B-50/GAP-43-induced formation of filopodia depends on Rho-GTPase

Molecular Biology of the Cell

Volumn 9, Issue 6, 1998, Pages 1279-1292

  Aarts, Lambertus H J ^a,b   Schrama, Loes H ^a,b   Hage, Willem J ^c   Bos, Johannes L ^a   Gispen, Willem Hendrik ^b   Schotman, Peter ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c HUBRECHT INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; NEUROMODULIN; RHO FACTOR;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; FIBROBLAST; NERVE FIBER GROWTH; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALIA; CLOSTRIDIUM BOTULINUM;

EID: 0031867054     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.6.1279     Document Type: Article

References (62)

1. Aarts, L.H.J., Van der Linden, J.A.M., Hage, W.J., Van Rozen, A.J., Oestreicher, A.B., Gispen, W.H., and Schotman, P. (1995). N-terminal cysteines essential for Golgi sorting of B-50 (GAP-43) in PC12 cells. Neuroreport 6, 969-972.
2. Aigner, L., Arber, S., Kapfhammer, J.P., Laux, T., Schneider, C., Botteri, F., Brenner, H.R., and Caroni, P. (1995). Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell 83, 269-278.
3. Aigner, L., and Caroni, P. (1993). Depletion of 43-kD growth-associated protein in primary sensory neurons leads to diminished formation and spreading of growth cones. J. Cell Biol. 123, 417-429.
4. Aigner, L., and Caroni, P. (1995). Absence of persistent spreading, branching, and adhesion in GAP-43-depleted growth cones. J. Cell Biol. 128, 647-660.
5. Apel, E.D., Litchfield, D.W., Clark, R.H., Krebs, E.G., and Storm, D.R. (1991). Phosphorylation of neuromodulin (GAP-43) by casein kinase II; identification of phosphorylation sites and regulation by calmodulin. J. Biol. Chem. 16, 10544-10551.
6. Bentley, D., and Toroian-Raymond, A. (1986). Disoriented pathfinding by pioneer neurone growth cones deprived of filopodia by cytochalasin treatment. Nature 323, 712-715.
7. Bray, D., and Hollenbeck, P.J. (1988). Growth cone motility and guidance. Annu. Rev. Cell Biol. 4, 43-61.
8. Bray, D., and White, J.G. (1988). Cortical flow in animal cells. Science 239, 883-888.
9. Chapman, E.R., Au, D., Alexander, K.A., Nicolson, T.A., and Storm, D.R. (1991). Characterization of the calmodulin binding domain of neuromodulin J. Biol. Chem. 266, 207-213.
10. Chardin, P., Boquet, P., Madaule, P., Popoff, M.R., Rubin, E.J., and Gill, D.M. (1989). The mammalian G protein rhoC is ADP-ribosylated by Clostridium botulinum exoenzyme C3 and affects actin microfilaments in Vero cells. EMBO J. 8, 1087-1092.
11. Chien, C.B., Rosenthal, D.E., Harris, W.A., and Holt, C.E. (1993). Navigational errors made by growth cones without filopodia in the embryonic Xenopus brain. Neuron 11, 237-251.
12. Chong, L.D., Traynor-Kaplan, A., Bokoch, G.M., and Schwartz, M.A. (1994). The small GTP-binding protein Rho regulates a phosphatidylinositol 4-phosphate 5-kinase in mammalian cells. Cell 79, 507-513.
13. Davenport, R.W., Dou, P., Rehder, V., and Kater, S.B. (1993). A sensory role for neuronal growth cone filopodia. Nature 361, 721-724.
14. Evan, G.I., Lewis, G.K., Ramsey, G., and Bishop, J.M. (1985). Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5, 3610-3616.
15. Gamby, C., Waage, M.C., Allen, R.G., and Baizer, L. (1996). Analysis of the role of calmodulin binding and sequestration in neuromodulin (GAP-43) function. J. Biol. Chem. 271, 26698-26705.
16. Gilmore, A.P., and Burridge, K. (1996). Regulation of vinculin binding to talin and actin by phosphatidyl-inositol-4-5-bisphosphate. Nature 381, 531-535.
17. Gomez, T.M., and Letourneau, P.C. (1994). Filopodia initiate choices made by sensory neuron growth cones at laminin/fibronectin borders in vitro. J. Neurosci. 14, 5959-5972.
18. Goodman, C.S. (1996). Mechanisms and molecules that control growth cone guidance. Annu. Rev. Neurosci. 19, 341-377.
19. Gossen, M., and Bujard, H. (1992). Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA 89, 5547-5551.
20. Hall, A. (1994). Small GTP-binding proteins and the regulation of the actin cytoskeleton. Annu. Rev. Cell Biol. 10, 31-54.
