Just in time and place: NOS/NO system assembly in neuromuscular junction formation

Microscopy Research and Technique

Volumn 55, Issue 3, 2001, Pages 171-180

  Blottner, Dieter ^a   Lück, Gabriele ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Acetylcholine receptor; Agrin; Postsynaptic complex; Redox related signaling; Skeletal muscle; Synapse development

Indexed keywords

AMINO ACIDS; MEMBRANES; PROTEINS; SIGNAL TRANSDUCTION; SIGNALING;

ACETYLCHOLINE RECEPTOR; AGRIN; MEMBRANE COMPONENTS; NEUROMUSCULAR JUNCTIONS; NITRIC OXIDE SIGNALING; POSTSYNAPTIC COMPLEX; REDOX-RELATED SIGNALING; SKELETAL MUSCLE; SYNAPSE DEVELOPMENT; SYNTHASES;

NITRIC OXIDE;

AGRIN; ARGININE; CHOLINERGIC RECEPTOR; DYSTROPHIN; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER; NICOTINE; NICOTINIC RECEPTOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; POSTSYNAPTIC DENSITY PROTEIN 95; POTASSIUM CHANNEL; RAPSYN; SODIUM CHANNEL; UNCLASSIFIED DRUG; UTROPHIN;

ARTICLE; MEMBRANE POTENTIAL; MOLECULAR MODEL; MYOTUBE; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; OXIDATION REDUCTION REACTION; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SECOND MESSENGER; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SYNAPSE;

EID: 0035499237     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/jemt.1168     Document Type: Article

References (152)

1. Abdelmoity A, Padre RC, Kimberley E, Burzynski E, Stull JT, Lau KS. 2000. Neuronal nitric oxide synthase localizes through multiple structural motifs to the sarcolemma in mouse myotubes. FEBS Lett 482:65-70.
2. Adams ME, Kramarcy N, Krall SP, Rossi SG, Rotundo RL, Sealock R, Froehner SC. 2000. Absence of alpha-syntrophin leads to structurally aberrant neuromuscular synapses deficient in utrophin. J Cell Biol 150:1385-1398.
3. Agnati LF, Zoli M, Stromberg I, Fuxe K. 1995. Intercellular communication in the brain: wiring versus volume transmission. Neuroscience 69:711-726.
4. Ahn AH, Kunkel LM. 1993. The structural and functional diversity of dystrophin. Nature Genetics 3:283-291.
5. Aonuma H, Nagayama T, Takahata M. 2000. Modulatory effects of nitric oxide on synaptic depression in the crayfish neuromuscular system. J Exp Biol 23:3595-3602.
6. Apel ED, Roberds SL, Campbell KP, Merlie JP. 1995. Rapsyn may function as a link between the acetylcholine receptor and the agrin-binding dystrophin-associated glycoprotein complex. Neuron 15: 115-126.
7. Apel ED, Glass DJ, Moscoso LM, Yancopoulos GD, Sanes JR. 1997. Rapsyn is required for MuSK signaling and recruits synaptic components to a MuSK-containing scaffold. Neuron 18:623-635.
8. Arnold DB, Clapham DE. 1999. Molecular determinants for subcellular localization of PSD-95 with an interacting K+ channel. Neuron 23:149-157.
9. Askanas V, Engel WK, Alvarez RB. 1998. Fourteen newly recognized proteins at the human neuromuscular junctions, and their nonjunctional accumulation in inclusion-body myositis. Ann NY Acad Sci 841:28-56.
10. Blake DJ, Tinsley JM, Davies KE, Knight AE, Winder SJ, Kendrick-Jones J. 1995. Coiled-coil regions in the carboxy-terminal domains of dystrophin and related proteins: potentials for protein-protein interactions. Trends Biochem Sci 20:133-135.
11. Blake DJ, Nawrotzki R, Loh NY, Gorecki DC, Davies KE. 1998. β-dystrobrevin, a member of the dystrophin-related protein family. Proc Natl Acad Sci USA 95:241-246.
12. Blottner D, Lück G. 1998. Nitric oxide synthase (NOS) in mouse skeletal muscle development and differentiated myoblasts. Cell Tissue Res 292:293-302.
