Role of extracellular matrix proteins and their receptors in the development of the vertebrate neuromuscular junction

Developmental Neurobiology

Volumn 71, Issue 11, 2011, Pages 982-1005

  Singhal, Neha ^a   Martin, Paul T ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Agrin; Extracellular matrix; Laminin; Neuromuscular junction; Synapse

Indexed keywords

ACETYLCHOLINESTERASE; AGRIN; BINDING PROTEIN; CELL MEMBRANE PROTEIN; COLLAGEN TYPE 13; COLLAGEN TYPE 4; DYSTROGLYCAN; ENTACTIN; FIBRONECTIN; INTEGRIN; LAMININ; LAMININ ALPHA2; MEMBRANE RECEPTOR; NEU DIFFERENTIATION FACTOR; PERLECAN; PROTEIN MUSK LRP4; SCLEROPROTEIN; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

ARTICLE; BASEMENT MEMBRANE; BIOCHEMICAL COMPOSITION; CELL MATURATION; CELL ULTRASTRUCTURE; DEVELOPMENTAL STABILITY; EXTRACELLULAR MATRIX; HUMAN; MOLECULAR GENETICS; MUSCLE FIBRIL; NERVE CELL DIFFERENTIATION; NEUROBIOLOGY; NEUROMUSCULAR FUNCTION; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NONHUMAN; PHENOTYPE; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SYNAPTOGENESIS; VERTEBRATE;

ANIMALS; CELL DIFFERENTIATION; EXTRACELLULAR MATRIX PROTEINS; HUMANS; NEUROGENESIS; NEUROMUSCULAR JUNCTION; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; SYNAPTIC MEMBRANES; VERTEBRATES;

EID: 80053912306     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20953     Document Type: Article

References (258)

1. 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.
2. Altiok N, Bessereau JL, Changeux JP. 1995. ErbB3 and ErbB2/neu mediate the effect of heregulin on acetylcholine receptor gene expression in muscle: Differential expression at the endplate. EMBO J 14: 4258-4266.
3. 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.
4. Arber S, Caroni P. 1995. Thrombospondin-4, an extracellular matrix protein expressed in the developing and adult nervous system promotes neurite outgrowth. J Cell Biol 131: 1083-1094.
5. Arikawa-Hirasawa E, Rossi SG, Rotundo RL, Yamada Y. 2002. Absence of acetylcholinesterase at the neuromuscular junctions of perlecan-null mice. Nat Neurosci 5: 119-123.
6. Aumailley M, Battaglia C, Mayer U, Reinhardt D, Nischt R, Timpl R, Fox JW. 1993. Nidogen mediates the formation of ternary complexes of basement membrane components. Kidney Int 43: 7-12.
7. Aumailley M, Bruckner-Tuderman L, Carter WG, Deutzmann R, Edgar D, Ekblom P, Engel J, et al. 2005. A simplified laminin nomenclature. Matrix Biol 24: 326-332.
8. Balice-Gordon RJ, Lichtman JW. 1990. In vivo visualization of the growth of pre- and postsynaptic elements of neuromuscular junctions in the mouse. J Neurosci 10: 894-908.
9. Barresi R, Campbell KP. 2006. Dystroglycan: From biosynthesis to pathogenesis of human disease. J Cell Sci 119: 199-207.
10. Bentzinger CF, Barzaghi P, Lin S, Ruegg MA. 2005. Overexpression of mini-agrin in skeletal muscle increases muscle integrity and regenerative capacity in laminin-alpha2-deficient mice. FASEB J 19: 934-942.
11. Bergamin E, Hallock PT, Burden SJ, Hubbard SR. 2010. The cytoplasmic adaptor protein Dok7 activates the receptor tyrosine kinase MuSK via dimerization. Mol Cell 39: 100-109.
12. Bernard V, Girard E, Hrabovska A, Camp S, Taylor P, Plaud B, Krejci E. 2011. Distinct localization of collagen Q and PRiMA forms of acetylcholinesterase at the neuromuscular junction. Mol Cell Neurosci 46: 272-281.
13. Blake DJ, Weir A, Newey SE, Davies KE. 2002. Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 82: 291-329.
14. Borges LS, Yechikhov S, Lee YI, Rudell JB, Friese MB, Burden SJ, Ferns MJ. 2008. Identification of a motif in the acetylcholine receptor beta subunit whose phosphorylation regulates rapsyn association and postsynaptic receptor localization. J Neurosci 28: 11468-11476.
15. Bowe MA, Deyst KA, Leszyk JD, Fallon JR. 1994. Identification and purification of an agrin receptor from Torpedo postsynaptic membranes: A heteromeric complex related to the dystroglycans. Neuron 12: 1173-1180.
16. Brandan E, Inestrosa NC. 1984. Binding of the asymmetric forms of acetylcholinesterase to heparin. Biochem J 221: 415-422.
17. Brandon EP, Lin W, D'Amour KA, Pizzo DP, Dominguez B, Sugiura Y, Thode S, et al. 2003. Aberrant patterning of neuromuscular synapses in choline acetyltransferase-deficient mice. J Neurosci 23: 539-549.
18. Broadie K, Baumgartner S, Prokop A. 2011. Extracellular matrix and its receptors in Drosophila neural development. Dev Neurobiol 71: 1102-1130.
19. Bromann PA, Weiner JA, Apel ED, Lewis RM, Sanes JR. 2004. A putative ariadne-like E3 ubiquitin ligase (PAUL) that interacts with the muscle-specific kinase (MuSK). Gene Expr Patterns 4: 77-84.
20. Burden SJ. 1993. Synapse-specific gene expression. Trends Genet 9: 12-16.
21. Burden SJ, Sargent PB, McMahan UJ. 1979. Acetylcholine receptors in regenerating muscle accumulate at original synaptic sites in the absence of the nerve. J Cell Biol 82: 412-425.
22. Burgess RW, Dickman DK, Nunez L, Glass DJ, Sanes JR. 2002. Mapping sites responsible for interactions of agrin with neurons. J Neurochem 83: 271-284.
23. Burgess RW, Nguyen QT, Son YJ, Lichtman JW, Sanes JR. 1999. Alternatively spliced isoforms of nerve- and muscle-derived agrin: Their roles at the neuromuscular junction. Neuron 23: 33-44.
24. Burgess RW, Skarnes WC, Sanes JR. 2000. Agrin isoforms with distinct amino termini: Differential expression, localization, and function. J Cell Biol 151: 41-52.
25. Burkin DJ, Gu M, Hodges BL, Campanelli JT, Kaufman SJ. 1998. A functional role for specific spliced variants of the alpha7beta1 integrin in acetylcholine receptor clustering. J Cell Biol 143: 1067-1075.
26. Burkin DJ, Kim JE, Gu M, Kaufman SJ. 2000. Laminin and alpha7beta1 integrin regulate agrin-induced clustering of acetylcholine receptors. J Cell Sci 113(Pt 16): 2877-2886.
27. Burkin DJ, Wallace GQ, Milner DJ, Chaney EJ, Mulligan JA, Kaufman SJ. 2005. Transgenic expression of {alpha}7{beta}1 integrin maintains muscle integrity, increases regenerative capacity, promotes hypertrophy, and reduces cardiomyopathy in dystrophic mice. Am J Pathol 166: 253-263.
