G proteins and axon growth

Seminars in Neuroscience

Volumn 9, Issue 5-6, 1998, Pages 209-219

  Vancura, Kathleen L ^a   Jay, Daniel G ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

Axon elongation; Cytoskeleton; Growth cone; GTP binding proteins; Neuronal development

Indexed keywords

ACTIN; GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; CELL TYPE; CYTOSKELETON; FIBROBLAST; GROWTH CONE; HUMAN; HUMAN CELL; NERVE FIBER GROWTH; NONHUMAN; PROTEIN FAMILY; REVIEW;

EID: 0032075958     PISSN: 10445765     EISSN: None     Source Type: Journal    
DOI: 10.1006/smns.1997.0118     Document Type: Article

References (90)

1. Neer E. J. Heterotrimeric G proteins: Organizers of transmembrane signals. Cell. 80:1995;249-257.
2. Kaziro Y., Itoh H., Kozasa T., Nakafuku M., Satoh T. Structure and function of signal-transducing GTP-binding proteins. Annu. Rev. Biochem. 60:1991;349-400.
3. Hall A. Small GTP-binding proteins and the regulation of the actin cytoskeleton. Annu. Rev. Cell. Biol. 10:1994;31-54.
4. Nuoffer C., Balch W. E. GTPases: Multifunctional molecular switches regulating vesicular traffic. Annu. Rev. Biochem. 63:1994;949-990.
5. Jessell T. M. Cell migration and axon guidance. Principles of Neural Science. 1991;Appleton & Lange, Norwalk. p. 908-928.
6. Davenport R. W., Dou P., Rehder V., Kater S. B. A sensory role for neuronal growth cone filopodia. Nature. 361:1993;721-724.
7. Tanaka E., Sabry J. Making the connection: Cytoskeletal rearrangements during growth cone guidance. Cell. 83:1995;171-176.
8. Bray D., Chapman K. Analysis of microspike movements on the neuronal growth cone. J. Neurosci. 5:1985;3204-3213.
9. Goldberg D. J., Burmeister D. W. Stages in axon formation: Observations of growth of Aplysia axons in culture using video-enhanced contrast-differential interference contrast microscopy. J. Cell Biol. 103:1986;1921-1931.
10. Gordon-Weeks P. R. Organization of microtubules in axonal growth cones: a role for microtubule-associated protein MAP1B. J. Neurocytol. 22:1993;717-725.
11. Letourneau P. C., Kater S. B., Macagno E. R. The Nerve Growth Cone. 1992;Raven Press, New York.
12. Bandtlow C., Zachleder T., Schwab M. E. Oligodendrocytes arrest neurite growth by contact inhibition. J. Neurosci. 10:1990;3837-3848.
13. O'Connor T. P., Duerr J. S., Bentley D. Pioneer growth cone steering decisions mediated by single filopodial contacts in situ. J. Neurosci. 10:1990;3935-3946.
14. Bovolenta P., Mason C. Growth cone morphology varies with position in the developing mouse visual pathway from retina to first targets. J. Neurosci. 7:1987;1447-1460.
15. Taghert P. H., Bastiani M. J., Ho R. K., Goodman C. S. Guidance of pioneer growth cones: Filopodial contacts and coupling revealed with an antibody to Lucifer Yellow. Dev. Biol. 94:1982;391-399.
16. Tosney K. W., Landmesser L. T. Growth cone morphology and trajectory in the lumbosacral region of the chick embryo. J. Neurosci. 1985;2345-2348.
17. Eisen J. S., Myers P. Z., Westerfield M. Pathway selection by growth cones of identified motoneurons in live zebra fish embryos. Nature. 320:1986;269-271.
18. Holt C. E. A single-cell analysis of early retinal ganglion cell differentiation in Xenopus: From soma to axon tip. J. Neurosci. 9:1989;3123-3145.
19. Letourneau P. C. Differences in the organization of actin in the growth cones compared with the neurites of cultured neurons from chick embryos. J. Cell. Biol. 97:1983;963-973.
20. Sabry J. H., O'Connor T. P., Evans L., Toroian R. A., Kirschner M., Bentley D. Microtubule behavior during guidance of pioneer neuron growth cones in situ. J. Cell Biol. 115:1991;381-395.
21. Hille B. G protein-coupled mechanisms and nervous signaling. Neuron. 9:1992;187-195.