13. Blottner D, Grozdanovic Z, Gossrau R. 1995. Histochemistry of nitric oxide synthase in the nervous system. Histochem J 27:785-811.
14. Blottner D, Gerlach EM, Rindermann C, Lück G. 2000. Neuronal regulation of NOS-1 in motoneuron/myotube co-cultures. Soc Neurosci (Abstr) 26:1090.
15. Bowen DC, Park JS, Bodine S, Stark JL, Valenzuela DM, Stitt TN, Yancoupoulos GD, Lindsay RM, Glass DJ, DiStefano PS. 1998. Localization and regulation of MuSK at the neuromuscular junction. Dev Biol 199:309-319.
16. Bredt DS. 1996. Targeting nitric oxide to its targets. Proc Soc Exp Biol Med 211:41-48.
17. Bredt DS, Snyder SH. 1989. Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc Natl Acad Sci USA 86:9030-9033.
18. Brenman JE, Bredt DS. 1997. Synaptic signaling by nitric oxide. Curr Opin Neurobiol 7:374-378.
19. Brenman JE, Chao DS, Gee SH, McGee AW, Craven SE, Santilano DR, Wu Z, Huang F, Xia H, Peters MF, Froehner SC, Bredt DS. 1996. Interaction of nitric oxide synthase with postsynaptic density protein PSD-95 and α1-syntrophin mediated by PDZ domains. Cell 84:757-767.
20. Brenman JE, Xia H, Chao DS, Black SM, Bredt DS. 1997. Regulation of neuronal nitric oxide synthase through alternative transcripts. Dev Neurosci 19:224-231.
21. Broillet MC. 1999. S-nitrosylation of proteins. Cell Mol Life Sci 55: 1036-1042.
22. Burden SJ. 1998. The formation of the neuromuscular synapses. Genes Dev 12:133-148.
23. Butler AR, Flitney FW, Williams DLH. 1995. NO, nitrosonium ions, nitroxide ions, nitrosothiols and iron-nitrosyls in biology: a chemist's perspective. Trends Pharmacol 16:18-22.
24. Chao DS, Gorospe JR, Brenman JE, Rafael JA, Peters MF, Froehner SC, Hoffman EP, Chamberlain JS, Bredt DS. 1996. Selective loss of sarcolemmal nitric oxide synthase in Becker muscular dystrophy. J Exp Med 184:609-618.
25. Chao DS, Silvagno F, Xia H, Cornwell TL, Lincoln TM, Bredt DS. 1997. Nitric oxide synthase and cyclic GMP-dependent protein kinase concentrated at the neuromuscular endplate. Neuroscience 76:665-672.
26. Chaubourt E, Fossier P, Baux G, Leprince C, Israel M, De La Porte S. 1999. Nitric oxide and 1-arginine cause an accumulation of utrophin at the sarcolemma: a possible compensation for dystrophin loss in Duchenne muscular dystrophy. Neurobiol Dis 6:499-507.
27. Chaubourt E, Voisin V, Fossier P, Baux G, Israel M, de La Porte S. 2000. The NO way to increase muscular utrophin expression? CR Acad Sci III, Paris 323:735-740.
28. Christopherson KS, Hillier BJ, Lim WA, Bredt DS. 1999. PSD-95 assembles a ternary complex with the N-methyl-D-aspartic acid receptor and a bivalent neuronal NO synthase PDZ domain. J Biol Chem 274:27467-27473.
29. Cho KO, Hunt CA, Kennedy MB. 1992. The rat brain postsynaptic density fraction contains a homologue of the Drosophila discs-large tumor suppressor protein. Neuron 9:929-942.
30. Choi YB, Tenneti L, Le DA, Ortiz J, Bai G, Chen HS, Lipton SA. 2000. Molecular basis of NMDA receptor-coupled ion channel modulation by S-nitrosylation. Nat Neurosci 3:15-21.
31. Colledge M, Froehner SC. 1998. Signals mediating ion channel clustering at the neuromuscular junction. Curr Opin Neurobiol 8:357-363.
32. Connor EA, Smith MA. 1994. Retrograde signaling in the formation and maintenance of the neuromuscular junction. J Neurobiol 25: 722-739.