28. Burkin DJ, Wallace GQ, Nicol KJ, Kaufman DJ, Kaufman SJ. 2001. Enhanced expression of the alpha 7 beta 1 integrin reduces muscular dystrophy and restores viability in dystrophic mice. J Cell Biol 152: 1207-1218.
29. Campanelli JT, Gayer GG, Scheller RH. 1996. Alternative RNA splicing that determines agrin activity regulates binding to heparin and alpha-dystroglycan. Development 122: 1663-1672.
30. Carlson SS, Valdez G, Sanes JR. 2010. Presynaptic calcium channels and alpha3-integrins are complexed with synaptic cleft laminins, cytoskeletal elements and active zone components. J Neurochem 115: 654-666.
31. Cartaud A, Strochlic L, Guerra M, Blanchard B, Lambergeon M, Krejci E, Cartaud J, et al. 2004. MuSK is required for anchoring acetylcholinesterase at the neuromuscular junction. J Cell Biol 165: 505-515.
32. Chandrasekharan K, Martin PT. 2010. Genetic defects in muscular dystrophy. Methods Enzymol 479: 291-322.
33. Chen F, Qian L, Yang ZH, Huang Y, Ngo ST, et al. 2007. Rapsyn interaction with calpain stabilizes AChR clusters at the neuromuscular junction. Neuron 55: 247-260.
34. Chen J, Billings SE, Nishimune H. 2011. Calcium channels link the muscle-derived synapse organizer laminin beta2 to Bassoon and CAST/Erc2 to organize presynaptic active zones. J Neurosci 31: 512-525.
35. Cheusova T, Khan MA, Schubert SW, Gavin AC, Buchou T, et al. 2006. Casein kinase 2-dependent serine phosphorylation of MuSK regulates acetylcholine receptor aggregation at the neuromuscular junction. Genes Dev 20: 1800-1816.
36. Chiu AY, Ko J. 1994. A novel epitope of entactin is present at the mammalian neuromuscular junction. J Neurosci 14: 2809-2817.
37. Chiu AY, Sanes JR. 1984. Development of basal lamina in synaptic and extrasynaptic portions of embryonic rat muscle. Dev Biol 103: 456-467.
38. Cho SI, Ko J, Patton BL, Sanes JR, Chiu AY. 1998. Motor neurons and Schwann cells distinguish between synaptic and extrasynaptic isoforms of laminin. J Neurobiol 37: 339-358.
39. Chu GC, Moscoso LM, Sliwkowski MX, Merlie JP. 1995. Regulation of the acetylcholine receptor epsilon subunit gene by recombinant ARIA: An in vitro model for transynaptic gene regulation. Neuron 14: 329-339.
40. Cifuentes-Diaz C, Velasco E, Meunier FA, Goudou D, Belkadi L, Faille L, Murawsky M, et al. 1998. The peripheral nerve and the neuromuscular junction are affected in the tenascin-C-deficient mouse. Cell Mol Biol 44: 357-379.
41. Cohen I, Rimer M, Lomo T, McMahan UJ. 1997. Agrin-induced postsynaptic-like apparatus in skeletal muscle fibers in vivo. Mol Cell Neurosci 9: 237-253.
42. Cohen MW, Hoffstrom BG, DeSimone DW. 2000. Active zones on motor nerve terminals contain alpha 3beta 1 integrin. J Neurosci 20: 4912-4921.
43. Cohn RD, Henry MD, Michele DE, Barresi R, Saito F, Moore SA, Flanagan JD, et al. 2002. Disruption of DAG1 in differentiated skeletal muscle reveals a role for dystroglycan in muscle regeneration. Cell 110: 639-648.
44. Cote PD, Moukhles H, Lindenbaum M, Carbonetto S. 1999. Chimaeric mice deficient in dystroglycans develop muscular dystrophy and have disrupted myoneural synapses. Nat Genet 23: 338-342.
45. DeChiara TM, Bowen DC, Valenzuela DM, Simmons MV, Poueymirou WT, Thomas S, Kinetz E, et al. 1996. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85: 501-512.
46. Deconinck AE, Potter AC, Tinsley JM, Wood SJ, Vater R, Young C, Metzinger L, et al. 1997. Postsynaptic abnormalities at the neuromuscular junctions of utrophin-deficient mice. J Cell Biol 136: 883-894.
47. Deconinck N, Tinsley J, De Backer F, Fisher R, Kahn D, Phelps S, Davies K, et al. 1997. Expression of truncated utrophin leads to major functional improvements in dystrophin-deficient muscles of mice. Nat Med 3: 1216-1221.
48. Denzer AJ, Schulthess T, Fauser C, Schumacher B, Kammerer RA, Engel J, Ruegg MA. 1998. Electron microscopic structure of agrin and mapping of its binding site in laminin-1. EMBO J 17: 335-343.
49. Durbeej M, Campbell KP. 2002. Muscular dystrophies involving the dystrophin-glycoprotein complex: An overview of current mouse models. Curr Opin Genet Dev 12: 349-361.
50. Egles C, Claudepierre T, Manglapus MK, Champliaud MF, Brunken WJ, Hunter DD. 2007. Laminins containing the beta2 chain modulate the precise organization of CNS synapses. Mol Cell Neurosci 34: 288-298.
51. Engel AG, Ohno K, Sine SM. 1999. Congenital myasthenic syndromes: Recent advances. Arch Neurol 56: 163-167.
52. Engel AG, Shen XM, Selcen D, Sine SM. 2010. What have we learned from the congenital myasthenic syndromes. J Mol Neurosci 40: 143-153.
53. Engvall E, Earwicker D, Haaparanta T, Ruoslahti E, Sanes JR. 1990. Distribution and isolation of four laminin variants; tissue restricted distribution of heterotrimers assembled from five different subunits. Cell Regul 1: 731-740.
54. Ervasti JM, Campbell KP. 1991. Membrane organization of the dystrophin-glycoprotein complex. Cell 66: 1121-1131.
55. Ervasti JM, Sonnemann KJ. 2008. Biology of the striated muscle dystrophin-glycoprotein complex. Int Rev Cytol 265: 191-225.
56. Escher P, Lacazette E, Courtet M, Blindenbacher A, Landmann L, Bezakova G, Lloyd KC, et al. 2005. Synapses form in skeletal muscles lacking neuregulin receptors. Science 308: 1920-1923.
57. Eusebio A, Oliveri F, Barzaghi P, Ruegg MA. 2003. Expression of mouse agrin in normal, denervated and dystrophic muscle. Neuromuscul Disord 13: 408-415.
58. Falls DL, Rosen KM, Corfas G, Lane WS, Fischbach GD. 1993. ARIA, a protein that stimulates acetylcholine receptor synthesis, is a member of the neu ligand family. Cell 72: 801-815.
59. Fambrough DM. 1979. Control of acetylcholine receptors in skeletal muscle. Physiol Rev 59: 165-227.
60. Farrugia ME, Vincent A. 2010. Autoimmune mediated neuromuscular junction defects. Curr Opin Neurol 23: 489-495.
61. Feng G, Krejci E, Molgo J, Cunningham JM, Massoulie J, Sanes JR. 1999. Genetic analysis of collagen Q: Roles in acetylcholinesterase and butyrylcholinesterase assembly and in synaptic structure and function. J Cell Biol 144: 1349-1360.