22. Stryer L. Visual excitation and recovery. J. Biol. Chem. 266:1991;10711-10714.
23. Neer E. J. G proteins: Critical control points for transmembrane signals. Protein Sci. 3:1994;3-14.
24. Higashijima T., Burnier J., Ross E. M. Regulation of Gi and Go by mastoparan, related amphiphilic peptides, and hydrophobic amines. J. Biol. Chem. 265:1990;14176-14186.
25. Greene L. A., Tischler A. S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. USA. 73:1976;2424-2428.
26. Doherty P., Ashton S. V., Moore S. E., Walsh F. S. Morphoregulatory activities of NCAM and N-Cadherin can be accounted for by G protein-dependent activation of L- and N-type neuronal Ca2+ channels. Cell. 67:1991;21-33.
27. Schuch U., Lohse M. J., Schachner M. Neural cell adhesion molecules influence second messenger systems. Neuron. 3:1989;13-20.
28. Williams E. J., Doherty P., Turner G., Reid R. A., Hemperly J. J., Walsh F. S. Calcium influx into neurons can solely account for cell contact-dependent neurite outgrowth stimulated by transfected L1. J. Cell Biol. 119:1992;883-892.
29. Williams E. J., Walsh F. S., Doherty P. Tyrosine kinase inhibitors can differentially inhibit integrin-dependent and CAM-stimulated neurite outgrowth. J. Cell Biol. 124:1994;1029-1037.
30. Igarashi M., Strittmatter S. M., Vartanian T., Fishman M. C. Mediation by G proteins of signals that cause collapse of growth cones. Science. 259:1993;77-79.
31. Kindt R. M., Lander A. D. Pertussis toxin specifically inhibits growth cone guidance by a mechanism independent of direct G protein inactivation. Neuron. 15:1995;79-88.
32. Strittmatter S. M., Vartanian T., Fishman M. C. GAP-43 as a plasticity protein in neuronal form and repair. J. Neurobiol. 23:1992;507-520.
33. o. Nature. 344:1990;836-841.
34. Edmonds B. T., Moomaw C. R., Hsu J. T., Slaughter C., Ellis L. The p38 and p34 polypeptides of growth cone particle membranes are the α- and β-subunits of G proteins. Dev. Brain Res. 56:1990;131-136.
35. Schmidt C. J., Zubiaur M., Valenzuela D., Neer E. J., Drager U. C. Go, a guanine nucleotide binding protein, is expressed during neurite extension in the embryonic mouse. J. Neurosci. Res. 38:1994;182-187.
36. o. J. Neurosci. 14:1994;2327-2338.
37. Xie R., Li L., Goshima Y., Strittmatter S. M. An activated mutant of the α subunit of Go increases neurite outgrowth via protein kinase. C. Dev. Brain Res. 87:1995;77-86.
38. Kater S. B., Mills L. R. Regulation of growth cone behavior by calcium. J. Neurosci. 11:1991;891-899.
39. 2+. Proc. Natl. Acad. Sci. USA. 85:1988;3633-3637.
40. Hescheler J., Rosenthal W., Trautwein W., Schultz G. The GTP-binding protein, Go, regulates neuronal calcium channels. Nature. 325:1987;445-447.
41. Kleuss C., Heschler J., Ewel C., Rosenthal W., Schultz G., Wittig B. Assignment of G-protein subtypes to specific receptors inducing inhibition of calcium channels. Nature. 353:1991;43-48.
42. o. J. Biol. Chem. 266:1991;22465-22471.
43. Meiri K. F., Pfenninger K. H., Willard M. Growth associated protein, GAP-43, a polypeptide that is induced when neurons extend axons, is a component of growth cones and corresponds to pp46 a major polypeptide of a subcellular fraction that is enriched in growth cones. Proc. Natl. Acad. Sci. USA. 83:1986;3537-3541.
44. Meiri K. F., Willard M., Johnson M. I. Distribution and phosphorylation of the growth associated protein GAP-43 in regenerating sympathetic neurons in culture. J. Neurosci. 8:1988;2571-2581.
45. Skene J. H. P., Jacobson R. D., Snipes G. J., MacGuire C. B., Norden J., Freeman J. A. A protein induced during nerve growth, GAP-43 is a major component of growth cone membranes. Science. 233:1986;783-785.
46. Goslin K., Schreyer D. J., Skene J. H., Banker G. A. Development of neuronal polarity: GAP-43 distinguishes axonal from dendritic growth cones. Nature. 336:1988;672-674.