33. Côtè PD, Moukhles H, Lindenbaum M, Carbonetto S. 1999. Chimaeric mice deficient in dystroglycans develop muscular dystrophy and have disrupted myoneuronal synapses. Nat Genet 3:338-342.
34. Couet J, Li S, Okamoto T, Ikezu T, Lisanti MP. 1997. Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. J Biol Chem 272:6525-6533.
35. Craven SE, Bredt DS. 1998. PDZ proteins organize synaptic signaling pathways. Cell 93:495-498.
36. Craven SE, Bredt DS. 2000. Synaptic targeting of the postsynaptic density protein PSD-95 mediated by a tyrosine-based trafficking signal. J Biol Chem 275:20045-20051.
37. Crosbie RH, Heighway J, Venzke DP, Lee JC, Campbell KP. 1997. Sarcospan: the 25kDa transmembrane component of the dystrophin-glycoprotein complex. J Biol Chem 272:31221-31224.
38. Crosbie RH, Straub V, Yun HY, Lee JC, Rafael JA, Chamberlain JS, Dawson VL, Dawson TM, Campbell KP. 1998. mdx muscle pathology is independent of nNOS perturbation. Hum Mol Genet 7:823-829.
39. Crosbie RH, Lebakken CS, Holt KH, Venzke DP, Straub V, Lee JC, Grady RM, Chamberlain JS, Sanes JR, Campbell KP. 1999. Membrane targeting and stabilization of sarcoglycan is mediated by the sarcoglycan subcomplex. J Cell Biol 145:153-165.
40. Curtis J, Finkbeiner S. 1999. Sending signals from the synapse to the nucleus: possible roles for CaMK, Ras/ERK, and SAPK pathways in the regulation of synaptic plasticity and neuronal growth. J Neurosci Res 58:88-95.
41. Dawson TM, Snyder SH. 1994. Gases as biological messengers: nitric oxide and carbon monoxide in the brain. J Neurosci 14:5147-5159.
42. DeChiara TM, Bowen DC, Valenzuela DM, Simmons MV, Poueymirou WT, Thomas WT, Kinetz E, Crompton DL, Rojas E, Park JS, Smith C, DiStefano PS, Glass DJ, Burden SJ, Yancopoulos GD. 1996. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85:501-512.
43. Decrouy A, Renaud JM, Lunde JA, Dickson G, Jasmin BJ. 1998. Mini-and full length dystrophin gene transfer induces the recovery of nitric oxide synthase at the sarcolemma of mdx4cv skeletal muscle fibers. Gene Ther 5:59-64.
44. Denninger JW, Marletta MA. 1999. Guanylate cyclase and the NO/ cGMP signaling pathway. Biochim Biophys Acta 1411:334-350.
45. Descarries LM, Cai S, Robitaille R, Josephson EM, Morest DK 1998. Localization and characterization of nitric oxide synthase at the frog neuromuscular junction. J Neurocytol 27:829-840.
46. Di Stasi AM, Mallozzi C, Macchia G, Petrucci TC, Minetti M. 1999. Peroxynitrite induces tyrosine nitration and modulates tyrosine phosphorylation of synaptic proteins. J Neurochem 73:727-735.
47. El-Husseini AE, Schnell E, Chetkovitch DM, Nicoll RA, Bredt DS. 2000a. PSD-95 involvement in maturation of excitatory synapses. Science 290:1364-1368.
48. El-Husseini AE, Topinka JR, Lehrer-Graiwer JE, Firestein BL, Craven SE, Aoki C, Bredt DS. 2000b. Ion channel clustering by membrane-associated guanylate kinases. Differential regulation by N-terminal lipid and metal binding motifs. J Biol Chem 275:23904-23910.
49. Engel AG. 1994. The neuromuscular junction. In: Engel AG, Franzini-Armstrong, editors. Myology: basic and clinical, Vol I. New York: McGraw-Hill, p 261-302.
50. Ervasti JM, Campbell KP. 1991. Membrane organization of the dystrophin-glycoprotein complex. Cell 66:1121-1131.
51. Eu JP, Sun J, Xu L, Stamler JS, Meissner G. 2000. The skeletal muscle calcium release channel: couples O2 sensor and NO signaling functions. Cell 102:499-509.