62. Finn AJ, Feng G, Pendergast AM. 2003. Postsynaptic requirement for Abl kinases in assembly of the neuromuscular junction. Nat Neurosci 6: 717-723.
63. Flanagan-Steet H, Fox MA, Meyer D, Sanes JR. 2005. Neuromuscular synapses can form in vivo by incorporation of initially aneural postsynaptic specializations. Development 132: 4471-4481.
64. Fox JW, Mayer U, Nischt R, Aumailley M, Reinhardt D, Wiedemann H, Mann K, et al. 1991. Recombinant nidogen consists of three globular domains and mediates binding of laminin to collagen type IV. EMBO J 10: 3137-3146.
65. Fox MA, Ho MS, Smyth N, Sanes JR. 2008. A synaptic nidogen: Developmental regulation and role of nidogen-2 at the neuromuscular junction. Neural Dev 3: 24.
66. Fox MA, Sanes JR, Borza DB, Eswarakumar VP, Fassler R, Hudson BG, John SW, et al. 2007. Distinct target-derived signals organize formation, maturation, and maintenance of motor nerve terminals. Cell 129: 179-193.
67. Frail DE, McLaughlin LL, Mudd J, Merlie JP. 1988. Identification of the mouse muscle 43, 000-dalton acetylcholine receptor-associated protein (RAPsyn) by cDNA cloning. J Biol Chem 263: 15602-15607.
68. Fu AK, Ip FC, Fu WY, Cheung J, Wang JH, Yung WH, Ip NY. 2005. Aberrant motor axon projection, acetylcholine receptor clustering, and neurotransmission in cyclin- dependent kinase 5 null mice. Proc Natl Acad Sci USA 102: 15224-15229.
69. Gassmann M, Lemke G. 1997. Neuregulins and neuregulin receptors in neural development. Curr Opin Neurobiol 7: 87-92.
70. Gautam M, Noakes PG, Moscoso L, Rupp F, Scheller RH, Merlie JP, Sanes JR. 1996. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85: 525-535.
71. Gautam M, Noakes PG, Mudd J, Nichol M, Chu GC, Sanes JR, Merlie JP. 1995. Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377: 232-236.
72. Gawlik K, Miyagoe-Suzuki Y, Ekblom P, Takeda S, Durbeej M. 2004. Laminin alpha1 chain reduces muscular dystrophy in laminin alpha2 chain deficient mice. Hum Mol Genet 13: 1775-1784.
73. Gerrow K, El-Husseini A. 2006. Cell adhesion molecules at the synapse. Front Biosci 11: 2400-2419.
74. Gesemann M, Brancaccio A, Schumacher B, Ruegg MA. 1998. Agrin is a high-affinity binding protein of dystroglycan in non-muscle tissue. J Biol Chem 273: 600-605.
75. Gesemann M, Cavalli V, Denzer AJ, Brancaccio A, Schumacher B, Ruegg MA. 1996. Alternative splicing of agrin alters its binding to heparin, dystroglycan, and the putative agrin receptor. Neuron 16: 755-767.
76. Gesemann M, Denzer AJ, Ruegg MA. 1995. Acetylcholine receptor-aggregating activity of agrin isoforms and mapping of the active site. J Cell Biol 128: 625-636.
77. Glass DJ, Bowen DC, Stitt TN, Radziejewski C, Bruno J, Ryan TE, Gies DR, et al. 1996. Agrin acts via a MuSK receptor complex. Cell 85: 513-523.
78. Godfrey EW, Nitkin RM, Wallace BG, Rubin LL, McMahan UJ. 1984. Components of Torpedo electric organ and muscle that cause aggregation of acetylcholine receptors on cultured muscle cells. J Cell Biol 99: 615-627.
79. Goodearl AD, Yee AG, Sandrock AWJr, Corfas G, Fischbach GD. 1995. ARIA is concentrated in the synaptic basal lamina of the developing chick neuromuscular junction. J Cell Biol 130: 1423-1434.
80. Grady RM, Merlie JP, Sanes JR. 1997. Subtle neuromuscular defects in utrophin-deficient mice. J Cell Biol 136: 871-882.
81. Grady RM, Zhou H, Cunningham JM, Henry MD, Campbell KP, Sanes JR. 2000. Maturation and maintenance of the neuromuscular synapse: Genetic evidence for roles of the dystrophin-glycoprotein complex. Neuron 25: 279-293.
82. Hagg P, Rehn M, Huhtala P, Vaisanen T, Tamminen M, Pihlajaniemi T. 1998. Type XIII collagen is identified as a plasma membrane protein. J Biol Chem 273: 15590-15597.
83. Hagg P, Vaisanen T, Tuomisto A, Rehn M, Tu H, Huhtala P, Eskelinen S, et al. 2001. Type XIII collagen: A novel cell adhesion component present in a range of cell-matrix adhesions and in the intercalated discs between cardiac muscle cells. Matrix Biol 19: 727-742.
84. Hall ZW. 1973. Multiple forms of acetylcholinesterase and their distribution in endplate and non-endplate regions of rat diaphragm muscle. J Neurobiol 4: 343-361.
85. Hallock PT, Xu CF, Park TJ, Neubert TA, Curran T, Burden SJ. 2010. Dok-7 regulates neuromuscular synapse formation by recruiting Crk and Crk-L. Genes Dev 24: 2451-2461.
86. Han B, Fischbach GD. 1999. Processing of ARIA and release from isolated nerve terminals. Philos Trans R Soc Lond B Biol Sci 354: 411-416.
87. Hara Y, Balci-Hayta B, Yoshida-Moriguchi T, Kanagawa M, Beltran-Valero de Bernabe D, Gundesli H, Willer T, et al. 2011. A dystroglycan mutation associated with limb-girdle muscular dystrophy. N Engl J Med 364: 939-946.
88. Hayashi YK, Chou FL, Engvall E, Ogawa M, Matsuda C, Hirabayashi S, Yokochi K, et al. 1998. Mutations in the integrin alpha7 gene cause congenital myopathy. Nat Genet 19: 94-97.
89. Herbst R, Avetisova E, Burden SJ. 2002. Restoration of synapse formation in Musk mutant mice expressing a Musk/Trk chimeric receptor. Development 129: 5449-5460.
90. Herbst R, Burden SJ. 2000. The juxtamembrane region of MuSK has a critical role in agrin-mediated signaling. EMBO J 19: 67-77.
91. Hezel M, de Groat WC, Galbiati F. 2010. Caveolin-3 promotes nicotinic acetylcholine receptor clustering and regulates neuromuscular junction activity. Mol Biol Cell 21: 302-310.
92. Hilgenberg LG, Su H, Gu H, O'Dowd DK, Smith MA. 2006. Alpha3Na+/K+-ATPase is a neuronal receptor for agrin. Cell 125: 359-369.
93. Hoch W, Ferns M, Campanelli JT, Hall ZW, Scheller RH. 1993. Developmental regulation of highly active alternatively spliced forms of agrin. Neuron 11: 479-490.
94. Hoffman EP, Brown RHJr, Kunkel LM. 1987. Dystrophin: The protein product of the Duchenne muscular dystrophy locus. Cell 51: 919-928.
