Crosstalk between Agrin and Wnt signaling pathways in development of vertebrate neuromuscular junction

Developmental Neurobiology

Volumn 74, Issue 8, 2014, Pages 828-838

  Barik, Arnab ^a   Zhang, Bin ^a   Sohal, Gurkirpal S ^a   Xiong, Wen Cheng ^a,b   Mei, Lin ^a,b  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Aneural clusters; LRP4; Musk; NMJ; WNT

Indexed keywords

AGRIN; BETA CATENIN; UNCLASSIFIED DRUG; WNT PROTEIN; WNT10B PROTEIN; WNT11 PROTEIN; WNT16 PROTEIN; WNT3A PROTEIN; WNT7A PROTEIN; WNT8A PROTEIN; WNT9A PROTEIN; WNT9B PROTEIN;

ARTICLE; CHOLINERGIC SYNAPSE; MOTONEURON; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; VERTEBRATE; WNT SIGNALING PATHWAY; ANIMAL; CELL DIFFERENTIATION; HUMAN; METABOLISM; PHYSIOLOGY; SYNAPSE;

AGRIN; ANIMALS; CELL DIFFERENTIATION; HUMANS; NEUROMUSCULAR JUNCTION; SYNAPSES; VERTEBRATES; WNT SIGNALING PATHWAY;

EID: 84903819812     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.22190     Document Type: Article

References (80)