52. Fang M, Jaffrey SR, Sawa A, Ye K, Luo X, Snyder SH. 2000. Dexras1: a G-protein specifically coupled to neuronal nitric oxide synthase via CAPON. Neuron 28:183-193.
53. Fanning AS, Anderson JM. 1999. Protein modules as organizers of membrane structure. Curr Opin Cell Biol 11:432-439.
54. Feener CA, Koenig M, Kunkel LM. 1989. Alternative splicing of human dystrophin mRNA generates isoforms at the carboxy terminus. Nature 338:509-511.
55. Firestein BL, Craven S, Bredt DS. 2000. Postsynaptic targeting of MAGUKs mediated by distinct N-terminal domains. NeuroReport 11:1-6.
56. Fischbach GD, Rosen KM. 1997. ARIA: a neuromuscular junction neuregulin. Annu Rev Neurosci 20:429-458.
57. Flucher BE, Daniels MP. 1989. Distribution of Na+ channels and ankyrin in neuromuscular junctions is complementary to that of acetylcholine receptors and the 43 kd protein. Neuron 3:163-175.
58. Förstermann U, Closs EI, Pollock JS, Nakane M, Schwarz P, Gath I, Kleinert H. 1994. Nitric oxide synthase isozymes. Characterization, purification, molecular cloning, and functions. Hypertension 23: 1121-1131.
59. Froehner SC, Murnane AA, Tobler M, Peng HB, Sealock R. 1987. A postsynaptic Mr 58,000 (58K) protein concentrated at acetylcholine receptor-rich sites in Torpedo electroplaques and skeletal muscle. J Cell Biol 104:1633-1646.
60. Froehner SC, Luetje CW, Scotland PB, Patrick J. 1990. The postsynaptic 43K protein clusters muscle nicotinic acetylcholine receptors in Xenopus oocytes. Neuron 5:403-410.
61. Froehner SC, Adams ME, Peters MF, Gee SH. 1997. Syntrophins: Modular adaptor proteins at the neuromuscular junction. Soc Gen Physiol Ser 52:197-207.
62. Fuhrer C, Gautam M, Sugiyama JE, Hall ZW. 1999. Roles of rapsyn and agrin in interaction of postsynaptic proteins with acetylcholine receptors. J Neurosci 19:6405-6416.
63. Garcia RA, Vasudevan K, Buonanno A. 2000. The neuregulin receptor ErbB-4 interacts with PDZ-containing proteins at neuronal synapses. Proc Natl Acad Sci USA 97:3596-3601.
64. Gath I, Closs EI, Godtel-Armbrust U, Schmitt S, Nakane M, Wessler I, Forstermann U. 1996. Inducible NO synthase II and neuronal NO synthase I are constitutively expressed in different structures of guinea pig skeletal muscle: implications for contractile function. FASEB J 10:1614-1620.
65. Gautam M, Noakes PG, Moscoso L, Rupp F, Scheller RH, Merlie P, Sanes JR. 1996. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85:525-535.
66. Gee SH, Madhavan R, Levinson SR, Caldwell JH, Sealock R, Froehner SC. 1998. Interaction of muscle and brain sodium channels with multiple members of the syntrophin family of dystrophin-associated proteins. J Neurosci 18:128-137.
67. Glass DJ, Bowen DC, Stitt TN, Radziejewski C, Bruno J, Ryan TE, Gies DR, Shah S, Mattsson K, Burden SJ, DiStefano PS, Valenzuela DM, DeChiara TM, Yancopoulos GD. 1996. Agrin acts via a MuSK receptor complex. Cell 85:513-523.
68. Gomperts SN. 1996. Clustering membrane proteins; It's all coming together with the PSD-95/SAP-90 protein family. Cell 84:659-662.
69. Grady RM, Teng H, Nichol MC, Cunningham JC, Wilkinson RS, Sanes JR. 1997. Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell 90:729-738.
70. Grady RM, Grange RW, Lau KS, Maimone MM, Nichol MC, Stull JT, Sanes JR. 1999. Role for alpha-dystrobrevin in the pathogenesis of dystrophin-dependent muscular dystrophies. Nat Cell Biol 1:215-220.
