GAP-43 augmentation of G protein-mediated signal transduction is regulated by both phosphorylation and palmitoylation

Journal of Neurochemistry

Volumn 70, Issue 3, 1998, Pages 983-992

  Nakamura, Fumio ^a   Strittmatter, Philipp ^a   Strittmatter, Stephen M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calmodulin; GAP 43; GTP binding protein; Palmitoylation; Protein kinase C

Indexed keywords

ASPARTIC ACID; CALMODULIN; CHLORIDE ION; GUANINE NUCLEOTIDE BINDING PROTEIN; MUTANT PROTEIN; NEUROMODULIN; PROTEIN KINASE C; SERINE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CHLORIDE CURRENT; CONTROLLED STUDY; NONHUMAN; OOCYTE; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; XENOPUS LAEVIS;

ANIMALIA; XENOPUS LAEVIS;

EID: 0031936177     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1998.70030983.x     Document Type: Article

References (48)

1. 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.
2. Alexander K. A., Cimler B. M., Meier K. E., and Storm D. R. (1987) Regulation of calmodulin binding to P-57. A neurospecific calmodulin binding protein. J. Biol. Chem. 262, 6108-6113.
3. Alexander K. A., Wakim B. T., Doyle G. S., Walsh K. A., and Storm D. R. (1988) Identification and characterization of the calmodulin-binding domain of neuromodulin, a neurospecific calmodulin-binding protein. J. Biol. Chem. 263, 7544-7549.
4. Apel E. D., Byford M. F., Au D., Walsh K. A., and Storm D. R. (1990) Identification of the protein kinase C phosphorylation site in neuromodulin. Biochemistry 29, 2330-2335.
5. Baetge E. E. and Hammang J. P. (1991) Neurite outgrowth in PC12 cells deficient in GAP-43. Neuron 6, 21-30.
6. Benowitz L. I. and Routtenberg A. (1997) GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 20, 84-91.
7. Chapman E. R., Au D., Alexander K. A., Nicolson T. A., and Storm D. R. (1991) Characterization of the calmodulin binding domain of neuromodulin. Functional significance of serine 41 and phenylalanine 42. J. Biol. Chem. 266, 207-213.
8. Coggins P. J. and Zwiers H. (1989) Evidence for single protein kinase C-mediated phosphorylation site in rat brain B-50. J. Neurochem. 53, 1895-1901.
9. Coggins P. J., McLean K., Nagy A., and Zwiers H. (1993) ADP-ribosylation of the neuronal phosphoprotein B-50/GAP-43. J. Neurochem. 60, 368-371.
10. Dekker L. V., De Graan P. N. E., Oestreicher A. B., Versteeg D. H. G., and Gispen W. H. (1989) Inhibition of noradrenaline release by antibodies against B-50 (GAP-43). Nature 342, 74-76.
11. Gamby C., Waage M. C., Allen R. G., and Baier L. (1996) Analysis of the role of calmodulin binding and sequestration in neuromodulin (GAP-43) function. J. Biol. Chem. 271, 26698-26705.
12. Gianotti C., Nunzi M. G., Gispen W. H., and Corradetti R. (1992) Phosphorylation of the presynaptic protein B-50 (GAP-43) is increased during electrically induced long-term potentiation. Neuron 8, 843-848.
13. Hess D. T., Patterson S. I., Smith D. S., and Skene J. H. P. (1993) Neuronal growth cone collapse and inhibition of protein fatty acylation by nitric oxide. Nature 366, 562-565.
14. Hirata M., Saito N., Kono M., and Tanaka C. (1991) Differential expression of the β I- and β II-PKC subspecies in the postnatal developing rat brain; an immunocytochemical study. Dev. Brain Res. 62, 229-238.
15. Igarashi M. and Komiya Y. (1991) Subtypes of protein kinase C in isolated nerve growth cones: only type II is associated with the membrane skeleton from growth cones. Biochem. Biophys. Res. Commun. 178, 751-757.
16. Igarashi M., Li W. W., Sudo Y., and Fishman M. C. (1995) Ligand-induced growth cone collapse: amplification and blockade by variant GAP-43 peptides. J. Neurosci. 15, 5660-5667.
17. Katz F., Ellis L., and Pfenninger K. H. (1985) Nerve growth cones isolated from fetal rat brain. III. Calcium-dependent protein phosphorylation. J. Neurosci. 5, 1402-1411.
18. Laurent A., Basset M., Doree M., and LePeuch C. J. (1988) Involvement of a calcium-phospholipid-dependent protein kinase in the maturation of Xenopus laevis oocytes. FEBS Lett. 226, 324-330.
19. Lechleiter J. D. and Clapham D. E. (1992) Molecular mechanisms of intracellular calcium excitability in X. laevis oocytes. Cell 69, 283-294.
