Regulation of Rho family GTPases is required to prevent axons from crossing the midline

Developmental Biology

Volumn 252, Issue 1, 2002, Pages 46-58

  Fritz, Janice L ^a   VanBerkum, Mark F A ^a  

^a WAYNE STATE UNIVERSITY   (United States)

Author keywords

Actin; Axon guidance; Cdc42; Drosophila; Myosin; Rac; Rho; Robo; Sos

Indexed keywords

GUANOSINE TRIPHOSPHATASE; ISOPROTEIN; MYOSIN; MYOSIN LIGHT CHAIN KINASE; PROFILIN; PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; ROUNDABOUT RECEPTOR; SOS PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENZYME REGULATION; NERVE CELL DIFFERENTIATION; NERVE FIBER TRANSPORT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

EID: 0036435544     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.2002.0842     Document Type: Article

References (61)

1. Allen, M. J., Shan, X., and Murphey, R. K. (2000). A role for Drosophila Drac1 in neurite outgrowth and synaptogenesis in the giant fiber system. Mol. Cell. Neurosci. 16, 754-765.
2. Amano, M., Ito, M., Kimura, K., Fukata, Y., Chihara, K., Nakano, T., M., and Kaibuchi, K. (1996). Phosphorylation and activation of Myosin by Rho and Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271, 20246-20249.
3. Appenstrom, P. (1999). Rho GTPases have multiple effects on the actin cytoskeleton. Exp. Cell Res. 246, 20-25.
4. Arthur, W. T., Petch, L. A., and Burridge, K. (2000). Integrin engagement suppresses RhoA activity via a c-src-dependent mechanism. Curr. Biol. 10, 719-722.
5. Bagrodia, S., and Cerione, R. A. (1999). PAK to the future. Trends Cell Biol. 9, 350-355.
6. Bashaw, G. J., Hu, H., Nobes, C. D., and Goodman, C. S. (2001). A novel Dbl family RhoGEF promotes Rho-dependent axon attraction to the central nervous system midline in Drosophila and overcomes Robo repulsion. J. Cell Biol. 155, 1117-1122.
7. Billuart, P., Winter, C. G., Maresh, A., and Luo, L. (2001). Regulating axon branch stability: The role of p190 RhoGAP in repressing a retraction signaling pathway. Cell 107, 195-207.
8. Braga, V. M. M., Machesky, L. M., Hall, A., and Hotchin, N. A. (1997). The small GTPases Rho and Rac are required for the establishment of cadherin-dependent cell-cell contacts. J. Cell Biol. 137, 1421-1231.
9. Brose, K., Bland, K. S., Wang, K. H., Arnott, D., Henzel, W., Goodman, C. S., Tessier-Lavigne, M., and Kidd, T. (1999). Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96, 795-806.
10. Chew, T. L., Masaracchia, R. A., Goeckeler, Z. M., and Wysolmerski, R. B. (1998). Phosphorylation of non-muscle myosin II regulatory light chain by p21-activated kinase (gamma-PAK). J. Muscle Res. Cell Motil. 19, 839-854.
11. Clark, E. A., King, W. G., Brugge, J. S., Symons, M., and Hynes, R. O. (1998). Integrin-mediated signals regulated by members of the Rho family GTPases. J. Cell Biol. 142, 573-386.
12. Dickson, B. J. (2001). Rho GTPases in growth cone guidance. Curr. Opin. Neurobiol. 11, 103-110.
13. Driessens, M. H., Hu, H., Nobes, C. D., Self, A., Jordens, I., Goodman, C. S., and Hall, A. (2001). Plexin-B Semaphorin receptors interact directly with active Rac and regulate the actin cytoskeleton by activating Rho. Curr. Biol. 11, 339-344.
14. Fournier, A. E., Nakamura, F., Kawamoto, S., Goshima, Y., Kalb, R. G., and Strittmatter, S. M. (2000). Semaphorin3A enhances endocytosis at sites of receptor-F-actin colocalization during growth cone collapse. J. Cell Biol. 149, 411-422.
15. Fritz, J. L., and VanBerkum, M. F. (2000). Calmodulin and Son of sevenless dependent signaling pathways regulate midline crossing of axons in the Drosophila CNS. Development 127, 1991-2000.
16. Gallo, G., and Letourneau, P. C. (1999). Axon guidance: A balance of signals sets axons on the right track. Curr. Biol. 9, R490-R492.
17. Goeckeler, Z. M., Masaracchia, R. A., Zeng, Q., Chew, T-L., Gallagher, P., and Wysolmerski, R. B. (2000). Phosphorylation of myosin light chain kinase by p21-activated kinase PAK2. J. Biol. Chem. 275, 18366-18374.