71. Grady RM, Zhou H, Cunningham JM, Sanes JR. 2000. Maturation and maintenance of the neuromuscular synapse: genetic evidence for roles of the dystrophin-glycoprotein complex. Neuron 25:279-293.
72. Gramolini AO, Jasmin BJ. 1998. Molecular mechanisms and putative signaling events controlling utrophin expression in mammalian skeletal muscle fibres. Neuromusc Disord 8:351-361.
73. Grinnell AD. 1995. Dynamics of nerve muscle interaction in developing and mature neuromuscular junctions. Physiol Rev 75:789-824.
74. Grozdanovic Z, Gossrau R. 1998. Co-localization of nitric oxide synthase I (NOS I) and NMDA-receptor subunit 1 (NMDAR-1) at the neuromuscular junction in rat and mouse skeletal muscle. Cell Tissue Res 291:57-63.
75. Grozdanovic Z, Nakos G, Dahrmann G, Mayer B, Gossrau R. 1995. Species-independent expression of nitric oxide synthase in the sarcolemma region of visceral and somatic striated muscle fibers. Cell Tissue Res 281:493-499.
76. Hall ZW, Sanes JR. 1993. Synaptic structure and development: the neuromuscular junction. Cell 72:99-121.
77. Hasegawa M, Cuenda A, Spillantini MG, Thomas GM, Buee-Scherrer V, Cohen P, Goedert M. 1999. Stress-activated protein kinase-3 interacts with the PDZ domain of alpha1-syntrophin. A mechanism for specific substrate recognition. J Biol Chem 274:12626-12631.
78. Hillier BJ, Christopherson KS, Prehoda KE, Bredt DS, Lim WA. 1999. Unexpected modes of PDZ domain scaffolding revealed by structure of nNOS-syntrophin complex. Science 284:812-815.
79. Hoch W. 1999. Formation of the neuromuscular junction. Agrin and its unusual receptors. Eur J Biochem 265:1-10.
80. Holt KH, Campbell KP. 1998. Assembly of the sarcoglycan complex. Insights for muscular dystrophy. J Biol Chem 273:34667-34670.
81. Hopf C, Hoch W. 1998. Dimerization of the muscle specific kinase induces receptor tyrosine phosphorylation of acetylcholine receptors and their aggregation on the surface of myotubes. J Biol Chem 273:6467-6473.
82. Huang PL, Lo EH. 1998. Genetic analysis of NOS isoforms nNOS and eNOS knockout animals. Progr Brain Res 118:13-25.
83. Huganir RL, Miles K. 1989. Protein phosphorylation of nicotinic acetylcholine receptors. Crit Rev Biochem Mol Biol 24:183-215.
84. Jaffrey SR, Snyder SH. 1996. PIN: an associated protein inhibitor of neuronal nitric oxide synthase. Science 274:774-777.
85. Jaffrey SR, Snowman AM, Eliasson MJ, Cohen NA, Snyder SH. 1998. CAPON: a protein associated with neuronal nitric oxide synthase that regulates its interactions with PSD-95. Neuron 20:115-124.
86. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH. 2001. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 3:193-197.
87. Jones G, Meier T, Lichtsteiner M, Witzemann V, Sakmann B, Brenner HR. 1997. Induction by agrin of ectopic and functional postsynaptic-like membrane in innervated muscle. Proc Natl Acad Sci USA 94:2654-2659.
88. Jones MA, Werle MJ. 2000. Nitric oxide is a downstream mediator of agrin-induced acetylcholine receptor aggregation. Mol Cell Neurosci 16:649-660.
89. Kameya S, Miyagoe Y, Nonaka I, Ikemoto T, Endo M, Hanaoka K, Nabeshima Y, Takeda S. 1999. α1-syntrophin gene disruption results in the absence of neuronal-type nitric-oxide synthase at the sarcolemma but does not induce muscle degeneration. J Biol Chem 274:2193-2200.
90. Kim E, Niethammer M, Rothschild A, Jan YN, Sheng M. 1995. Clustering of Shaker-type K+ channels by interaction with a family of membrane-associated guanylate kinases. Nature 378:85-88.
91. -). Neuron 24:461-469.
