Agrin regulates growth cone turning of Xenopus spinal motoneurons

Development

Volumn 132, Issue 19, 2005, Pages 4309-4316

  Xu, Xiaohua ^a   Fu, Amy K Y ^b   Ip, Fanny C F ^b   Wu, Chien Ping ^a   Duan, Shumin ^a   Poo, Mu Ming ^a,c   Yuan, Xiao Bing ^a   Ip, Nancy Y ^a,b  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Axon guidance; Calcium signaling; Neurite outgrowth; PI3 kinase; Rac1

Indexed keywords

AGRIN; NEUTRALIZING ANTIBODY; PHOSPHATIDYLINOSITOL 3 KINASE; RAC1 PROTEIN;

ANIMAL CELL; ARTICLE; CALCIUM SIGNALING; CELL CULTURE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; EXTRACELLULAR SPACE; GROWTH CONE; INCUBATION TIME; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SPINAL CORD NERVE CELL; XENOPUS LAEVIS;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AGRIN; ANIMALS; CALCIUM SIGNALING; CELLS, CULTURED; EMBRYO, NONMAMMALIAN; GROWTH CONES; MOTOR NEURONS; NEURITES; RAC1 GTP-BINDING PROTEIN; SPINAL CORD; XENOPUS LAEVIS;

ANIMALIA; XENOPUS LAEVIS;

EID: 27644555676     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02016     Document Type: Article

References (53)

