. 2003;32:619-47.
45. Meyer D, Birchmeier C. Multiple essential functions of neuregulin in development. Nature. 1995;378:386-90. Erratum in: Nature 1995;378:753.
46. Sandrock Jr AW, Dryer SE, Rosen KM, Gozani SN, Kramer R, Theill LE, et al. Maintenance of acetylcholine receptor number by neuregulins at the neuromuscular junction in vivo. Science. 1997;276:599-603.
47. Escher P, Lacazette E, Courtet M, Blindenbacher A, Landmann L, Bezakova G, et al. Synapses form in skeletal muscles lacking neuregulin receptors. Science. 2005;308:1920-3.
48. Jaworski A, Burden SJ. Neuromuscular synapse formation in mice lacking motor neuron-and skeletal muscle-derived neuregulin-1. J Neurosci. 2006;26:655-61.
49. Rimer M. Neuregulins at the neuromuscular synapse: past, present, and future. J Neurosci Res. 2007;85:1827-33.
50. Tansey MG, Chu GC, Merlie JP. ARIA/HRG regulates AChR epsilon subunit gene expression at the neuromuscular synapse via activation of phosphatidylinositol 3-kinase and Ras/MAPK pathway. J Cell Biol. 1996;134:465-76.
51. Altiok N, Altiok S, Changeux JP. Heregulin-stimulated acetylcholine receptor gene expression in muscle: requirement for MAP kinase and evidence for a parallel inhibitory pathway independent of electrical activity. EMBO J. 1997;16:717-25.
52. Si J, Luo Z, Mei L. Induction of acetylcholine receptor gene expression by ARIA requires activation of mitogen-activated protein kinase. J Biol Chem. 1996;271:19752-9.
53. Si J, WangQ, Mei L. Essential roles of c-JUNand c-JUNN-terminal kinase (JNK) in neuregulin-increased expression of the acetylcholine receptor epsilon-subunit. J Neurosci. 1999;19:8498-508.
54. LaMarco K, Thompson CC, Byers BP, Walton EM, McKnight SL. Identification of Ets-and notch-related subunits in GA binding protein. Science. 1991;253:789-92.
55. Thompson CC, Brown TA, McKnight SL. Convergence of Etsand notch-related structural motifs in a heteromeric DNA binding complex. Science. 1991;253:762-8.
56. Schaeffer L, Duclert N, Huchet-Dymanus M, Changeux JP. Implication of a multisubunit Ets-related transcription factor in synaptic expression of the nicotinic acetylcholine receptor. EMBO J. 1998;17:3078-90.
57. Fromm L, Burden SJ. Transcriptional pathways for synapsespecific, neuregulin-induced and electrical activity-dependent transcription. J Physiol Paris. 1998;92:173-6.
58. Sapru MK, Florance SK, Kirk C, Goldman D. Identification of a neuregulin and protein-tyrosine phosphatase response element in the nicotinic acetylcholine receptor epsilon subunit gene: regulatory role of an Rts transcription factor. Proc Natl Acad Sci U S A. 1998;95:1289-94.
59. Briguet A, Ruegg MA. The Ets transcription factor GABP is required for postsynaptic differentiation in vivo. J Neurosci. 2000;20:5989-96.
60. Lacazzette E, Le Calvez S, Gajendran N, Brenner HR. A novel pathway for MuSK to induce genes in neuromuscular synapse formation. J Cell Biol. 2003;161:727-36.
61. Strochlic L, Cartaud A, Mejat A, Graihe R, Shaeffer L, Changeux JP, et al. 14-3-3 gamma associates with muscle specific kinase and regulates synaptic gene transcription at vertebrate neuromuscular synapse. Proc Natl Acad Sci. 2004;101:18189-94.
62. Salpeter MM, Cooper DL, Levitt-Gilmour T. Degradation rates of acetylcholine receptors can be modified in the postjunctional plasma membrane of the vertebrate neuromuscular junction. J Cell Biol. 1986;103(4):1399-403.