1. 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.
2. Banerjee S, Gordon L, Donn TM, Berti C, Moens CB, Burden SJ, Granato M. 2011. A novel role for MuSK and non-canonical Wnt signaling during segmental neural crest cell migration. Development 138:3287-3296.
3. Barik A. Xiong W-C, Mei L. 2012. MuSK: A Kinase Critical for the Formation and Maintenance of the Neuromuscular Junction. In: Mukai H (eds), Protein Kinase Technologies: Neuromethods. Humana Press. 203-217.
4. Barth AI, Caro-Gonzalez HY, Nelson WJ. 2008. Role of adenomatous polyposis coli (APC) and microtubules in directional cell migration and neuronal polarization. Semin Cell Dev Biol 19:245-251.
5. Campagna JA, Ruegg MA, Bixby JL. 1995. Agrin is a differentiation-inducing "stop signal" for motoneurons in vitro. Neuron 15:1365-1374.
6. Cheusova T, Khan MA, Schubert SW, Gavin AC, Buchou T, Jacob G, Sticht H, Allende J, Boldyreff B, Brenner HR, Hashemolhosseini S. 2006. Casein kinase 2-dependent serine phosphorylation of MuSK regulates acetylcholine receptor aggregation at the neuromuscular junction. Genes Dev 20:1800-1816.
7. Ciani L, Salinas PC. 2008. From neuronal activity to the actin cytoskeleton: A role for CaMKKs and betaPIX in spine morphogenesis. Neuron 57:3-4.
8. Clevers H, Nusse R. 2012. Wnt/beta-catenin signaling and disease. Cell 149:1192-1205.
9. Cossu G, Borello U. 1999. Wnt signaling and the activation of myogenesis in mammals. EMBO J 18:6867-6872.
10. DeChiara TM, Bowen DC, Valenzuela DM, Simmons MV, Poueymirou WT, Thomas S, Kinetz E, Compton 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.
11. Dobbins GC, Luo S, Yang Z, Xiong WC, Mei L. 2008. alpha-Actinin interacts with Rapsyn in Agrin-stimulated AChR clustering. Mol Brain 1:18.
12. Etienne-Manneville S, Manneville JB, Nicholls S, Ferenczi MA, Hall A. 2005. Cdc42 and Par6-PKCzeta regulate the spatially localized association of Dlg1 and APC to control cell polarization. J Cell Biol 170:895-901.
13. Froehner SC, Scotland PB, Patrick J. 1990. The postsynaptic 43K protein clusters muscle nicotinic acetylcholine receptors in Xenopus oocytes. Neuron 5:403-410.
14. 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.
15. 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.
16. 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.
17. Gordon LR, Gribble KD, Syrett CM, Granato M. 2012. Initiation of synapse formation by Wnt-induced MuSK endocytosis. Development 139:1023-1033.
18. Gordon MD, Nusse R. 2006. Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors. J Biol Chem 281:22429-22433.
19. Hall AC, Lucas FR, Salinas PC. 2000. Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 100:525-535.
20. Hamuro J, Higuchi O, Okada K, Ueno M, Iemura S, Natsume T, Spearman H, et al. 2008. Mutations causing DOK7 congenital myasthenia ablate functional motifs in Dok-7. J Biol Chem 283:5518-5524.
21. Hart M, Concordet JP, Lassot I, Albert I, del los Santos R, Durand H, Perret C, et al. 1999. The F-box protein beta-TrCP associates with phosphorylated beta-catenin and regulates its activity in the cell. Curr Biol 9:207-210.
22. He X, Semenov M, Tamai K, Zeng X. 2004. LDL receptor-related proteins 5 and 6 in Wnt/beta-catenin signaling: Arrows point the way. Development 131:1663-1677.
23. Henriquez JP, Webb A, Bence M, Bildsoe H, Sahores M, Hughes SM, Salinas PC. 2008. Wnt signaling promotes AChR aggregation at the neuromuscular synapse in collaboration with Agrin. Proc Natl Acad Sci USA 105:18812-18817.
24. Herz J, Willnow TE. 1994. Functions of the LDL receptor gene family. Ann NY Acad Sci 737:14-19.
25. Jing L, Gordon LR, Shtibin E, Granato M. 2010. Temporal and spatial requirements of unplugged/MuSK function during zebrafish neuromuscular development. PLoS One 5:e8843.
26. Jing L, Lefebvre JL, Gordon LR, Granato M. 2009. Wnt signals organize synaptic prepattern and axon guidance through the zebrafish unplugged/MuSK receptor. Neuron 61:721-733.
27. 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.
28. Kim SE, Huang H, Zhao M, Zhang X, Zhang A, Semonov MV, MacDonald BT, 2013. "Wnt stabilization of beta-catenin reveals principles for morphogen receptor-scaffold assemblies." Science 340:867-870.
29. Klassen MP, Shen K. 2007. Wnt signaling positions neuromuscular connectivity by inhibiting synapse formation in C. elegans. Cell 130:704-716.
30. Koles K, Nunnari J, Korkut C, Barria R, Brewer C, Li Y, Leszyk J, et al. 2012. Mechanism of evenness interrupted (Evi)-exosome release at synaptic boutons. J Biol Chem 287:16820-16834.
31. Korkut C, Ataman B, Ramachandran P, Ashley J, Barria R, Gherbesi N, Budnik V. 2009. Trans-synaptic transmission of vesicular Wnt signals through Evi/Wntless. Cell 139:393-404.
32. Korkut C, Budnik V. 2009. WNTs tune up the neuromuscular junction. Nat Rev Neurosci 10:627-634.
33. Kuroda K, Kuang S, Taketo MM, Rudnicki MA. 2013. Canonical Wnt signaling induces BMP-4 to specify slow myofibrogenesis of fetal myoblasts. Skelet Muscle 3:5.
34. Li XM, Dong XP, Luo SW, Zhang B, Lee DH, Ting AK, Neiswender H, et al. 2008. Retrograde regulation of motoneuron differentiation by muscle beta-catenin. Nat Neurosci 11:262-268.
35. Liu CY, Zha ZY, Zhou X, Zhang H, Huang W, Zhao D, Li T, et al. 2010. The hippo tumor pathway promotes TAZ degradation by phosphorylating a phosphodegron and recruiting the SCF{beta}-TrCP E3 ligase. J Biol Chem 285:37159-37169.
36. Liu Y, Sugiura Y, Wu F, Mi W, Taketo MM, Cannon S, Carroll T, et al. 2012. beta-Catenin stabilization in skeletal muscles, but not in motor neurons, leads to aberrant motor innervation of the muscle during neuromuscular development in mice. Dev Biol 366:255-267.
37. Logan CY, Nusse R. 2004. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781-810.
38. 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.