1. Alder, J., Kanki, H., Valtorta, F., Greengard, P. and Poo, M. M. (1995). Overexpression of synaptophysin enhances neurotransmitter secretion at Xenopus neuromuscular synapses. J. Neurosci. 15, 511-519.
2. Bezakova, G. and Ruegg, M. A. (2003). New insights into the roles of agrin. Nat. Rev. Mol. Cell Biol. 4, 295-308.
3. Bixby, J. L., Baerwald-De la Torre, K., Wang, C., Rathjen, F. G. and Ruegg, M. A. (2002). A neuronal inhibitory domain in the N-terminal half of agrin. J. Neurobiol. 50, 164-179.
4. Burgess, R. W., Dickman, D. K., Nunez, L., Glass, D. J. and Sanes, J. R. (2002). Mapping sites responsible for interactions of agrin with neurons. J. Neurochem. 83, 271-284.
5. Campagna, J. A., Ruegg, M. A. and Bixby, J. L. (1995). Agrin is a differentiation-inducing "stop signal" for motoneurons in vitro. Neuron 15, 1365-1374.
6. Cohen, N. A., Kaufmann, W. E., Worley, P. F. and Rupp, F. (1997). Expression of agrin in the developing and adult rat brain. Neuroscience 76, 581-596.
7. Croll, S. D., Chesnutt, C. R., Rudge, J. S., Acheson, A., Ryan, T. E., Siuciak, J. A., DiStefano, P. S., Wiegand, S. J. and Lindsay, R. M. (1998). Co-infusion with a TrkB-Fc receptor body carrier enhances BDNF distribution in the adult rat brain. Exp. Neurol. 152, 20-33.
8. Daniels, R. H., Hall, P. S. and Bokoch, G. M. (1998). Membrane targeting of p21-activated kinase 1 (PAK1) induces neurite outgrowth from PC12 cells. EMBO J. 17, 754-764.
9. DeChiara, T. M., Bowen, D. C., Valenzuela, D. M., Simmons, M. V., Poueymirou, W. T., Thomas, S., Kinetz, E., Compton, D. L., Rojas, E., Park, J. S. et al. (1996). The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85, 501-512.
10. Fu, A. K., Smith, F. D., Zhou, H., Chu, A. H., Tsim, K. W., Peng, B. H. and Ip, N. Y. (1999). Xenopus muscle-specific kinase: molecular cloning and prominent expression in neural tissues during early embryonic development. Eur. J. Neurosci. 11, 373-382.
11. Gautam, M., Noakes, P. G., Moscoso, L., Rupp, F., Scheller, R. H., Merlie, J. P. and Sanes, J. R. (1996). Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85, 525-535.
12. Glass, D. J., Bowen, D. C., Stitt, T. N., Radziejewski, C., Bruno, J., Ryan, T. E., Gies, D. R., Shah, S., Mattsson, K., Burden, S. J. et al. (1996). Agrin acts via a MuSK receptor complex. Cell 85, 513-523.
13. Gomez, T. M. and Spitzer, N. C. (1999). In vivo regulation of axon extension and pathfinding by growth-cone calcium transients. Nature 397, 350-355.
14. Hawkins, P. T., Eguinoa, A., Qiu, R. G., Stokoe, D., Cooke, F. T., Walters, R., Wennstrom, S., Claesson-Welsh, L., Evans, T., Symons, M. et al. (1995). PDGF stimulates an increase in GTP-Rac via activation of phosphomositide 3-kinase. Curr. Biol. 5, 393-403.
15. Hilgenberg, L. G., Hoover, C. L. and Smith, M. A. (1999). Evidence of an agrin receptor in cortical neurons. J. Neurosci. 19, 7384-7393.
16. Hoch, W., Ferns, M., Campanelli, J. T., Hall, Z. W. and Scheller, R. H. (1993). Developmental regulation of highly active alternatively spliced forms of agrin. Neuron 11, 479-490.
17. Hong, K., Nishiyama, M., Henley, J., Tessier-Lavigne, M. and Poo, M. (2000). Calcium signalling in the guidance of nerve growth by netrin-1. Nature 403, 93-98.
18. Hoover, C. L., Hilgenberg, L. G. and Smith, M. A. (2003). The COOH-terminal domain of agrin signals via a synaptic receptor in central nervous system neurons. J. Cell Biol. 161, 923-932.
19. Ip, F. C., Glass, D. G., Gies, D. R., Cheung, J., Lai, K. O., Fu, A. K., Yancopoulos, G. D. and Ip, N. Y. (2000). Cloning and characterization of muscle-specific kinase in chicken. Mol. Cell Neurosci. 16, 661-673.
20. Ji, R. R., Bose, C. M., Lesuisse, C., Qiu, D., Huang, J. C., Zhang, Q. and Rupp, F. (1998). Specific agrin isoforms induce cAMP response element binding protein phosphorylation in hippocampal neurons. J. Neurosci. 18, 9695-9702.
21. Jones, M. A. and Werle, M. J. (2004). Agrin-induced AChR aggregate formation requires cGMP and aggregate maturation requires activation of cGMP-dependent protein kinase. Mol. Cell Neurosci. 25, 195-204.
22. Karasewski, L. and Ferreira, A. (2003). MAPK signal transduction pathway mediates agrin effects on neurite elongation in cultured hippocampal neurons. J. Neurobiol. 55, 14-24.
23. Kaufmann, N., Wills, Z. P. and Van Vactor, D. (1998). Drosophila Rac1 controls motor axon guidance. Development 125, 453-461.
24. Kleiman, R. J. and Reichardt, L. F. (1996). Testing the agrin hypothesis. Cell 85, 461-464.
25. Kroger, S. and Schroder, J. E. (2002). Agrin in the developing CNS: new roles for a synapse organizer. News Physiol. Sci. 17, 207-212.
26. Kundra, V., Escobedo, J. A., Kazlauskas, A., Kim, H. K., Rhee, S. G., Williams, L. T. and Zetter, B. R. (1994). Regulation of chemotaxis by the platelet-derived growth factor receptor-beta. Nature 367, 474-476.