21. He, Q., Dent, E.W., and Meiri, K.F. (1997). Modulation of actin filament behavior by GAP-43 (neuromodulin) is dependent on the phosphorylation status of serine 41, the protein kinase C site. J. Neurosci. 17, 3515-3524.
22. Hens, J.J.H., Benfenati, F., Nielander, H.B., Valtorta, F., Gispen, W.H., and De Graan, P.N.E. (1993). B-50/GAP-43 binds to actin filaments without affecting actin polymerization and filament organization. J. Neurochem. 61, 1530-1533.
23. Holtmaat, A.J.G.D., Dijkhuizen, P.A., Oestreicher, A.B., Romijn, H.J., Van der Lugt, N.M.T., Berns, A., Margolis, F.L., Gispen, W.H., and Verhaagen, J. (1995). Directed expression of the growth-associated protein B-50/GAP-43 to olfactory neurons in transgenic mice results in changes in axon morphology and extraglomerular fiber growth. J. Neurosci. 15, 7953-7965.
24. Holtmaat, A.J.G.D., Hermens, W.T.J.M.C., Sonnemans, M.A.F., Giger, R.J., Van Leeuwen, F.W., Kaplitt, M.G., Oestreicher, A.B., Gispen, W.H., and Verhaagen, J. (1997). Adenoviral vector-mediated expression of B-50/GAP-43 induces alterations in the membrane organization of olfactory axon terminals in vivo. J. Neurosci. 17, 6575-6586.
25. Janmey, P.A. (1994). Phosphoinositides and calcium as regulators of cellular actin assembly and disassembly. Annu. Rev. Physiol. 56, 169-191.
26. Jap Tjoen San, E.R.A., Schmidt-Michels, M.H., Oestreicher, A.B., Gispen, W.H., and Schotman, P. (1992). Inhibition of nerve growth factor-induced B-50/GAP-43 expression by antisense oligomers interferes with neurite outgrowth of PC12 cells. Biochem. Biophys. Res. Commun. 187, 839-846.
27. Jap Tjoen San, E.R.A., Van Rozen, A.J., Nielander, H.B., Oestreicher, A.B., Gispen, W.H., and Schotman, P. (1995). Expression levels of B-50/GAP-43 in PC12 cells are decisive for the complexity of their neurites and growth cones. J. Mol. Neurosci. 6, 185-200.
28. Jin, Z., and Strittmatter, S.M. (1997). Rac1 mediates collapsin-1-induced growth cone collapse. J. Neurosci. 17, 6256-6236.
29. Jolles, J., Zwiers, H., Van Dongen, C.J., Schotman, P., Wirtz, K.W.A., and Gispen, W.H. (1980). Modulation of brain polyphosphoinositide metabolism by ACTH-sensitive protein phosphorylation. Nature 286, 623-625.
30. Lang, P., and Bertoglio, J. (1995). Inhibition of lymphocyte-mediated cytotoxicity by Clostridium botulinum C3 transferase. Methods Enzymol. 256, 320-327.
31. Liu, Y., Fisher, D.A., and Storm, D.R. (1994). Intracellular sorting of neuromodulin (GAP-43) mutants modified in the membrane targeting domain. J. Neurosci. 14, 5807-5817.
32. Luo, L.Q., Jan, L.Y., and Jan, Y.N. (1997). Rho family small GTP-binding proteins in growth cone signalling. Curr. Opin. Neurobiol. 7, 81-86.
33. Machesky, L.M., and Hall, A. (1996). Rho: A connection between membrane receptor signalling and the cytoskeleton. Trends Cell Biol. 6: 304-310.
34. Machesky, L.M., and Hall, A. (1997). Role of actin polymerization and adhesion to extracellular matrix in Rac- and Rho-induced cytoskeletal reorganization. J. Cell Biol. 138: 913-926.
35. Meiri, K.F., and Gordon-Weeks, P.R. (1990). GAP-43 in growth cones is associated with areas of membrane that are tightly bound to substrate and is a component of a membrane skeleton subcellular fraction. J. Neurosci. 10, 256-266.
36. Meiri, K.F., Hammang, J.P., Dent, E.W., and Baetge, E.E. (1996). Mutagenesis of ser41 to ala inhibits the association of GAP-43 with the membrane skeleton of GAP-43-deficient PC12B cells: effects on cell adhesion and the composition of neurite cytoskeleton and membrane. J. Neurobiol. 29, 213-232.
37. Mercken, M., Lubke, U., Vandermeeren, M., Gheuens, J., and Oestreicher, A.B. (1992). Immunocytochemical detection of the growth associated protein B-50 by newly characterized monoclonal antibodies in human brain and muscle. J. Neurobiol. 23, 309-321.
38. Morton, A.J., and Buss, T.N. (1992). Accelerated differentiation in response to retinoic acid after retrovirally mediated gene transfer of GAP-43 into mouse neuroblastoma cells. Eur. J. Neurosci. 4, 910-916.
39. Nielander, H.B., French, P., Oestreicher, A.B., Gispen, W.H., and Schotman, P. (1993). Spontaneous morphological changes by over-expression of the growth-associated protein B-50/GAP-43 in a PC12 cell line. Neurosci. Lett. 162, 46-50.