95. Holmes WE, Sliwkowski MX, Akita RW, Henzel WJ, Lee J, Park JW, Yansura D, et al. 1992. Identification of heregulin, a specific activator of p185erbB2. Science 256: 1205-1210.
96. Hoyte K, Kang C, Martin PT. 2002. Definition of pre- and postsynaptic forms of the CT carbohydrate antigen at the neuromuscular junction: Ubiquitous expression of the CT antigens and the CT GalNAc transferase in mouse tissues. Brain Res Mol Brain Res 109: 146-160.
97. Hughes BW, Kusner LL, Kaminski HJ. 2006. Molecular architecture of the neuromuscular junction. Muscle Nerve 33: 445-461.
98. Hunter DD, Porter BE, Bulock JW, Adams SP, Merlie JP, Sanes JR. 1989. Primary sequence of a motor neuron-selective adhesive site in the synaptic basal lamina protein S-laminin. Cell 59: 905-913.
99. Huze C, Bauche S, Richard P, Chevessier F, Goillot E, Gaudon K, Ben Ammar A, et al. 2009. Identification of an agrin mutation that causes congenital myasthenia and affects synapse function. Am J Hum Genet 85: 155-167.
100. Ibraghimov-Beskrovnaya O, Milatovich A, Ozcelik T, Yang B, Koepnick K, Francke U, Campbell KP. 1993. Human dystroglycan: Skeletal muscle cDNA, genomic structure, origin of tissue specific isoforms and chromosomal localization. Hum Mol Genet 2: 1651-1657.
101. Ichtchenko K, Hata Y, Nguyen T, Ullrich B, Missler M, Moomaw C, Sudhof TC. 1995. Neuroligin 1: A splice site-specific ligand for beta-neurexins. Cell 81: 435-443.
102. Inoue A, Setoguchi K, Matsubara Y, Okada K, Sato N, Iwakura Y, Higuchi O, et al. 2009. Dok-7 activates the muscle receptor kinase MuSK and shapes synapse formation. Sci Signal 2: ra7.
103. Jaworski A, Burden SJ. 2006. Neuromuscular synapse formation in mice lacking motor neuron- and skeletal muscle-derived Neuregulin-1. J Neurosci 26: 655-661.
104. Jennings CG, Dyer SM, Burden SJ. 1993. Muscle-specific trk-related receptor with a kringle domain defines a distinct class of receptor tyrosine kinases. Proc Natl Acad Sci USA 90: 2895-2899.
105. Jenniskens GJ, Oosterhof A, Brandwijk R, Veerkamp JH, van Kuppevelt TH. 2000. Heparan sulfate heterogeneity in skeletal muscle basal lamina: Demonstration by phage display-derived antibodies. J Neurosci 20: 4099-4111.
106. Jo SA, Zhu X, Marchionni MA, Burden SJ. 1995. Neuregulins are concentrated at nerve-muscle synapses and activate ACh-receptor gene expression. Nature 373: 158-161.
107. 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.
108. Kadler KE, Baldock C, Bella J, Boot-Handford RP. 2007. Collagens at a glance. J Cell Sci 120: 1955-1958.
109. Kim ML, Chandrasekharan K, Glass M, Shi S, Stahl MC, Kaspar B, Stanley P, Martin PT. 2008. O-fucosylation of muscle agrin determines its ability to cluster acetylcholine receptors. Mol Cell Neurosci 39: 452-464.
110. Kim N, Burden SJ. 2008. MuSK controls where motor axons grow and form synapses. Nat Neurosci 11: 19-27.
111. Kim N, Stiegler AL, Cameron TO, Hallock PT, Gomez AM, Huang JH, Hubbard SR, et al. 2008. Lrp4 is a receptor for Agrin and forms a complex with MuSK. Cell 135: 334-342.
112. Koenig M, Hoffman EP, Bertelson CJ, Monaco AP, Feener C, Kunkel LM. 1987. Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 50: 509-517.
113. Korkut C, Budnik V. 2009. WNTs tune up the neuromuscular junction. Nat Rev Neurosci 10: 627-634.
114. Krejci E, Thomine S, Boschetti N, Legay C, Sketelj J, Massoulie J. 1997. The mammalian gene of acetylcholinesterase-associated collagen. J Biol Chem 272: 22840-22847.
115. Kummer TT, Misgeld T, Sanes JR. 2006. Assembly of the postsynaptic membrane at the neuromuscular junction: Paradigm lost. Curr Opin Neurobiol 16: 74-82.
116. Lacazette E, Le Calvez S, Gajendran N, Brenner HR. 2003. A novel pathway for MuSK to induce key genes in neuromuscular synapse formation. J Cell Biol 161: 727-736.
117. Lampe AK, Bushby KM. 2005. Collagen VI related muscle disorders. J Med Genet 42: 673-685.
118. LaRochelle WJ, Froehner SC. 1986. Determination of the tissue distributions and relative concentrations of the postsynaptic 43-kDa protein and the acetylcholine receptor in Torpedo. J Biol Chem 261: 5270-5274.
119. Latvanlehto A, Fox MA, Sormunen R, Tu H, Oikarainen T, Koski A, Naumenko N, et al. 2010. Muscle-derived collagen XIII regulates maturation of the skeletal neuromuscular junction. J Neurosci 30: 12230-12241.
120. Lee CY, Tseng LF, Chin TH. 1967. Influence of denervation on the localization of neurotoxins from clapid venom in rat diaphragm. Nature 215: 1177-1178.
121. Lemke G. 2006. Neuregulin-1 and myelination. Sci STKE 2006: pe11.
122. Lemke GE, Brockes JP. 1984. Identification and purification of glial growth factor. J Neurosci 4: 75-83.
123. Letinsky MS, Fischbeck KH, McMahan UJ. 1976. Precision of reinnervation of original postsynaptic sites in frog muscle after a nerve crush. J Neurocytol 5: 691-718.
124. Leu M, Bellmunt E, Schwander M, Farinas I, Brenner HR, Muller U. 2003. Erbb2 regulates neuromuscular synapse formation and is essential for muscle spindle development. Development 130: 2291-2301.
125. Lin W, Burgess RW, Dominguez B, Pfaff SL, Sanes JR, Lee KF. 2001. Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature 410: 1057-1064.
126. Lin W, Dominguez B, Yang J, Aryal P, Brandon EP, Gage FH, Lee KF. 2005. Neurotransmitter acetylcholine negatively regulates neuromuscular synapse formation by a Cdk5-dependent mechanism. Neuron 46: 569-579.
127. Lin W, Sanchez HB, Deerinck T, Morris JK, Ellisman M, Lee KF. 2000. Aberrant development of motor axons and neuromuscular synapses in erbB2-deficient mice. Proc Natl Acad Sci USA 97: 1299-1304.
128. Linnoila J, Wang Y, Yao Y, Wang ZZ. 2008. A mammalian homolog of Drosophila tumorous imaginal discs. Tid1, mediates agrin signaling at the neuromuscular junction Neuron 60: 625-641.
129. Love DR, Hill DF, Dickson G, Spurr NK, Byth BC, Marsden RF, Walsh FS, et al. 1989. An autosomal transcript in skeletal muscle with homology to dystrophin. Nature 339: 55-58.