27. Lai, K. O. and Ip, N. Y. (2003a). Central synapse and neuromuscular junction: same players, different roles. Trends Genet. 19, 395-402.
28. Lai, K. O. and Ip, N. Y. (2003b). Postsynaptic signaling of new players at the neuromuscular junction. J. Neurocytol. 32, 727-741.
29. Lautermilch, N. J. and Spitzer, N. C. (2000). Regulation of calcineurin by growth cone calcium waves controls neurite extension. J. Neurosci. 20, 315-325.
30. Lundquist, E. A. (2003). Rac proteins and the control of axon development. Curr. Opin. Neurobiol. 13, 384-390.
31. Luo, L., Liao, Y. J., Jan, L. Y. and Jan, Y. N. (1994). Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 8, 1787-1802.
32. Luo, Z., Wang, Q., Dobbins, G. C., Levy, S., Xiong, W. C. and Mei, L. (2003). Signaling complexes for postsynaptic differentiation. J. Neurocytol. 32, 697-708.
33. Mantych, K. B. and Ferreira, A. (2001). Agrin differentially regulates the rates of axonal and dendritic elongation in cultured hippocampal neurons. J. Neurosci. 21, 6802-6809.
34. McMahon, S., Bennett, D. L., Priestley, J. V. and Shelton, D. L. (1995). The biological effects of endogenous nerve growth factor on adult sensory neurons revealed by a trkA-IgG fusion molecule. Nat. Med. 1, 774-780.
35. Ming, G. L., Song, H. J., Berninger, B., Holt, C. F., Tessier-Lavigne, M. and Poo, M. M. (1997). cAMP-dependent growth cone guidance by netrin-1. Neuron 19, 1225-1235.
36. Ming, G., Song, H., Berninger, B., Inagaki, N., Tessier-Lavigne, M. and Poo, M. (1999). Phospholipase C-gamma and phosphoinositide 3-kinase mediate cytoplasmic signaling in nerve growth cone guidance. Neuron 23, 139-148.
37. Ming, G-I., Wong, S. T., Henley, J., Yuan, X.-b., Song, H.-j., Spitzer, N. C. and Poo, M.-m. (2002). Adaptation in the chemotactic guidance of nerve growth cones. Nature 417, 411-418.
38. Nishiyama, M. H. A., Tsai, L., Henley, J. R., Goshima, Y., Tessier-Lavigne, M., Poo, M. M. and Hong, K. (2003). Cyclic AMP/GMP-dependent modulation of Ca2+ channels sets the polarity of nerve growth-cone turning. Nature 423, 990-995.
39. Nobes, C. D., Hawkins, P., Stephens, L. and Hall, A. (1995). Activation of the small GTP-binding proteins rho and rac by growth factor receptors. J. Cell Sci. 108, 225-233.
40. O'Connor, L. T., Lauterborn, J. C., Gall, C. M. and Smith, M. A. (1994). Localization and alternative splicing of agrin mRNA in adult rat brain: transcripts encoding isoforms that aggregate acetylcholine receptors are not restricted to cholinergic regions. J. Neurosci. 14, 1141-1152.
41. Rupp, F., Payan, D. G., Magill-Solc, C., Cowan, D. M. and Scheller, R. H. (1991). Structure and expression of a rat agrin. Neuron 6, 811-823.
42. Song, H. J., Ming, G. L. and Poo, M. M. (1997). cAMP-induced switching in turning direction of nerve growth cones. Nature 388, 275-279.
43. Takei, K., Shin, R.-M., Inoue, T., Kato, K. and Mikoshiba, K. (1998). Regulation of nerve growth mediated by Inositol 1,4,5-Trisphosphate receptors in growth cones. Science 282, 1705-1708.
44. Threadgill, R., Bobb, K. and Ghosh, A. (1997). Regulation of dendritic growth and remodeling by Rho, Rac, and Cdc42. Neuron 19, 625-634.
45. Valenzuela, D. M., Stitt, T. N., DiStefano, P. S., Rojas, E., Mattsson, K., Compton, D. L., Nunez, L., Park, J. S., Stark, J. L., Gies, D. R. 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.
46. Wennstrom, S., Siegbahn, A., Yokote, K., Arvidsson, A. K., Heldin, C. H., Mori, S. and Claesson-Welsh, L. (1994). Membrane ruffling and chemotaxis transduced by the PDGF beta-receptor require the binding site for phosphatidylinositol 3′ kinase. Oncogene 9, 651-660.
47. Weston, C., Yee, B., Hod, E. and Prives, J. (2000). Agrin-induced acetylcholine receptor clustering is mediated by the small guanosine triphosphatases Rac and Cdc42. J. Cell Biol. 150, 205-212.
48. Wong, S. T., Henley, J. R., Kanning, K. C., Huang, K. H., Bothwell, M. and Poo, M. M. (2002). A p75(NTR) and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat. Neurosci 5, 1302-1308.
49. Yang, J. F., Ng, Y. P., Pun, S., Ip, N. Y. and Tsim, K. W. K. (1997). The EGF-like domain of chick acetylcholine receptor-inducing activity (ARIA) contains its full biological activity. FEBS Lett. 403, 163-167.
50. Yuan, X. B., Jin, M., Xu, X., Song, Y. Q., Wu, C. P., Poo, M. M. and Duan, S. (2003). Signalling and crosstalk of Rho GTPases in mediating axon guidance. Nat. Cell Biol. 5, 38-45.
51. Zhang, J., Lefebvre, J. L., Zhao, S. and Granato, M. (2004). Zebrafish unplugged reveals a role for muscle-specific kinase homologs in axonal pathway choice. Nat Neurosci. 7, 1303-1309.
52. Zheng, J. (2000). Turning of nerve growth cones induced by localized increases in intracellular calcium ions. Nature 403, 89-93.
53. Zheng, J. Q., Wan, J. J. and Poo, M. M. (1996). Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J. Neurosci. 16, 1140-1149.