39. MacDonald BT, Tamai K, He X. 2009. Wnt/beta-catenin signaling: Components, mechanisms, and diseases. Dev Cell 17:9-26.
40. Masiakowski P, Carroll RD. 1992. A novel family of cell surface receptors with tyrosine kinase-like domain. J Biol Chem 267:26181-26190.
41. Masiakowski P, Yancopoulos GD. 1998. The Wnt receptor CRD domain is also found in MuSK and related orphan receptor tyrosine kinases. Curr Biol 8:R407.
42. Mathew D, Ataman B, Chen J, Zhang Y, Cumberledge S, Budnik V. 2005. Wingless signaling at synapses is through cleavage and nuclear import of receptor DFrizzled2. Science 310:1344-1347.
43. McMahan UJ. 1990. The Agrin hypothesis. Cold Spring Harb Symp Quant Biol 55:407-418.
44. Nathke I. 2004. APC at a glance. J Cell Sci 117:4873-4875.
45. 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.
46. 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.
47. Packard M, Koo ES, Gorczyca M, Sharpe J, Cumberledge S, Budnik V. 2002. The Drosophila Wnt, wingless, provides an essential signal for pre- and postsynaptic differentiation. Cell 111:319-330.
48. Reist NE, Werle MJ, McMahan UJ. 1992. Agrin released by motor neurons induces the aggregation of acetylcholine receptors at neuromuscular junctions. Neuron 8:865-868.
49. Ruegg MA, Bixby JL. 1998. Agrin orchestrates synaptic differentiation at the vertebrate neuromuscular junction. Trends Neurosci 21:22-27.
50. 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.
51. Sahores M, Gibb A, Salinas PC. 2010. Frizzled-5, a receptor for the synaptic organizer Wnt7a, regulates activity-mediated synaptogenesis. Development 137:2215-2225.
52. Salinas PC, Zou Y. 2008. Wnt signaling in neural circuit assembly. Annu Rev Neurosci 31:339-358.
53. Sansom OJ, Reed KR, Hayes AJ, Ireland H, Brinkmann H, Newton IP, Batlle E, et al. 2004. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev 18:1385-1390.
54. 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.
55. Segditsas S, Tomlinson I. 2006. Colorectal cancer and genetic alterations in the Wnt pathway. Oncogene 25:7531-7537.
56. Simons M, Mlodzik M. 2008. Planar cell polarity signaling: From fly development to human disease. Annu Rev Genet 42:517-540.
57. Sohal GS. 1995. Sixth Annual Stuart Reiner Memorial Lecture: Embryonic development of nerve and muscle. Muscle Nerve 18:2-14.
58. Speese SD, Budnik V. 2007. Wnts: Up-and-coming at the synapse. Trends Neurosci 30:268-275.
59. Stiegler AL, Burden SJ, Hubbard SR. 2006. Crystal structure of the Agrin-responsive immunoglobulin-like domains 1 and 2 of the receptor tyrosine kinase MuSK. J Mol Biol 364:424-433.
60. Strochlic L, Falk J, Goillot E, Sigoillot S, Bourgeois F, Delers P, Rouviere J, et al. 2012. Wnt4 participates in the formation of vertebrate neuromuscular junction. PLoS One 7:e29976.
61. Tsim KW, Ruegg MA, Escher G, Kroger S, McMahan UJ. 1992. cDNA that encodes active Agrin. Neuron 8:677-689.
62. Valenzuela DM, Stitt TN, DiStefano PS, Rojas E, Mattsson K, Compton DL, Nunez L, et al. 1995. Receptor tyrosine kinase specific for the skeletal muscle lineage: Expression in embryonic muscle, at the neuromuscular junction, and after injury. Neuron 15:573-584.
63. 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.
64. Wang J, Ruan NJ, Qian L, Lei WL, Chen F, Luo ZG. 2008. Wnt/beta-catenin signaling suppresses Rapsyn expression and inhibits acetylcholine receptor clustering at the neuromuscular junction. J Biol Chem 283:21668-21675.
65. Weatherbee SD, Anderson KV, Niswander LA. 2006. LDL-receptor-related protein 4 is crucial for formation of the neuromuscular junction. Development 133:4993-5000.
66. 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.
67. Weston C, Yee B, Hod E, Prives J. 2000. Agrin-induced acetylcholine receptor clustering is mediated by the small guanosine triphosphatases Rac and Cdc42. J Cell Biol 150:205-212.
68. Weston CA, Teressa G, Weeks BS, Prives J. 2007. Agrin and laminin induce acetylcholine receptor clustering by convergent, Rho GTPase-dependent signaling pathways. J Cell Sci 120:868-875.
69. Wu H, Lu Y, Barik A, Joseph A, Taketo MM, Xiong WC, Mei L. 2012. beta-Catenin gain of function in muscles impairs neuromuscular junction formation. Development 139:2392-2404.
70. Wu H, Xiong WC, Mei L. 2010. To build a synapse: Signaling pathways in neuromuscular junction assembly. Development 137:1017-1033.
71. Yumoto N, Kim N, Burden SJ. 2012. Lrp4 is a retrograde signal for presynaptic differentiation at neuromuscular synapses. Nature 489:438-442.
72. Zhang B, Liang C, Bates R, Yin Y, Xiong WC, Mei L. 2012. Wnt proteins regulate acetylcholine receptor clustering in muscle cells. Mol Brain 5:7.
73. Zhang B, Luo S, Dong XP, Zhang X, Liu C, Luo Z, Xiong WC, Mei L. 2007. Beta-catenin regulates acetylcholine receptor clustering in muscle cells through interaction with Rapsyn. J Neurosci 27:3968-3973.
74. Zhang B, Luo S, Wang Q, Suzuki T, Xiong WC, Mei L. 2008. LRP4 serves as a coreceptor of Agrin. Neuron 60:285-297.
75. Zhang B, Luo S, Dong XP, Zhang X, Liu C, Luo Z, Xiong WC, et al. Beta-catenin regulates acetylcholine receptor clustering in muscle cells through interaction with Rapsyn. J Neurosci 27:3968-3973.
76. Zhang B, Xiong WC, Mei L. 2009. Get ready to Wnt: Prepatterning in neuromuscular junction formation. Dev Cell 16:325-327.
77. Zhang J, Granato M. 2000. The zebrafish unplugged gene controls motor axon pathway selection. Development 127:2099-2111.
78. Zhang J, Lefebvre JL, Zhao S, Granato M. 2004. Zebrafish unplugged reveals a role for muscle-specific kinase homologs in axonal pathway choice. Nat Neurosci 7:1303-1309.
79. Zong Y, Jin R. 2012. Structural mechanisms of the Agrin-LRP4-MuSK signaling pathway in neuromuscular junction differentiation. Cell Mol Life Sci 70:3077-3088.
80. Zong Y, Zhang B, Gu S, Lee K, Zhou J, Yao G, Figueiredo D, et al. 2012. Structural basis of Agrin-LRP4-MuSK signaling. Genes Dev 26:247-258.