130. Lu Z, Je HS, Young P, Gross J, Lu B, Feng G. 2007. Regulation of synaptic growth and maturation by a synapse-associated E3 ubiquitin ligase at the neuromuscular junction. J Cell Biol 177: 1077-1089.
131. Luo ZG, Je HS, Wang Q, Yang F, Dobbins GC, Yang ZH, Xiong WC, et al. 2003. Implication of geranylgeranyltransferase I in synapse formation. Neuron 40: 703-717.
132. Luo ZG, Wang Q, Zhou JZ, Wang J, Luo Z, Liu M, He X, et al. 2002. Regulation of AChR clustering by Dishevelled interacting with MuSK and PAK1. Neuron 35: 489-505.
133. Madhavan R, Zhao XT, Ruegg MA, Peng HB. 2005. Tyrosine phosphatase regulation of MuSK-dependent acetylcholine receptor clustering. Mol Cell Neurosci 28: 403-416.
134. Magill-Solc C, McMahan UJ. 1990a. Agrin-like molecules in motor neurons. J Physiol (Paris) 84: 78-81.
135. Magill-Solc C, McMahan UJ. 1990b. Synthesis and transport of agrin-like molecules in motor neurons. J Exp Biol 153: 1-10.
136. Marchionni MA, Goodearl AD, Chen MS, Bermingham-McDonogh O, Kirk C, Hendricks M, Danehy F, et al. 1993. Glial growth factors are alternatively spliced erbB2 ligands expressed in the nervous system. Nature 362: 312-318.
137. Marshall LM, Sanes JR, McMahan UJ. 1977. Reinnervation of original synaptic sites on muscle fiber basement membrane after disruption of the muscle cells. Proc Natl Acad Sci USA 74: 3073-3077.
138. Martin PT. 2003. Dystroglycan glycosylation and its role in matrix binding in skeletal muscle. Glycobiology 13: 55R-66R.
139. Martin PT. 2006. Mechanisms of disease: Congenital muscular dystrophies-glycosylation takes center stage. Nat Clin Pract Neurol 2: 222-230.
140. Martin PT, Ettinger AJ, Sanes JR. 1995. A synaptic localization domain in the synaptic cleft protein laminin beta 2 (s-laminin). Science 269: 413-416.
141. Martin PT, Kaufman SJ, Kramer RH, Sanes JR. 1996. Synaptic integrins in developing, adult, and mutant muscle: Selective association of alpha1, alpha7A, and alpha7B integrins with the neuromuscular junction. Dev Biol 174: 125-139.
142. Martin PT, Sanes JR. 1997. Integrins mediate adhesion to agrin and modulate agrin signaling. Development 124: 3909-3917.
143. Martin PT, Scott LJ, Porter BE, Sanes JR. 1999. Distinct structures and functions of related pre- and postsynaptic carbohydrates at the mammalian neuromuscular junction. Mol Cell Neurosci 13: 105-118.
144. Martin PT, Xu R, Rodino-Klapac LR, Oglesbay E, Camboni M, Montgomery CL, Shontz K, et al. 2009. Overexpression of Galgt2 in skeletal muscle prevents injury resulting from eccentric contractions in both mdx and wild-type mice. Am J Physiol Cell Physiol 296: C476-C488.
145. Maselli RA, Ng JJ, Anderson JA, Cagney O, Arredondo J, Williams C, Wessel HB. 2009. Mutations in LAMB2 causing a severe form of synaptic congenital myasthenic syndrome. J Med Genet 46: 203-208.
146. Massoulie J, Millard CB. 2009. Cholinesterases and the basal lamina at vertebrate neuromuscular junctions. Curr Opin Pharmacol 9: 316-325.
147. Matsumura K, Ervasti JM, Ohlendieck K, Kahl SD, Campbell KP. 1992. Association of dystrophin-related protein with dystrophin-associated proteins in mdx mouse muscle. Nature 360: 588-591.
148. May P, Woldt E, Matz RL, Boucher P. 2007. The LDL receptor-related protein (LRP) family: An old family of proteins with new physiological functions. Ann Med 39: 219-228.
149. Mayer U, Saher G, Fassler R, Bornemann A, Echtermeyer F, von der Mark H, Miosge N, et al. 1997. Absence of integrin alpha 7 causes a novel form of muscular dystrophy. Nat Genet 17: 318-323.
150. McMahan UJ, Sanes JR, Marshall LM. 1978. Cholinesterase is associated with the basal lamina at the neuromuscular junction. Nature 271: 172-174.
151. Meier T, Marangi PA, Moll J, Hauser DM, Brenner HR, Ruegg MA. 1998a. A minigene of neural agrin encoding the laminin-binding and acetylcholine receptor-aggregating domains is sufficient to induce postsynaptic differentiation in muscle fibres. Eur J Neurosci 10: 3141-3152.
152. Meier T, Masciulli F, Moore C, Schoumacher F, Eppenberger U, Denzer AJ, Jones G, et al. 1998b. Agrin can mediate acetylcholine receptor gene expression in muscle by aggregation of muscle-derived neuregulins. J Cell Biol 141: 715-726.
153. Michele DE, Barresi R, Kanagawa M, Saito F, Cohn RD, Satz JS, Dollar J, et al. 2002. Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature 418: 417-422.
154. Michele DE, Campbell KP. 2003. Dystrophin-glycoprotein complex: Post-translational processing and dystroglycan function. J Biol Chem 278: 15457-15460.
155. Miner JH. 2011. Glomerular basement membrane composition and the filtration barrier. Pediatr Nephrol 26: 1413-1417.
156. Miner JH, Cunningham J, Sanes JR. 1998. Roles for laminin in embryogenesis: Exencephaly, syndactyly, and placentopathy in mice lacking the laminin alpha5 chain. J Cell Biol 143: 1713-1723.
157. Miner JH, Go G, Cunningham J, Patton BL, Jarad G. 2006. Transgenic isolation of skeletal muscle and kidney defects in laminin beta2 mutant mice: Implications for Pierson syndrome. Development 133: 967-975.
158. Miner JH, Sanes JR. 1994. Collagen IV alpha 3, alpha 4, and alpha 5 chains in rodent basal laminae: Sequence, distribution, association with laminins, and developmental switches. J Cell Biol 127: 879-891.
159. Misgeld T, Kummer TT, Lichtman JW, Sanes JR. 2005. Agrin promotes synaptic differentiation by counteracting an inhibitory effect of neurotransmitter. Proc Natl Acad Sci USA 102: 11088-11093.
160. Mittaud P, Camilleri AA, Willmann R, Erb-Vogtli S, Burden SJ, Fuhrer C. 2004. A single pulse of agrin triggers a pathway that acts to cluster acetylcholine receptors. Mol Cell Biol 24: 7841-7854.
161. Moll J, Barzaghi P, Lin S, Bezakova G, Lochmuller H, Engvall E, Muller U, et al. 2001. An agrin minigene rescues dystrophic symptoms in a mouse model for congenital muscular dystrophy. Nature 413: 302-307.
162. Montanaro F, Carbonetto S, Campbell KP, Lindenbaum M. 1995. Dystroglycan expression in the wild type and mdx mouse neural retina: Synaptic colocalization with dystrophin, dystrophin-related protein but not laminin. J Neurosci Res 42: 528-538.