92. Kobzik L, Reid MB, Bredt DS, Stamler JS. 1994. Nitric oxide in skeletal muscle. Nature 372:546-548.
93. Kobzik L, Stringer B, Balligand JL, Reid MB, Stamler JS. 1995. Endothelial type nitric oxide synthase in skeletal muscle fibers: mitochondrial relationships. Biochem Biophys Res Commun 211: 375-381.
94. Kramarcy NR, Sealock R. 2000. Syntrophin isoforms at the neuromuscular junction: developmental time course and differential localization. Mol Cell Neurosci 15:262-274.
95. Kusner LL, Kaminski HJ. 1996. Nitric oxide synthase is concentrated at the skeletal muscle endplate. Brain Res 730:238-242.
96. Lee KH, Baek MY, Moon KY, Song WK, Chung CH, Ha DB, Kang MS. 1994. Nitric oxide as a messenger molecule for myoblast fusion. J Biol Chem 269:14371-14374.
97. Lindgren CA, Laird MV. 1994. Nitroprusside inhibits neurotransmitter release at the frog neuromuscular junction. Neuroreport 5:2205-2208.
98. Lück G, Oberbäumer I, Blottner D. 1998. In situ identification of neuronal nitric oxide synthase mRNA in mouse and rat skeletal muscle. Neurosci Lett 246:77-80.
99. Lück G, Hoch W, Hopf C, Blottner D. 2000. Nitric oxide synthase (NOS-1) coclustered with agrin-induced AChR-specializations on cultured skeletal myotubes. Mol Cell Neurosci 16:269-281.
100. Luise M, Presotto C, Senter L, Betto R, Ceoldo S, Furlan S, Salvatori S, Sabbadini RA, Salviati G. 1993. Dystrophin is phosphorylated by endogenous protein kinases. Biochem J 293:243-247.
101. Lupa MT, Krzemien DM, Schaller KL, Caldwell JH. 1993. Aggregation of sodium channels during development and maturation of the neuromuscular junction. J Neurosci 13:1326-1336.
102. Marchand S, Bignami F, Stetzkowski-Marden F, Cartaud J. 2000. The myristoylated protein rapsyn is cotargeted with the nicotinic acetylcholine receptor to the postsynaptic membrane via exocytotic pathway. J Neurosci 20:521-528.
103. Marchand S, Steztkowski-Marden F, Cartaud J. 2001. Differential targeting of components of the dystrophin complex to the postsynaptic membrane. Eur J Neurosci 13:221-229.
104. McMahan UJ. 1990. The agrin hypothesis. Cold Spring Harbor Symp. Quant Biol 55:407-418.
105. Megeath LJ, Fallon JR. 1998. Intracellular calcium regulates agrin-induced acetylcholine receptor clustering. J Neurosci 18:672-678.
106. Meier T, Wallace BG. 1998. Formation of the neuromuscular junction: molecules and mechanisms. BioEssays 20:819-829.
107. Meier T, Masciulli F, Moore C, Schoumacher F, Eppenberger U, Denzer AJ, Jones G, Brenner HR. 1998. Agrin can mediate acetylcholine receptor gene expression in muscle by aggregation of muscle-derived neuregulins. J Cell Biol 141:715-726.
108. Merlie JP, Sanes JR. 1985. Concentration of acetylcholine receptor mRNA in synaptic regions of adult muscle fibres. Nature 317:66-68.
109. Merzaros LG, Minarovic I, Zahradnikova A. 1996. Inhibition of the skeletal muscle ryanodine receptor calcium release channel by nitric oxide. FEBS Lett 380:49-52.
110. Moncada S, Palmer RM, Higgs EA. 1991. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43:109-142.
111. Moscoso LM, Merlie JP, Sanes JR. 1995. N-CAM, 43K-rapsyn, and S-laminin mRNAs are concentrated at synaptic sites in muscle fibers. Mol Cell Neurosci 6:80-89.
112. Nakane M, Schmidt HH, Pollock JS, Forstermann U, Murad F. 1993. Cloned human brain nitric oxide synthase is highly expressed in skeletal muscle. FEBS Lett 316:175-180.
113. Nawrotzki R, Loh NY, Ruegg MA, Davies KE, Blake DJ. 1998. Characterization of α-dystrobrevin in muscle. J Cell Sci 111:2595-2605.