63. Fu AK, Ip FC, Fu WY, Cheung J, Wang JH, Yung WH, et al. Aberrant motor axon projection, acetylcholine receptor clustering, and neurotransmission in cyclin-dependent kinase 5 null mice. Proc Natl Acad Sci U S A. 2005;102:15224-9.
64. Lin W, Dominguez B, Yang J, Aryal P, Brandon EP, Gage FH, et al. Neurotransmitter acetylcholine negatively regulates neuromuscular synapse formation by a Cdk-5-dependent mechanism. Neuron. 2005;46:569-79.
65. Tang H, Sun Z, Goldman D. CaM kinase II-dependent suppression of nicotinic acetylcholine receptor delta-subunit promoter activity. J Biol Chem. 2001;276:26057-65.
66. Misgeld T, Burgess RW, Lewis RM, Cunningham JM, Lichtman JW, Sanes JR. Roles of neurotransmitter in synapse formation: development of neuromuscular junctions lacking choline acetyltransferase. Neuron. 2002;36:635-48.
67. Brandon EP, Lin W, D'Amour KA, Pizzo DP, Dominguez B, Sugiura Y, et al. Aberrant patterning of neuromuscular synapses in choline acetyltransferase-deficient mice. J Neurosci. 2003;23:539-49.
68. Laufer R, Changeux JP. Calcitonin gene-related peptide and cyclic AMP stimulate phosphoinositide turnover in skeletal muscle cells. Interaction between two second messenger systems. J Biol Chem. 1989;264:2683-9.
69. Sanes JR, Lichtman JW. Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci. 2001;11:791-805.
70. Eftimie R, Brenner HR, Buonanno A. Myogenin and MyoD join a family of skeletal muscle genes regulated by electrical activity. Proc Natl Acad Sci U S A. 1991;88:1349-53.
71. Gundersen K, Rabben I, Klocke BJ, Merlie JP. Overexpression of myogenin in muscles of transgenic mice: interaction with Id-1, negative crossregulation of myogenic factors, and induction of extrasynaptic acetylcholine receptor expression. Mol Cell Biol. 1995;15:7127-34.
72. Li L, Zhou J, James G, Heller-Harrison R, Czech MP, Olson EN. FGF inactivates myogenic helix-loop-helix proteins through phosphorylation of a conserved protein kinase C site in their DNA-binding domains. Cell. 1992;71:1181-94.
73. Mendelzon D, Changeux JP, Nghiêm HO. Phosphorylation of myogenin in chick myotubes: regulation by electrical activity and by protein kinase C. Implications for acetylcholine receptor gene expression. Biochemistry. 1994;33:2568-75.
74. Macpherson P, Kostrominova T, Tang H, Goldman D. Protein kinase C and calcium/calmodulin-activated protein kinase II (CaMK II) suppress nicotinic acetylcholine receptor gene expression in mammalian muscle. A specific role for CaMK II in activitydependent gene expression. J Biol Chem. 2002;277:15638-46.
75. Méjat A, Ramond F, Bassel-Duby R, Khochbin S, Olson EN, Schaeffer L. Histone deacetylase 9 couples neuronal activity to muscle chromatin acetylation and gene expression. Nat Neurosci. 2005;8:313-21.
76. Tang H, Goldman D. Activity-dependent gene regulation in skeletal muscle is mediated by a histone deacetylase (HDAC)-Dach2-myogenin signal transduction cascade. Proc Natl Acad Sci U S A. 2006;103:16977-82.
77. Cohen TJ, Waddell DS, Barrientos T, Lu Z, Feng G, Cox GA, et al. The histone deacetylase HDAC4 connects neural activity to muscle transcriptional reprogramming. J Biol Chem. 2007;282:33752-9.
78. Tang H, Macpherson P, Marvin M, Meadows E, Klein WH, Yang XJ, et al. A histone deacetylase 4/myogenin positive feedback loop coordinates denervation-dependent gene induction and suppression. Mol Biol Cell. 2009;20:1120-31.
79. Berghella L, De Angelis L, De Buysscher T, Mortazavi A, Biressi S, Forcales SV, et al. A highly conserved molecular switch binds MSY-3 to regulate myogenin repression in postnatal muscle. Genes Dev. 2008;22:2125-38.