18. Hall, A., and Nobes, C. D. (2000). Rho GTPases: Molecular switches that control the organization and dynamics of the actin cytoskeleton. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 965-970.
19. Harris, R., Sabatelli, L. M., and Seeger, M. A. (1996). Guidance cues at the Drosophila CNS midline: Identification and characterization of two Drosophila Netrin/UNC-6 homologs. Neuron 17, 217-228.
20. Hoang, B., and Chiba, A. (1998). Genetic analysis on the role of Integrin during axon guidance in Drosophila. J. Neurosci. 18, 7847-7855.
21. Hu, H., Marton, T. F., and Goodman, C. S. (2001). Plexin B mediates axon guidance in Drosophila by simultaneously inhibiting Rac and enhancing Rho signaling. Neuron 32, 39-51.
22. Jay, D. G. (2000). The clutch hypothesis revisited: Ascribing the roles of actin-associated proteins in filopodial protrusion in the nerve growth cone. J. Neurobiol. 44, 114-125.
23. Jin, Z., and Strittmatter, S. M. (1997). Rac1 mediates collapsin-1-induced growth cone collapse. J. Neurosci. 17, 6256-6263.
24. Karim, F. D., Chang, H. C., Therrien, M., Wassarman, D. A., Laverty, T., and Rubin, G. M. (1996). A screen for genes that function downstream of Ras1 during Drosophila eye development. Genetic 143, 315-329.
25. Kaufmann, N., Wills, Z. P., and Van Vactor, D. (1998). Drosophila Rac1 controls motor axon guidance. Development 125, 453-461.
26. Kidd, T., Brose, K., Mitchell, K. J., Fetter, R. D., Tessier-Lavigne, M., Goodman, C. S., and Tear, G. (1998). Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 92, 205-215.
27. Kidd, T., Bland, K. S., and Goodman, C. S. (1999). Slit is the midline repellent for the robo receptor in Drosophila. Cell 96, 785-794.
28. Kim, M. D., Kolodziej, P., and Chiba, A. (2002a). Growth cone pathfinding and filopodial dynamics are mediated separately by Cdc42 activation. J. Neurosci. 22, 1794-1806.
29. Kim, Y-S, Furman, S., Sink, H., and VanBerkum, M. F. A. (2001). Calmodulin and profilin co-regulate axon outgrowth in Drosophila. J. Neurobiol. 47, 26-38.
30. Kim, Y-S., Fritz, J. L., Seneviratne, A. K., and VanBerkum, M. F. A. (2002). Constitutively active myosin light chain kinase alters axon guidance decisions in Drosophila embryos. Dev. Biol. 249, 367-381.
31. Kimura, K., Ito, M., Amano, M., Chihara, K., Fukata, Y., Nakafuku, M., Yamamori, B., Feng, J., Nakano, T., Okawa, K., Iwamatsu, A., and Kaibuchi, K. (1996). Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248.
32. Kimura, K., Kukata, Y., Matsuoka, Y., Bennet, V., Matsuura, Y., Okawa, K., Iwamatsu, A., and Kaibuchi, K. (1998). Regulation of the association of Adductin with actin filaments by Rho-associated Kinase (Rho Kinase). J. Biol. Chem. 273, 5542-5548.
33. Kjoller, L., and A. Hall. (1999). Signaling to Rho GTPases. Exp. Cell Res. 253, 166-179.
34. Kolodziej, P. A., Timpe, L. C., Mitchell, K. J., Fried, S. R., Goodman, C. S., Jan, L. Y., and Jan, Y. N. (1996). Frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 87, 197-204.
35. Kuhn, T. B., Meberg, P. J., Brown, M. D., Bernstein, B. W., Minamide, L. S., Jensen, J. R., Okada, K., Soda, E. A., and Bamberg, J. R. (2000). Regulating actin dynamics in neuronal growth cones by ADF/cofilin and the Rho family GTPases. J. Neurobiol. 44, 126-144.
36. Kuroda, S., Fukata, M., Nakagawa, M., and Kaibuchi, K. (1999). Cdc42, Rac1, and their effector IQGAP as molecular switches for cadherin-mediated cell-cell adhesion. Biochem. Biophys. Res. Commun. 262, 1-6.
37. Lee, T., Winter, C., Marticke, S. S., Lee, A., and Luo, L. (2000). Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis. Neuron 25, 307-316.
38. Li, H. S., Chen, J. H., Wu, W., Fagaly, T., Zhou, L., Yuan, W., Dupuis, S., Jiang, Z. H., Nash, W., Gick, C., Ornitz, D. M., Wu, J. Y., and Rao, Y. (1999). Vertebrate slit, a secreted ligand for the transmembrane protein roundabout, is a repellent for olfactory bulb axons. Cell 96, 807-818.