114. Newey SE, Benson MA, Ponting CP, Davies KE, Blake DJ. 2000. Alternative splicing of dystrobrevin regulates the stoichiometry of syntrophin binding to the dystrophin protein complex. Curr Biol 10:1295-1298.
115. Ohlendiek K, Errasti JM, Matsumura K, Kahl SD, Leveille CJ, Campbell KP. 1991. Dystrophin-related protein is localized to neuromuscular junctions of adult skeletal muscle. Neuron 7:499-508.
116. Olivier L, Coureau O, Courtouis Y, Vigny M. 1996. Accumulation of NO synthase (type-1) at the neuromuscular junction. NeuroReport 22:924-926.
117. Peters MF, Kramarcey NR, Sealock R, Froehner SC. 1994. β2-syntrophin: localisation at the neuromuscular junction in skeletal muscle. NeuroReport 5:1577-1580.
118. Peters MF, Adams ME, Froehner SC. 1997. Differential association of syntrophin pairs with the dystrophin complex. J Cell Biol 138:81-93.
119. Piluso G, Mirabella M, Ricci E, Belsito A, Abbondanza C, Servidei S, Puca AA, Tonali P, Puca GA, Nigro V. 2000. γ1- and γ2-syntrophin, two novel dystrophin-binding proteins localized in neural cells. J Biol Chem 275:15851-15860.
120. Poo Mu-ming. 2001. Neurotrophins as synaptic modulators. Nat Rev 2:24-32.
121. Rafael JA, Brown SC. 2000. Dystrophin and utrophin: genetic analysis of their role in skeletal muscle. Microsc Res Tech 48:155-166.
122. Reid MB. 1998. Role of nitric oxide in skeletal muscle: Synthesis, distribution and functional importance. Acta Physiol Scand 162: 401-409.
123. Ribera J, Marsal J, Casanovas A, Hukkanan M, Tarabal O, Esquerda JE. 1998. Nitric oxide synthase at rat neuromuscular junctions and in nerve terminals of Torpedo electric organ. J Neurosci Res 51:90-102.
124. Rimer M, Cohen I, Lomo T, Burden SJ, McMahan UJ. 1998. Neuregulins and erbB-receptors at neuromuscular junctions and at agrin-induced postsynaptic-like apparatus in skeletal muscle. Mol Cell Neurosci 12:1-15.
125. Ruegg MA, Bixby JL. 1998. Agrin orchestrates synaptic differentiation at the vertebrate neuromuscular junction. Trends Neurosci 21:22-27.
126. Sadaulet-Puccio HM, Rajala M, Kunkel LM. 1997. Dystrobrevin and dystrophin: an interaction through coiled-coil motifs. Proc Natl Acad Sci USA 94:12413-12418.
127. Salt TE, Zhang H, Mayer B, Benz B, Binns KE, Do KQ. 2000. Novel mode of nitric oxide neurotransmission mediated via S-nitrosocysteinyl-glycine. Eur J Neurosci 12:3919-3925.
128. Sanes JR, Lichtman JW. 1999. Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22:389-442.
129. Sanes JR, Apel ED, Burgess RW, Emerson RB, Feng G, Gautam M, Glass D, Grady RM, Krejci E, Lichtman JW, Lu JT, Massoulie J, Miner JH, Moscoso LM, Nguyen Q, Nichol M, Noakes PG, Patton BL, Son YJ, Yancopoulos GD, Zhou H. 1998. Development of the neuromuscular junction: Genetic analysis in mice. Physiol Rev (Paris) 92:167-172.
130. Schulman H. 1997. Nitric oxide: a spatial second messenger. Mol Psychiatry 2:296-299.
131. Silvagno F, Xia H, Bredt DS. 1996. Neuronal nitric oxide synthase-μ, an alternatively spliced isoform present in differentiated skeletal muscle. J Biol Chem 271:11204-11208.
132. Snider WD, Lichtman JW. 1996. Are neurotrophins synaptotrophins? Mol Cell Neurosci 7:433-442.
133. Stamler JS. 1994. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 78:931-936.
134. Stamler JS, Meissner G. 2001. Physiology of nitric oxide in skeletal muscle. Physiol Rev 81:209-237.
135. Stamler JS, Toone EJ, Lipton SA, Sucher NJ. 1997. (S)NO signals: transduction, regulation, and a consensus motif. Neuron 18:691-696.