163. Moscoso LM, Chu GC, Gautam M, Noakes PG, Merlie JP, Sanes JR. 1995. Synapse-associated expression of an acetylcholine receptor-inducing protein. ARIA/heregulin, and its putative receptors Erb B2 and Erb B3, in developing mammalian muscle Dev Biol 172: 158-169.
164. Moscoso LM, Cremer H, Sanes JR. 1998. Organization and reorganization of neuromuscular junctions in mice lacking neural cell adhesion molecule, tenascin-C, or fibroblast growth factor-5. J Neurosci 18: 1465-1477.
165. 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.
166. Nguyen HH, Jayasinha V, Xia B, Hoyte K, Martin PT. 2002. Overexpression of the cytotoxic T cell GalNAc transferase in skeletal muscle inhibits muscular dystrophy in mdx mice. Proc Natl Acad Sci USA 99: 5616-5621.
167. Nishimune H, Sanes JR, Carlson SS. 2004. A synaptic laminin-calcium channel interaction organizes active zones in motor nerve terminals. Nature 432: 580-587.
168. Nishimune H, Valdez G, Jarad G, Moulson CL, Muller U, Miner JH, Sanes JR. 2008. Laminins promote postsynaptic maturation by an autocrine mechanism at the neuromuscular junction. J Cell Biol 182: 1201-1215.
169. Nitkin RM, Smith MA, Magill C, Fallon JR, Yao YM, Wallace BG, McMahan UJ. 1987. Identification of agrin, a synaptic organizing protein from Torpedo electric organ. J Cell Biol 105: 2471-2478.
170. Noakes PG, Gautam M, Mudd J, Sanes JR, Merlie JP. 1995. Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin beta 2. Nature 374: 258-262.
171. Ohlendieck K, Ervasti 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.
172. Okada K, Inoue A, Okada M, Murata Y, Kakuta S, Jigami T, Kubo S, et al. 2006. The muscle protein Dok-7 is essential for neuromuscular synaptogenesis. Science 312: 1802-1805.
173. Panzer JA, Gibbs SM, Dosch R, Wagner D, Mullins MC, Granato M, Balice-Gordon RJ. 2005. Neuromuscular synaptogenesis in wild-type and mutant zebrafish. Dev Biol 285: 340-357.
174. Patton BL, Chiu AY, Sanes JR. 1998. Synaptic laminin prevents glial entry into the synaptic cleft. Nature 393: 698-701.
175. Patton BL, Connoll AM, Martin PT, Cunningham JM, Mehta S, Pestronk A, Miner JH, et al. 1999. Distribution of ten laminin chains in dystrophic and regenerating muscles. Neuromuscul Disord 9: 423-433.
176. Patton BL, Cunningham JM, Thyboll J, Kortesmaa J, Westerblad H, Edstrom L, Tryggvason K, et al. 2001. Properly formed but improperly localized synaptic specializations in the absence of laminin alpha4. Nat Neurosci 4: 597-604.
177. Patton BL, Miner JH, Chiu AY, Sanes JR. 1997. Distribution and function of laminins in the neuromuscular system of developing, adult, and mutant mice. J Cell Biol 139: 1507-1521.
178. Peng HB, Ali AA, Daggett DF, Rauvala H, Hassell JR, Smalheiser NR. 1998. The relationship between perlecan and dystroglycan and its implication in the formation of the neuromuscular junction. Cell Adhes Commun 5: 475-489.
179. Peters MF, Adams ME, Froehner SC. 1997. Differential association of syntrophin pairs with the dystrophin complex. J Cell Biol 138: 81-93.
180. Peters MF, Sadoulet-Puccio HM, Grady MR, Kramarcy NR, Kunkel LM, Sanes JR, Sealock R, et al. 1998. Differential membrane localization and intermolecular associations of alpha-dystrobrevin isoforms in skeletal muscle. J Cell Biol 142: 1269-1278.
181. Ponomareva ON, Ma H, Vock VM, Ellerton EL, Moody SE, Dakour R, Chodosh LA, et al. 2006. Defective neuromuscular synaptogenesis in mice expressing constitutively active ErbB2 in skeletal muscle fibers. Mol Cell Neurosci 31: 334-345.
182. Poschl E, Mayer U, Stetefeld J, Baumgartner R, Holak TA, Huber R, Timpl R. 1996. Site-directed mutagenesis and structural interpretation of the nidogen binding site of the laminin gamma1 chain. EMBO J 15: 5154-5159.
183. Rafael JA, Tinsley JM, Potter AC, Deconinck AE, Davies KE. 1998. Skeletal muscle-specific expression of a utrophin transgene rescues utrophin-dystrophin deficient mice. Nat Genet 19: 79-82.
184. Reinhardt D, Mann K, Nischt R, Fox JW, Chu ML, Krieg T, Timpl R. 1993. Mapping of nidogen binding sites for collagen type IV, heparan sulfate proteoglycan, and zinc. J Biol Chem 268: 10881-10887.
185. 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.
186. Rooney JE, Gurpur PB, Burkin DJ. 2009. Laminin-111 protein therapy prevents muscle disease in the mdx mouse model for Duchenne muscular dystrophy. Proc Natl Acad Sci USA 106: 7991-7996.
187. Rooney JE, Gurpur PB, Yablonka-Reuveni Z, Burkin DJ. 2009. Laminin-111 restores regenerative capacity in a mouse model for alpha7 integrin congenital myopathy. Am J Pathol 174: 256-264.
188. Rotundo RL. 2003. Expression and localization of acetylcholinesterase at the neuromuscular junction. J Neurocytol 32: 743-766.
189. Ruegg MA, Tsim KW, Horton SE, Kroger S, Escher G, Gensch EM, McMahan UJ. 1992. The agrin gene codes for a family of basal lamina proteins that differ in function and distribution. Neuron 8: 691-699.
190. Ruggiu M, Herbst R, Kim N, Jevsek M, Fak JJ, Mann MA, Fischbach G, et al. 2009. Rescuing Z+ agrin splicing in Nova null mice restores synapse formation and unmasks a physiologic defect in motor neuron firing. Proc Natl Acad Sci USA 106: 3513-3518.
191. Rupp F, Payan DG, Magill-Solc C, Cowan DM, Scheller RH. 1991. Structure and expression of a rat agrin. Neuron 6: 811-823.
192. Sadasivam G, Willmann R, Lin S, Erb-Vogtli S, Kong XC, Ruegg MA, Fuhrer C. 2005. Src-family kinases stabilize the neuromuscular synapse in vivo via protein interactions, phosphorylation, and cytoskeletal linkage of acetylcholine receptors. J Neurosci 25: 10479-10493.
193. Sandrock AWJr, Dryer SE, Rosen KM, Gozani SN, Kramer R, Theill LE, Fischbach GD. 1997. Maintenance of acetylcholine receptor number by neuregulins at the neuromuscular junction in vivo. Science 276: 599-603.
194. Sandrock AWJr, Goodearl AD, Yin QW, Chang D, Fischbach GD. 1995. ARIA is concentrated in nerve terminals at neuromuscular junctions and at other synapses. J Neurosci 15: 6124-6136.