47. Jay D. G. Selective destruction of protein function by chromophore-assisted laser inactivation. Proc. Natl. Acad. Sci. USA. 85:1988;5454-5458.
48. Jay D. G., Keshishian H. Laser inactivation of fasciclin I disrupts axon adhesion of grasshopper pioneer neurons. Nature. 348:1990;548-550.
49. Diamond P., Mallavarapu A., Schnipper J., Booth J., Park L., O'Connor T. P., Jay D. G. Fasciclin I and II have distinct roles in the development of grasshopper pioneer neurons. Neuron. 11:1993;1-20.
50. Chang H. Y., Takei K., Sydor A. M., Born T., Rusnak F., Jay D. G. Asymmetric retraction of growth cone filopodia following focal inactivation of calcineurin. Nature. 376:1995;868-690.
51. Wang F., Wolenski J. S., Cheney R. E., Mooseker M. S., Jay D. G. Function of Myosin-V in filopodial extension of neuronal growth cones. Science. 273:1996;660-663.
52. Sydor A. M., Su A. L., Wang F.-S., Xu A., Jay D. G. Talin and vinculin functions have distinct roles in filopodial motility in the neuronal growth cone. J. Cell Biol. 134:1996;1197-1207.
53. Vancura K., Wang P., Lee G., Jay D. G. Tau and GAP-43 are potential downstream effectors of calcineurin during growth cone motility. Am. Soc. Cell. Biol. Annu. Meeting Abstr. 1995.
54. Aigner L., Caroni P. Deletion of 43-kD growth-associated protein in primary sensory neurons leads to diminished formation and spreading of growth cones. J. Cell Biol. 123:1993;417-429.
55. Aigner L., Caroni P. Absence of persistent spreading, branching, and adhesion in GAP-43 depleted growth cones. J. Cell Biol. 128:1995;647-660.
56. Strittmatter S. M., Fankhauser C., Huang P. L., Mashimo H., Fishman M. C. Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43. Cell. 80:1995;445-452.
57. ++. Proc. Natl. Acad. Sci. USA. 94:1997;1727-1732.
58. Nobes C. D., Hall A. Rho, rac, & cdc42 GTPases: Regulators of actin structures, cell adhesion and motility. Biochem. Soc. Transact. 23:1995b;456-459.
59. Ridley A. J., Paterson H. F., Johnston C. L., Diekmann D., Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell. 70:1992;401-410.
60. Chant J., Stowers L. GTPase cascades choreographing cellular behavior: Movement, morphogenesis, and more. Cell. 81:1995;1-4.
61. Luo L., Liao Y. J., Jan L. Y., Jan Y. N. Distinct morphogenetic functions of similar small GTPases:Drosophila. Genes Dev. 8:1994;1787-1802.
62. Ridley A. J., Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell. 70:1992;389-399.
63. Burridge K., Fath K., Kelly T., Nuckolis G., Turner C. Focal adhesions: Transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu. Rev. Cell Biol. 4:1988;487-525.
64. Gumbiner B. M. Proteins associated with the cytoplasmic surface of adhesion molecules. Neuron. 11:1993;551-564.
65. Turner C. E., Burridge K. Transmembrane molecular assemblies in cell-extracellular matrix interactions. Curr. Opin. Cell. Biol. 3:1991;849-853.
66. Sastry S. K., Horwitz A. F. Integrin cytoplasmic domains: Mediators of cytoskeletal linkages and extra- and intracellular initiated transmembrane signaling. Curr. Opin. Cell. Biol. 5:1993;819-831.
67. Nobes C. D., Hall A. Rho, rac, & cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell. 81:1995a;53-62.
68. Kozma R., Ahmed S., Best A., Lim L. The Ras-related protein cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol. Cell. Biol. 15:1995;1942-1952.
69. Jalink K., Moolenaar W. H. Thrombin receptor activation causes rapid neural cell rounding and neurite retraction independent of classic second messengers. J. Cell Biol. 118:1992;411-419.
70. Jalink K., van Corven E. J., Hengeveld T., Morii N., Narumiya S., Moolenaar W. H. Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP Ribosylation of the small GTP-binding protein rho. J. Cell Biol. 126:1994;801-810.