20. Lechleiter J., Girard S., Clapham D., and Peralta E. (1991) Subcellular patterns of calcium release determined by G protein-specific residues of muscarinic receptors. Nature 350, 505-508.
21. Matsumoto M. and Barnard E. A. (1994) Effects of an activator and an inhibitor of protein kinase C on serotonin receptors induced by rat brain mRNA in Xenopus oocytes. Neurosci. Lett. 167, 183-186.
22. Mein K. F., Pfenninger K. H., and Willard M. B. (1986) 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 traction enriched in growth cones. Proc. Natl. Acad. Sci. USA 83, 3537-3541.
23. Milligan G., Parenti M., and Magee A. I. (1995) The dynamic role of palmitoylation in signal transduction. Trends Biochem. Sci. 20, 181-187.
24. Parker I. and Miledi R. (1989) Nonlinearity and facilitation in phosphoinositide signaling studies by the use of caged inositol triphosphate in Xenopus oocytes. J. Neurosci. 9, 4068-4077.
25. Philibert K. and Zwiers H. (1995) Evidence for multisite ADP-ribosylation of neuronal phosphoprotein B-50/GAP-43. Mol. Cell. Biochem. 149-150, 183-190.
26. Ross E. M. (1995) Protein modification. Palmitoylation in G-protein signaling pathways. Curr. Biol. 5, 107-109.
27. Routtenberg A. (1985) Protein kinase C activation leading to protein F1 phosphorylation may regulate synaptic plasticity by presynaptic terminal growth. Behav. Neural Biol. 44, 186-200.
28. Sahara S., Sato K., Aoto M., Ohnishi T., Kaise H., Koide H., Ogita K., and Fukami Y. (1992) Characterization of protein kinase C in Xenopus oocytes. Biochem. Biophys. Res. Commun. 182, 105-114.
29. Sakuta H., Sekiguchi M., Okamoto K., and Sakai Y. (1991) Desensitization of endogenous angiotensin II receptors in Xenopus oocytes: a role of protein kinase C. Eur. J. Pharmacol. 208, 41-47.
30. Shea T. B., Perrone B. N., 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.
31. Skene J. H. P. (1989) Axonal growth-associated proteins. Annu. Rev. Neurosci. 12, 127-156.
32. Skene J. H. and Virag I. (1989) Posttranslational membrane attachment and dynamic fatty acylation of a neuronal growth cone protein GAP-43. J. Cell Biol. 108, 613-624.
33. Skene J. H. P., Jacobson R. D., Snipes G. J., McGuire C. B., Norden J. J., and Freeman J. A. (1986) A protein induced during nerve growth (GAP-43) is a major component of growth-cone membranes. Science 233, 783-785.
34. Sternweis P. C. and Robishaw J. D. (1984) Isolation of two proteins with high affinity for guanine nucleotides from membranes of bovine brain. J. Biol. Chem. 259, 13806-13813.
35. o is a major growth cone protein subject to regulation by GAP-43. Nature 344, 836-841.
36. o. GAP-43 stimulates isolated α subunits by a novel mechanism. J. Biol. Chem. 266, 22465-22471.
37. Strittmatter S. M., Vartanian T., and Fishman M. C. (1992) GAP-43 as a plasticity protein in neuronal form and repair. J. Neurobiol. 23, 507-520.
38. Strittmatter S. M., Cannon S. C., Ross E. M., Higashijima T., and Fishman M. C. (1993) GAP-43 augments G protein-coupled receptor transduction in Xenopus laevis oocytes. Proc. Natl. Acad. Sci. USA 90, 5327-5331.
39. o promote an increased number of neurites per cell. J. Neurosci. 14, 2327-2338.
40. Strittmatter S. M., Igarashi M., and Fishman M. C. (1994b) GAP-43 amino terminal peptides modulate growth cone morphology and neunte outgrowth. J. Neurosci. 14, 5503-5513.
41. Strittmatter S. M., Valenzuela D., and Fishman M. C. (1994c) 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.
42. 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.
43. o stimulation by GAP-43. EMBO J. 11, 2095-2102.
44. Weiner M. P., Costa G. L., Schoettlin W., Cline J., Mathur E., and Bauer J. C. (1994) Site-directed mutagenesis of double-stranded DNA by the polymerase chain reaction. Gene 151, 119-123.
45. 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.
46. o increases neurite outgrowth via protein kinase C. Dev. Brain Res. 87, 77-86.
47. Yankner B. A., Benowitz L. I., Villa-Komaroff L., and Neve R. L. (1990) Transfection of PC12 cells with the human GAP43 gene: effects on neurite outgrowth and regeneration. Mol. Brain Res 7, 39-44.
48. Zuber M. X., Strittmatter S. M., and Fishman M. C. (1989) A growth cone membrane targeting signal in the amino terminus of a neuronal protein. Nature 341, 345-348.