136. Stricker NL, Christopherson KS, Yi BA, Schatz PJ, Raab RW, Dawes G, Bassett DE, Bredt DS, Li M. 1997. PDZ domain of neuronal nitric oxide synthase recognizes novel C-terminal peptide sequences. Nat Biotechnol 15:336-342.
137. Suzuki A, Yoshida M, Ozawa E. 1995. Mammalian α1- and β1-syntrophin bind to the alternative splice-prone region of the dystrophin COOH terminus. J Cell Biol 128:373-381.
138. Taguchi J, Ohta H, Talman WT. 1995. Identification and pharmacological characterisation of an S-nitrosogluthation binding site in rat brain. Soc Neurosci (Abstract) 2:254.16.
139. Teng KK, Esposito DK, Schwartz GD, Lander HM, Hempstead BL. 1999. Activation of c-Ha-Ras by nitric oxide modulates survival responsiveness in neuronal PC12 cells. J Biol Chem 274:37315-37320.
140. Tews DS, Goebel HH, Schneider I, Gunkel A, Stennert E, Neiss WF. 1997. Expression of different isoforms of nitric oxide synthase in experimentally denervated and reinnervated skeletal muscle. J Neuropathol Exp Neurol 56:1283-1289.
141. Urazaev AK, Naumenko NV, Poletayev GI, Nikolsky EE, Vyskocil F. 1996. Nitroprusside decreases the early post-denervation depolarization of diaphragm muscle fibres of the rat. Eur J Pharmacol 316:219-222.
142. Wagner KR, Cohen JB, Huganir RL. 1993. The 87K postsynaptic membrane protein from Torpedo is a protein-tyrosine kinase substrate homologous to dystrophin. Neuron 10:511-522.
143. Wakayama Y, Inoue M, Murahashi M, Shibuya S, Jimi T, Kojima H, Oniki H. 1997. Ultrastructural localization of α1 syntrophin and neuronal nitric oxide synthase in normal skeletal myofiber, and their relation to each other and to dystrophin. Acta Neuropathol 94:455-464.
144. Wallace BG. 1995. Regulation of the interaction of nicotinic acetylcholine receptors with the cytoskeleton by agrin-activated protein phosphorylation. J Cell Biol 128:1121-1129.
145. Wang T, Xie Z, Lu B. 1995. Nitric oxide mediates activity-dependent synaptic suppression at developing neuromuscular synapses. Nature 374:262-266.
146. Wang Y, Newton DC, Robb GB, Kau CL, Miller TL, Cheung AH, Hall AV, VanDamme S, Wilcox JN, Marsden PA. 1999a. RNA diversity has profound effects on the translation of neuronal nitric oxide synthase. Proc Natl Acad Sci USA 96:12150-12155.
147. Wang Y, Newton DC, Marsden PA. 1999b. Neuronal NOS: Gene structure, mRNA diversity, and functional relevance. Crit Rev Neurobiol 13:21-43.
148. Wildemann B, Bicker G. 1999. Developmental expression of nitric oxide/cyclic GMP synthesizing cells in the nervous system of Drosophila melanogaster. J Neurobiol 38:1-15.
149. Wörl J, Mayer B, Neuhuber WL. 1994. Nitrergic innervation of the rat esophagus: focus on motor endplates. J Auton Nerv Syst 49:227-233.
150. Xu KY, Huso DL, Dawson TM, Bredt DS, Becker LC. 1999. Nitric oxide synthase in cardiac sarcoplasmic reticulum. Proc Natl Acad Sci USA 96:657-662.
151. Yang CC, Alvarez RB, Engel WK, Haun CK, Askanas V. 1997. Immunolocalization of nitric oxide synthase at the postsynaptic density domain of human and rat neuromuscular junctions - light and electron microscopic studies. Exp Neurol 148:34-44.
152. Yun HY, Gonzalez-Zulueta M, Dawson VL, Dawson TM. 1998. Nitric oxide mediates N-methyl-D-aspartate receptor-induced activation of p21ras. Proc Natl Acad Sci USA 95:5773-5778.