40. Nobes, C.D., and Hall, A. (1995). Rho, Rac and Cdc-42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62
41. O'Connor, T.P., Duerr, J.S., and Bentley, D. (1990). Pioneer growth cone steering decisions mediated by single filopodial contacts in situ. J. Neurosci. 10, 3935-3946.
42. Oestreicher, A.B., De Graan, P.N.E., Gispen, W.H., Verhaagen, J., and Schrama, L.H. (1997). B-50, the growth associated protein-43: modulation of cell morphology and communication in the nervous system. Prog. Neurobiol. 53, 627-686.
43. Pisano, M.R., Hegazy, M.G., Reimann, E.W., and Dokas, L.A. (1988). Phosphorylation of protein B-50 (GAP-43) from adult rat brain cortex by casein kinase II. Biochem. Biophys. Res. Commun. 155, 1207-1212.
44. Qiu, R.-G., Chen, J., Kirn, D., McCormick, F., and Symons, M. (1995). An essential role for Rac in Ras transformation. Nature 374, 457-459.
45. Qiu, R.-G., Chen, J., McCormick, F., and Symons, M. (1995). A role for Rho in Ras transformation. Proc. Natl. Acad. Sci. USA 92, 11781-11785.
46. Ridley, A.J., and Hall, A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
47. Sekine, A., Fujiwara, M., and Narumiya, S. (1989). Asparagine residue in the rho gene product is the modification site for bofulinum ADP-ribosyltransferase. J. Biol. Chem. 264, 8602-8605.
48. Shea, T.B. (1994). Delivery of anti-GAP-43 antibodies into neuroblastoma cells reduces growth cone size. Biochem. Biophys. Res. Commun. 203, 459-464.
49. Shea, T.B., Perrone-Bizzozero, N.I., Beermann, M.L., and Benowitz, L.I. (1991). Phospholipid-mediated delivery of anti-GAP-43 antibodies into neuroblastoma cells prevents neuritogenesis. J. Neurosci. 11, 1685-1690.
50. Strittmatter, S.M., Fankhauser, C., Huang, P.L., Mashimo, H., and Fishman, M.C. (1995). Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43. Cell 80, 445-452.
51. Strittmatter, S.M., Valenzuela, D., and Fishman, M.C. (1994). An amino-terminal domain of the growth-associated protein GAP-43 mediates its effects on filopodial formation and cell spreading. J. Cell Sci. 107, 195-204.
52. o stimulation by GAP-43. EMBO J. 11, 2095-2102.
53. Sydor, A.M., Su, A.L., Wang, F.S., Xu, A., and Jay, D.G. (1996). Talin and vinculin play distinct roles in filopodial motility in the neuronal growth cone. J. Cell Biol. 134, 1197-1207.
54. Symons, M. (1996). Rho family GTPases: the cytoskeleton and beyond. Trends Biochem. Sci. 21, 178-181.
55. Tsukita, S., Yonemura, S., and Tsukita, Sh. (1997). ERM proteins: head-to-tail regulation of actin-plasma membrane interaction. Trends Biochem. Sci. 22, 53-58.
56. Van Hooff, C.O.M., De Graan, P.N.E., Oestreicher, A.B., and Gispen, W.H. (1988). B-50 phosphorylation and polyphosphoinositide metabolism in nerve growth cone membranes. J. Neurosci. 8, 1789-1795.
57. Varnum-Finney, B., and Reichardt, L.F. (1994). Vinculin-deficient PC12 cell lines extend unstable lamellipodia and filopodia and have a reduced rate of neurite outgrowth. J. Cell Biol. 127, 1071-1084.
58. Widmer, F., and Caroni, P. (1993). Phosphorylation-site mutagenesis of the growth-associated protein GAP-43 modulates its effects on cell spreading and morphology. J. Cell Biol. 120, 503-512.
59. Wiederkehr, A., Staple, J., and Caroni, P. (1997). The motility-associated proteins GAP-43, MARCKS, and CAP-23 share unique targeting and surface activity-inducing properties. Exp. Cell Res. 236, 103-116.
60. Yankner, B.A., Benowitz, L.I., Villa-Komaroff, L., and Neve, R.L. (1990). Transfection of PC12 cells with the human GAP-43 gene: effects on neurite outgrowth and regeneration. Mol. Brain Res. 7, 39-44.
61. Zheng, Y., Glaven, J.A., Wu, W.J., and Cerione, R.A. (1996). Phosphatidylinositol 4,5-bisphosphate provides an alternative to guanine nucleotide exchange factors by stimulating the dissociation of GDP from Cdc42Hs. J. Biol. Chem. 271, 23815-23819.
62. Zuber, M.X., Goodman, D.W., Karns, L.R., and Fishman, M.C. (1989). The neuronal growth-associated protein GAP-43 induces filopodia in non-neuronal cells. Science 244, 1193-1195.