71. Kuhn T. B., Bamburg J. R. The small GTPase rac is essential for the formation and differentiation of neurites from motorneurons mediated by extracellular matrix molecules. Am. Soc. Cell. Biol. Annu. Meeting Abstr. 1996.
72. Pfenninger K. H., Maylie-Pfenninger M. F. Lectin labeling of sprouting neurons. II. Relative movement and appearance of glycoconjugates during plasmalemmal expansion. J. Cell Biol. 89:1981;547-559.
73. Craig A. M., Wyborski R. J., Banker G. Preferential addition of newly synthesized membrane protein at axonal growth cones. Nature. 375:1995;592-594.
74. Dai J., Sheetz M. P. Axon membrane flows from the growth cone to the cell body. Cell. 83:1995;693-701.
75. Simons K., Zerial M. Rab proteins and the road maps for intracellular transport. Neuron. 11:1993;789-799.
76. Salminen A., Novick P. J. A ras-like protein is required for a post-Golgi event in yeast secretion. Cell. 49:1987;527-538.
77. Huber L. A., Dupree P., Dotti C. G. A deficiency of the small GTPase rab8 inhibits membrane traffic in developing neurons. Mol. Cell. Biol. 15:1995;918-924.
78. Huber L. A., De Hoop M. J., Dupree P., Zerial M., Simons K., Dotti C. Protein transport to the dendritic plasma membrane of cultured neurons is regulated by rab8p. J. Cell Biol. 123:1993;47-55.
79. Pagano R. E., Martin O. C., Kang H. C., Haugland R. P. A novel fluorescent ceramide analog for studying membrane traffic in animal cells: Accumulation at the Golgi apparatus results in altered spectral properties of the sphingolipid precursor. J. Cell Biol. 113:1991;1267-1279.
80. De Hoop M. J., Huber L. A., Stenmark H., Williamson E., Zerial M., Parton R. G., Dotti C. G. The involvementof the small GTP-binding protein rab5a in neuronal endocytosis. Neuron. 13:1994;11-22.
81. Chavrier P., Parton R. G., Hauri H. P., Simons K., Zerial M. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell. 62:1990;317-329.
82. Fischer von Mollard G., Mignery G. A., Baumert M., Perin M. S., Hanson T. J., Burger P. M., Jahn R., Sudhof T. C. Rab3 is a small GTP-binding protein exclusively localized to synaptic vesicles. Proc. Natl. Acad. Sci. USA. 87:1992;1988-1992.
83. Matteoli M., Takei K., Cameron R., Hurlbut P., Johnston P. A., Sudhof T. C., Jahn R., De Camilli P. Association of rab3a with synaptic vesicles at late stages of the secretory pathway. J. Cell Biol. 115:1991;625-633.
84. Oberhauser A. F., Monck J. R., Balch W. E., Fernandez J. M. Exocytic fusion is activated by rab3a peptides. Nature. 360:1992;270-273.
85. 2+. Nature. 364:1993;540-544.
86. Ayala J., Touchot N., Zahraoui A., Tavitian A., Prochiantz A. The product of rab2, a small GTP binding protein, increases neuronal adhesion, and neurite growthin vitro. Neuron. 4:1990;797-805.
87. Lamarche N., Tapon N., Stowers L., Burbelo P. D., Aspenstrom P., Bridges T., Chant J., Hall A. Rac and cdc42 induce actin polymerization and G1 cell cycle progression independently of p65PAK and the JNK/SAPK MAP kinase cascade. Cell. 87:1996;519-525.
88. Araki S., Kikuchi A., Hata Y., Isomura M., Takai Y. Regulation of reversible binding of smg p25A, a ras p21-like GTP-binding protein, to synaptic plasma membranes and vesicles by its specific regulatory protein, GDP dissociation inhibitor. J. Biol Chem. 265:1990;13007-13015.
89. Regazzi R., Kikuchi A., Takai Y., Wollheim C. B. The GTP-binding proteins in the cytosol of insulin-secreting cells are complexed to GDP dissociation inhibitor proteins. J. Biol. Chem. 267:1992;17512-17519.
90. Ren M., Zeng J., De Lemos-Chiarandini C., Rosenfeld M., Adesnik M., Sabatini D. D. In its active form, the GTP-binding protein rab8 interacts with a stress-activated protein kinase. Proc. Natl. Acad. Sci. USA. 93:1996;5151-5155.