195. Sanes JR. 2003. The basement membrane/basal lamina of skeletal muscle. J Biol Chem 278: 12601-12604.
196. Sanes JR, Apel ED, Burgess RW, Emerson RB, Feng G, Gautam M, Glass D, et al. 1998. Development of the neuromuscular junction: Genetic analysis in mice. J Physiol Paris 92: 167-172.
197. Sanes JR, Engvall E, Butkowski R, Hunter DD. 1990. Molecular heterogeneity of basal laminae: Isoforms of laminin and collagen IV at the neuromuscular junction and elsewhere. J Cell Biol 111: 1685-1699.
198. Sanes JR, Hall ZW. 1979. Antibodies that bind specifically to synaptic sites on muscle fiber basal lamina. J Cell Biol 83: 357-370.
199. Sanes JR, Lichtman JW. 1999. Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22: 389-442.
200. Sanes JR, Lichtman JW. 2001. Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci 2: 791-805.
201. Sanes JR, Marshall LM, McMahan UJ. 1978. Reinnervation of muscle fiber basal lamina after removal of myofibers. Differentiation of regenerating axons at original synaptic sites. J Cell Biol 78: 176-198.
202. Sanes JR, Schachner M, Covault J. 1986. Expression of several adhesive macromolecules (N-CAM. L1, J1, NILE, uvomorulin, laminin, fibronectin, and a heparan sulfate proteoglycan) in embryonic, adult, and denervated adult skeletal muscle J Cell Biol 102: 420-431.
203. Sann SB, Xu L, Nishimune H, Sanes JR, Spitzer NC. 2008. Neurite outgrowth and in vivo sensory innervation mediated by a Ca(V)2.2-laminin beta 2 stop signal. J Neurosci 28: 2366-2374.
204. Schaeffer L, de Kerchove d'Exaerde A, Changeux JP. 2001. Targeting transcription to the neuromuscular synapse. Neuron 31: 15-22.
205. Schwander M, Leu M, Stumm M, Dorchies OM, Ruegg UT, Schittny J, Muller U. 2003. Beta1 integrins regulate myoblast fusion and sarcomere assembly. Dev Cell 4: 673-685.
206. Schwander M, Shirasaki R, Pfaff SL, Muller U. 2004. Beta1 integrins in muscle, but not in motor neurons, are required for skeletal muscle innervation. J Neurosci 24: 8181-8191.
207. Scotton P, Bleckmann D, Stebler M, Sciandra F, Brancaccio A, Meier T, Stetefeld J, et al. 2006. Activation of muscle-specific receptor tyrosine kinase and binding to dystroglycan are regulated by alternative mRNA splicing of agrin. J Biol Chem 281: 36835-36845.
208. Sealock R, Wray BE, Froehner SC. 1984. Ultrastructural localization of the Mr 43, 000 protein and the acetylcholine receptor in Torpedo postsynaptic membranes using monoclonal antibodies. J Cell Biol 98: 2239-2244.
209. Sigoillot SM, Bourgeois F, Lambergeon M, Strochlic L, Legay C. 2010. ColQ controls postsynaptic differentiation at the neuromuscular junction. J Neurosci 30: 13-23.
210. Smith CL, Mittaud P, Prescott ED, Fuhrer C, Burden SJ. 2001. Src. Fyn, and Yes are not required for neuromuscular synapse formation but are necessary for stabilization of agrin-induced clusters of acetylcholine receptors J Neurosci 21: 3151-3160.
211. Snellman A, Keranen MR, Hagg PO, Lamberg A, Hiltunen JK, Kivirikko KI, Pihlajaniemi T. 2000. Type XIII collagen forms homotrimers with three triple helical collagenous domains and its association into disulfide-bonded trimers is enhanced by prolyl 4-hydroxylase. J Biol Chem 275: 8936-8944.
212. Sobel A, Heidmann T, Changeux JP. 1977. [Purification of a protein binding quinacrine and histrionicotoxin from membrane fragments rich in cholinergic receptors in Torpedo marmorata]. C R Acad Sci Hebd Seances Acad Sci D 285: 1255-1258.
213. Son YJ, Scranton TW, Sunderland WJ, Baek SJ, Miner JH, Sanes JR, Carlson SS. 2000. The synaptic vesicle protein SV2 is complexed with an alpha5-containing laminin on the nerve terminal surface. J Biol Chem 275: 451-460.
214. Song WK, Wang W, Foster RF, Bielser DA, Kaufman SJ. 1992. H36-alpha 7 is a novel integrin alpha chain that is developmentally regulated during skeletal myogenesis. J Cell Biol 117: 643-657.
215. Sugita S, Saito F, Tang J, Satz J, Campbell K, Sudhof TC. 2001. A stoichiometric complex of neurexins and dystroglycan in brain. J Cell Biol 154: 435-445.
216. Sund M, Vaisanen T, Kaukinen S, Ilves M, Tu H, Autio-Harmainen H, Rauvala H, et al. 2001. Distinct expression of type XIII collagen in neuronal structures and other tissues during mouse development. Matrix Biol 20: 215-231.
217. Sunesen M, Changeux JP. 2003. Transcription in neuromuscular junction formation: Who turns on whom? J Neurocytol 32: 677-684.
218. Talts JF, Andac Z, Gohring W, Brancaccio A, Timpl R. 1999. Binding of the G domains of laminin alpha1 and alpha2 chains and perlecan to heparin, sulfatides, alpha-dystroglycan and several extracellular matrix proteins. EMBO J 18: 863-870.
219. Talts JF, Sasaki T, Miosge N, Gohring W, Mann K, Mayne R, Timpl R. 2000. Structural and functional analysis of the recombinant G domain of the laminin alpha4 chain and its proteolytic processing in tissues. J Biol Chem 275: 35192-35199.
220. Tang H, Macpherson P, Argetsinger LS, Cieslak D, Suhr ST, Carter-Su C, Goldman D. 2004. CaM kinase II-dependent phosphorylation of myogenin contributes to activity-dependent suppression of nAChR gene expression in developing rat myotubes. Cell Signal 16: 551-563.
221. Tang H, Macpherson P, Marvin M, Meadows E, Klein WH, Yang XJ, Goldman D. 2009. A histone deacetylase 4/myogenin positive feedback loop coordinates denervation-dependent gene induction and suppression. Mol Biol Cell 20: 1120-1131.
222. Tang H, Veldman MB, Goldman D. 2006. Characterization of a muscle-specific enhancer in human MuSK promoter reveals the essential role of myogenin in controlling activity-dependent gene regulation. J Biol Chem 281: 3943-3953.
223. Till JH, Becerra M, Watty A, Lu Y, Ma Y, Neubert TA, Burden SJ, et al. 2002. Crystal structure of the MuSK tyrosine kinase: Insights into receptor autoregulation. Structure 10: 1187-1196.
224. Tinsley J, Deconinck N, Fisher R, Kahn D, Phelps S, Gillis JM, Davies K. 1998. Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat Med 4: 1441-1444.
225. Torres JC, Inestrosa NC. 1983. Heparin solubilizes asymmetric acetylcholinesterase from rat neuromuscular junction. FEBS letters 154: 265-268.
226. Trachtenberg JT, Thompson WJ. 1996. Schwann cell apoptosis at developing neuromuscular junctions is regulated by glial growth factor. Nature 379: 174-177.