39. Li, X., Saint-Cry-Proulx, E., Aktories, K., and Lamarche-Vane, N. (2002). Rac1 and Cdc42 but not RhoA or Rho kinase activities are required for neurite outgrowth induced by the Netrin-1 receptor DCC (deleted in colorectal cancer) in NIE-115 neuroblastoma cells. J. Biol. Chem. 277, 15207-15214.
40. Lin, D. M., Fetter, R. D., Kopczynski, C., Grenningloh, G., and Goodman, C. S. (1994). Genetic analysis of Fasciclin II in Drosophila: Defasciculation, refasciculation, and altered fasciculation. Neuron 13, 1055-1069.
41. 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.
42. Luo, L. (2000). Rho GTPases in neuronal morphogenesis. Nat. Rev. Neurosci. 1, 173-180.
43. Murray, M. J., and Whitington, P. M. (1999). Effects of roundabout on growth cone dynamics, filopodial length, and growth cone morphology at the midline and throughout the neuropile. J. Neurosci. 19, 7901-7912.
44. Ng, J., Nardine, T., Harms, M., Tzu, J., Goldstein, A., Sun, Y., Dietzl, G., Dickson, B. J., and Luo, L. (2002). Rac GTPases control axon growth, guidance, and branching. Nature 416, 442-447.
45. Nimnual, A. S., Yatsula, B. A., and Bar-Sagi, D. (1998). Coupling of Ras and Rac guanosine triphosphatases through the Ras exchanger Sos. Science 279, 560-563.
46. Nobes, C. D., and Hall, A. (1995). Rho, Rac, and Cdc42 regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellapodia, and filopodia. Cell 81, 53-62.
47. Nobes, C. D., and Hall, A. (1999). Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell Biol. 144, 1235-1244.
48. Price, L. S., Leng, J., Schwartz, M. A., and Bokoch, G. M. (1998) Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol. Biol. Cell 9, 1862-1871.
49. Rangarajan, R., Gong, Q., and Gaul, U. (1999). Migration and function of glia in the developing Drosophila eye. Development 126, 3285-3292.
50. Ranscht, B. (2000). Cadherins: Molecular codes for axon guidance and synapse formation. Int. J. Dev. Neurosci. 18, 643-651.
51. Sanders, L. C., Matsumura, F., Bokoch, G. M., and de Lanerolle, P. (1999). Inhibition of myosin light chain kinase by p21-activated kinase. Science 283, 2083-2085.
52. Sells, M. A., Boyd, J. T., and Chernoff, J. (1999). p21-activated kinase 1 (Pak1) regulated cell motility in mammalian fibroblasts. J. Cell Biol. 145, 837-849.
53. Shekarabi, M., and Kennedy, T. E. (2002). The nitrin-1 receptor DCC promotes filopodia formation and spreading by activating Cdc42 and Rac1. Mol. Cell. Neurosci. 19, 1-17.
54. Strutt, D. I., Weber, U., and Mlodzik, M. (1997). The role of RhoA in tissue polarity and Frizzled signaling. Nature 387, 292-295.
55. Suter, D. M., and Forscher, P. (2000). Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance. J. Neurobiol. 44, 97-113.
56. Tapon, N., and Hall, A. (1997). Rho, Rac, and Cdc42 GTPases regulate the organization of the actin cytoskeleton. Curr. Opin. Cell Biol. 9, 86-92.
57. Tessier-Lavigne, M., and Goodman, C. S. (1996). The molecular biology of axon guidance. Science 274, 1123-1133.
58. VanBerkum, M. F., and Goodman, C. S. (1995). Targeted disruption of Ca(2+)-Calmodulin signaling in Drosophila growth cones leads to stalls in axon extension and errors in axon guidance. Neuron 14, 43-56.
59. Wahl, S., Barth, H., Ciossek, T., Aktories, K., and Mueller, B. K. (2000). Ephrin-A5 induces collapse of growth cones by activating Rho and Rho kinase. J. Cell Biol. 149, 263-270.
60. Wong, K., Ren, X-R., Huang, Y-Z., Xie, Y., Liu, G., Saito, H., Tang, H., Wen, L., Brady-Kalney, S. M., Mei, L., Wu, J. Y., Xiong, W-C., and Rao, Y. (2001). Signal transduction in neuronal migration: Roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway. Cell 107, 209-221.
61. Yang, C., Huang, M., DeBiasio, J., Pring, M., Joyce, M., Miki, H., Takenawa, T., and Zigmond, S. H. (2000). Profilin enhances Cdc42-induced nucleation of actin polymerization. J. Cell Biol. 150, 1001-1012.