80. Vincent A, Newland C, Croxen R, Beeson D. Genes at the junction-candidates for congenital myasthenic syndromes. Trends Neurosci. 1997;20:15-22.
81. Engel AG, Sine SM. Current understanding of congenital myasthenic syndromes. Curr Opin Pharmacol. 2005;5:308-21.
82. Ohno K, Quiram PA, Milone M, Wang HL, Harper MC, Pruitt 2nd JN, et al. Congenital myasthenic syndromes due to heteroallelic nonsense/missense mutations in the acetylcholine receptor epsilon subunit gene: identification and functional characterization of six new mutations. Hum Mol Genet. 1997;6:753-66.
83. Ohno K, Engel AG, Shen XM, Selcen D, Brengman J, Harper CM, et al. Rapsyn mutations in humans cause end-plate acetylcholine-receptor deficiency and myasthenic syndrome. Am J Hum Genet. 2002;70:875-85.
84. Nogajski JH, Kiernan MC, Ouvrier RA, Andrews PI. Congenital myasthenic syndromes. J Clin Neurosci. 2009;16:1-11.
85. Beeson D, Higuchi O, Palace J, Cossins J, Spearman H, Maxwell S, et al. Dok-7 mutations underlie a neuromuscular junction synaptopathy. Science. 2006;29(313):1975-8.
86. Selcen D, Milone M, Shen XM, Harper CM, Stans AA, Wieben ED, et al. Dok-7 myasthenia: phenotypic and molecular genetic studies in 16 patients. Ann Neurol. 2008;64:71-87.
87. Yamanashi Y, Higuch O, Beeson D. Dok-7/MuSK signaling and a congenital myasthenic syndrome. Acta Myol. 2008;27:25-9.
88. Duclert A, Savatier N, Schaeffer L, Changeux JP. Identification of an element crucial for the sub-synaptic expression of the acetylcholine receptor epsilon-subunit gene. J Biol Chem. 1996;19(271):17433-8.
89. Ohno K, Anlar B, Engel AG. Congenital myasthenic syndrome caused by a mutation in the Ets-binding site of the promoter region of the acetylcholine receptor epsilon subunit gene. Neuromuscul Disord. 1999;9:131-5.
90. Nichols P, Croxen R, Vincent A, Rutter R, Hutchinson M, Newsom-Davis J, et al. Mutation of the acetylcholine receptor epsilon-subunit promoter in congenital myasthenic syndrome. Ann Neurol. 1999;45:439-43.
91. Conti-Fine BM, Milani M, Kaminski HJ. Myasthenia gravis: past, present, and future. J Clin Invest. 2006;116:2843-54.
92. Vincent A, Lang B, Kleopa KA. Autoimmune channelopathies and related neurological disorders. Neuron. 2006;5 (52):123-38.
93. Fambrough DM, Drachman DB, Satyamurti S. Neuromuscular junction in myasthenia gravis: decreased acetylcholine receptors. Science. 1973;182:293-5.
94. Hoch W, McConville J, Helms S, Newsom-Davis J, Melms A, Vincent A. Auto-antibodies to the receptor tyrosine kinase MuSK in patients with myasthenia gravis without acetylcholine receptor antibodies. Nat Med. 2001;7:365-8.
95. Shiraishi H, Motomura M, Yoshimura T, Fukudome T, Fukuda T, Nakao Y, et al. Acetylcholine receptors loss and postsynaptic damage inMuSK antibody-positive myasthenia gravis. Ann Neurol. 2005;57:289-93.
96. Higuchi O, Hamuro J, Motomura M, Yamanashi Y. Autoantibodies to low-density lipoprotein receptor-related protein 4 in myasthenia gravis. Ann Neurol. 2011;69:418-22.
97. Janssen DS, Shepard PT, Katzmarzyk R, Roubenoff. The healthcare costs of sarcopenia in the United States. J Am Geriatr Soc. 2004;52:80-5.