227. Tsen G, Halfter W, Kroger S, Cole GJ. 1995. Agrin is a heparan sulfate proteoglycan. J Biol Chem 270: 3392-3399.
228. Tsim KW, Ruegg MA, Escher G, Kroger S, McMahan UJ. 1992. cDNA that encodes active agrin. Neuron 8: 677-689.
229. Ushkaryov YA, Petrenko AG, Geppert M, Sudhof TC. 1992. Neurexins: Synaptic cell surface proteins related to the alpha-latrotoxin receptor and laminin. Science 257: 50-56.
230. Valdez G, Tapia JC, Kang H, Clemenson GDJr, Gage FH, Lichtman JW, Sanes JR. 2010. Attenuation of age-related changes in mouse neuromuscular synapses by caloric restriction and exercise. Proc Natl Acad Sci USA 107: 14863-14868.
231. van der Flier A, Gaspar AC, Thorsteinsdottir S, Baudoin C, Groeneveld E, Mummery CL, Sonnenberg A. 1997. Spatial and temporal expression of the beta1D integrin during mouse development. Dev Dyn 210: 472-486.
232. Voermans NC, Bonnemann CG, Huijing PA, Hamel BC, van Kuppevelt TH, de Haan A, Schalkwijk J, et al. 2008. Clinical and molecular overlap between myopathies and inherited connective tissue diseases. Neuromuscul Disord 18: 843-856.
233. Voermans NC, Verrijp K, Eshuis L, Balemans MC, Egging D, Sterrenburg E, van Rooij IA, et al. 2011. Mild muscular features in Tenascin-X knockout mice: A model of Ehlers-Danlos syndrome. Connective tissue research.
234. Wallace BG, Nitkin RM, Reist NE, Fallon JR, Moayeri NN, McMahan UJ. 1985. Aggregates of acetylcholinesterase induced by acetylcholine receptor-aggregating factor. Nature 315: 574-577.
235. Wang J, Jing Z, Zhang L, Zhou G, Braun J, Yao Y, Wang ZZ. 2003. Regulation of acetylcholine receptor clustering by the tumor suppressor APC. Nat Neurosci 6: 1017-1018.
236. Watty A, Burden SJ. 2002. MuSK glycosylation restrains MuSK activation and acetylcholine receptor clustering. J Biol Chem 277: 50457-50462.
237. Watty A, Neubauer G, Dreger M, Zimmer M, Wilm M, Burden SJ. 2000. The in vitro and in vivo phosphotyrosine map of activated MuSK. Proc Natl Acad Sci USA 97: 4585-4590.
238. Weatherbee SD, Anderson KV, Niswander LA. 2006. LDL-receptor-related protein 4 is crucial for formation of the neuromuscular junction. Development 133: 4993-5000.
239. Weston C, Gordon C, Teressa G, Hod E, Ren XD, Prives J. 2003. Cooperative regulation by Rac and Rho of agrin-induced acetylcholine receptor clustering in muscle cells. J Biol Chem 278: 6450-6455.
240. Williamson RA, Henry MD, Daniels KJ, Hrstka RF, Lee JC, Sunada Y, Ibraghimov-Beskrovnaya O, et al. 1997. Dystroglycan is essential for early embryonic development: Disruption of Reichert's membrane in Dag1-null mice. Hum Mol Genet 6: 831-841.
241. Wlodarczyk J, Mukhina I, Kaczmarek L, Dityatev A. 2011. Extracellular matrix molecules, their receptors, and secreted proteases in synaptic plasticity. Dev Neurobiol 71: 1040-1053.
242. Woldeyesus MT, Britsch S, Riethmacher D, Xu L, Sonnenberg-Riethmacher E, Abou-Rebyeh F, Harvey R, et al. 1999. Peripheral nervous system defects in erbB2 mutants following genetic rescue of heart development. Genes Dev 13: 2538-2548.
243. Wu H, Xiong WC, Mei L. 2010. To build a synapse: Signaling pathways in neuromuscular junction assembly. Development 137: 1017-1033.
244. Xia B, Hoyte K, Kammesheidt A, Deerinck T, Ellisman M, Martin PT. 2002. Overexpression of the CT GalNAc transferase in skeletal muscle alters myofiber growth, neuromuscular structure, and laminin expression. Dev Biol 242: 58-73.
245. Xu R, Chandrasekharan K, Yoon JH, Camboni M, Martin PT. 2007. Overexpression of the cytotoxic T cell (CT) carbohydrate inhibits muscular dystrophy in the dyW mouse model of congenital muscular dystrophy 1A. Am J Pathol 171: 181-199.
246. Xu R, DeVries S, Camboni M, Martin PT. 2009. Overexpression of Galgt2 reduces dystrophic pathology in the skeletal muscles of alpha sarcoglycan-deficient mice. Am J Pathol 175: 235-247.
247. Yang D, Bierman J, Tarumi YS, Zhong YP, Rangwala R, Proctor TM, Miyagoe-Suzuki Y, et al. 2005. Coordinate control of axon defasciculation and myelination by laminin-2 and -8. J Cell Biol 168: 655-666.
248. Yang X, Arber S, William C, Li L, Tanabe Y, Jessell TM, Birchmeier C, et al. 2001. Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 30: 399-410.
249. Yang X, Li W, Prescott ED, Burden SJ, Wang JC. 2000. DNA topoisomerase IIbeta and neural development. Science 287: 131-134.
250. Yoon JH, Chandrasekharan K, Xu R, Glass M, Singhal N, Martin PT. 2009. The synaptic CT carbohydrate modulates binding and expression of extracellular matrix proteins in skeletal muscle: Partial dependence on utrophin. Mol Cell Neurosci 41: 448-463.
251. Yurchenco PD, Amenta PS, Patton BL. 2004. Basement membrane assembly, stability and activities observed through a developmental lens. Matrix Biol 22: 521-538.
252. Yurchenco PD, O'Rear JJ. 1994. Basal lamina assembly. Curr Opin Cell Biol 6: 674-681.
253. Yurchenco PD, Patton BL. 2009. Developmental and pathogenic mechanisms of basement membrane assembly. Curr Pharm Des 15: 1277-1294.
254. Zhang B, Luo S, Wang Q, Suzuki T, Xiong WC, Mei L. 2008. LRP4 serves as a coreceptor of agrin. Neuron 60: 285-297.
255. Zhao XT, Qian YK, Chan AW, Madhavan R, Peng HB. 2007. Regulation of ACh receptor clustering by the tyrosine phosphatase Shp2. Dev Neurobiol 67: 1789-1801.
256. Zhu D, Yang Z, Luo Z, Luo S, Xiong WC, Mei L. 2008. Muscle-specific receptor tyrosine kinase endocytosis in acetylcholine receptor clustering in response to agrin. J Neurosci 28: 1688-1696.
257. Zhu X, Lai C, Thomas S, Burden SJ. 1995. Neuregulin receptors, erbB3 and erbB4, are localized at neuromuscular synapses. EMBO J 14: 5842-5848.
258. Ziober BL, Vu MP, Waleh N, Crawford J, Lin CS, Kramer RH. 1993. Alternative extracellular and cytoplasmic domains of the integrin alpha 7 subunit are differentially expressed during development. J Biol Chem 268: 26773-26783.