98. Balice-Gordon RJ. Age-related changes in neuromuscular innervations. Muscle Nerve. 1997;5:S83-7.
99. Gutmann E, Hanzlikova V. Basic mechanisms of aging in the neuromuscular system. Mech Ageing Dev. 1973;1:327-49.
100. Ceballos D, Cuadras J, Verdu E, Navarro X. Morphometric and ultrastructural changes with ageing in mouse peripheral nerve. J Anat. 1999;195:563-76.
101. Gonzalez M, Ruggiero FP, Chang Q, Shi YJ, Rich MM, Kraner S, et al. Disruption of Trkb-mediated signaling induces disassembly of postsynaptic receptor clusters at neuromuscular junctions. Neuron. 1999;24:567-83.
102. Belluardo N, Westerblad H, Mudo G, Casabona A, Bruton J, Caniglia GO, et al. Neuromuscular junction disassembly and muscle fatigue in mice lacking neurotrophin-4. Mol Cell Neurosci. 2001;18:56-7.
103. Payne AM, Zheng Z, Messi ML, Milligan CE, Gonzalez E, Delbono O. Motor neurone targeting of IGF-1 prevents specific force decline in ageing mouse muscle. J Physiol. 2006;570:283-94.
104. Kim JH, Kwak HB, Leeuwenburgh C, Lawler JM. Lifelong exercise and mild (8%) caloric restriction attenuate age-induced alterations in plantaris muscle morphology, oxidative stress and IGF-1 in the Fischer-344 rat. Exp Gerontol. 2008;43:317-29.
105. Deschenes MR, Roby MA, Eason MK, Harris MB. Remodeling of the neuromuscular junction precedes sarcopenia related alterations in myofibers. Exp Gerontol. 2010;45:389-93.
106. Vandervoort AA. Aging of the human neuromuscular system. Muscle Nerve. 2002;25:17-25.
107. Hiona A, Leeuwenburgh C. The role of mitochondrial DNA mutations in aging and sarcopenia: implications for the mitochondrial vicious cycle theory of aging. Exp Gerontol. 2008;43:24-33.
108. Zhou J, Yi J, Fu R, Liu, Siddique ET, Rios E, et al. Hyperactive intracellular calcium signaling associated with localized mitochondrial defects in skeletal muscle of an animal model of amyotrophic lateral sclerosis. J Biol Chem. 2010;285:705-12.
109. Jang YC, Lustgarten MS, Liu Y, Muller FL, Bhattacharya A, Liang H, et al. Increased superoxide in vivo accelerates age-associated muscle atrophy through mitochondrial dysfunction and neuromuscular junction degeneration. FASEB J. 2010;24:1376-90.
110. Payne AM, Zheng Z, Gonzalez E, Wang ZM, Messi ML, Delbono O. External Ca(2+)-dependent excitation-contraction coupling in a population of ageing mouse skeletal muscle fibres. J Physiol. 2004;560:137-55.
111. Jang YC, Van Remmen H. Age-associated alterations of the neuromuscular junction. Exp Gerontol. 2011;46:193-8.
112. Muller FL, Song W, Liu Y, Chaudhuri A, Pieke-Dahl S, Strong R, et al. Absence of CuZn superoxide dismutase leads to elevated oxidative stress and acceleration of age-dependent skeletal muscle atrophy. Free Radic Biol Med. 2006;40:1993-2004.
113. Rangaraju S, Hankins D, Madorsky I, Madorsky E, Lee WH, Carter CS, et al. Molecular architecture of myelinated peripheral nerves is supported by calorie restriction with aging. Aging Cell. 2009;8:178-91.
114. Opalach K, Rangaraju S, Madorsky I, Leeuwenburgh C, Notterpek L. Lifelong calorie restriction alleviates age-related oxidative damage in peripheral nerves. Rejuvenation Res. 2010;13:65-74.
115. von Haehling S, Morley JE, Coats AJS, Anker SD. Ethical guidelines for authorship and publishing in the Journal of Cachexia, Sarcopenia and Muscle. J Cachexia Sarcopenia Muscle. 2010;1:7-8.