GAP43 phosphorylation is critical for growth and branching of retinotectal arbors in zebrafish

Developmental Neurobiology

Volumn 70, Issue 13, 2010, Pages 897-911

  Leu, Byunghee ^a,b   Koch, Eric ^a,c   Schmidt, John T ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c NEW YORK INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Activity feedback; Branching control; Expression vectors; Fusion proteins; GAP43; Growth control; Phosphorylation; Protein kinase C; Retinotectal arbors; Synapse signaling

Indexed keywords

ARTICLE; FEMALE; MALE; MOTONEURON; MUSCLE CONTRACTILITY; NONHUMAN; ONTOGENY; PATTERN GENERATOR; PRIORITY JOURNAL; REGULATORY MECHANISM; SEX DIFFERENTIATION; SEXUAL BEHAVIOR; SEXUAL MATURATION; VOCAL CORD; VOCALIZATION; XENOPUS LAEVIS;

ANIMALS; CELL DIFFERENTIATION; GAP-43 PROTEIN; GROWTH CONES; NEUROGENESIS; PHOSPHORYLATION; RETINA; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION; SUPERIOR COLLICULI; VISUAL PATHWAYS; ZEBRAFISH;

EID: 78649361203     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20829     Document Type: Article

References (85)

1. Aarts LH, Schrama LH, Hage WJ, Bos JL, Gispen WH, Schotman P. 1998. B-50/GAP-43-induced formation of filopodia depends on Rho-GTPase. Mol Biol Cell 9:1279-1292.
2. Aarts LH, Verkade P, van Dalen JJ, van Rozen AJ, Gispen WH, Schrama LH, Schotman P. 1999. B-50/GAP-43 potentiates cytoskeletal reorganization in raft domains. Mol Cell Neurosci 14:85-97.
3. Alexander KA, Wakim BT, Doyle GS, Walsh KA, Storm DR. 1988. Identification and characterization of the calmodulin-binding domain of neuromodulin, a neurospecific calmodulin-binding protein. J Biol Chem 263:7544-7549.
4. Alsina B, Vu T, Cohen-Cory S. 2001. Visualizing synapse formation in arborizing optic axons in vivo: Dynamics and modulation by BDNF. Nat Neurosci 4:1093-1101.
5. Apel ED, Storm DR. 1992. Functional domains of neuromodulin (GAP-43). Perspect Dev Neurobiol 1:3-11.
6. Benowitz LI, Routtenberg A. 1997. GAP-43: An intrinsic determinant of neuronal development and plasticity. Trends Neurosci 20:84-91.
7. Bhattacharya M, Babwah AV, Ferguson SS. 2004. Small GTP-binding protein-coupled receptors. Biochem Soc Trans 32:1040-1044.
8. Bormann P, Zumsteg VM, Roth LWA, Reinhard E. 1998. Target contact regulates GAP-43 and alpha-Tubulin mRNA levels in regenerating retinal ganglion cells. J Neurosci Res 52:405-419.
9. Cantallops I, Routtenberg A. 1999. Activity-dependent regulation of axonal growth: posttranscriptional control of the GAP-43 gene by the NMDA receptor in developing hippocampus. J Neurobiol 41:208-220.
10. Clements MP, Bliss TV, Lynch MA. 1991. Increase in arachidonic acid concentration in a postsynaptic membrane fraction following the induction of long-term potentiation in the dentate gyrus. Neuroscience 45:379-389.
11. Cline HT, Constantine-Paton M. 1990. NMDA receptor agonist and antagonists alter retinal ganglion cell arbor structure in the developing frog retinotectal projection. J Neurosci 10:1197-1216.
12. Chao S, Benowitz LI, Krainc D, Irwin N. 1996. Use of a two-hybrid system to investigate molecular interactions of GAP-43. Brain Res Mol Brain Res 40:195-202.
13. Cogen J, Cohen-Cory S. 2000. Nitric oxide modulates retinal ganglion cell axon arbor remodeling in vivo. J Neurobiol 45:120-133.
14. Cohen-Cory S. 1999. BDNF modulates, but does not mediate, activity-dependent branching and remodeling of optic axon arbors in vivo. J Neurosci 19:9996-10003.
15. Cohen-Cory S, Kidane AH, Shirkey NJ, Marshak S. 2010. Brain-derived neurotrophic factor and the development of structural neuronal connectivity. Dev Neurobiol 70:271-288.
16. Colicos MA, Collins BE, Sailor MJ, Goda Y. 2001. Remodeling of synaptic actin induced by photoconductive stimulation. Cell 107:605-616.
17. Constantine-Paton M, Cline HT. 1998. LTP and activity-dependent synaptogenesis: The more alike they are, the more different they become. Curr Opin Neurobiol 8:139-148.
18. Davenport RW, Thies E, Cohen ML. 1999. Neuronal growth cone collapse triggers lateral extensions along trailing axons. Nat Neurosci 2:254-259.
19. DeGraan PN, Hens JJ, Gispen WH. 1994. Presynaptic PKC substrate B-50 (GAP-43) and neurotransmitter release: Studies with permeated synaptosomes. Neurotoxicology 15:41-47.
20. Debski EA, Cline HT. 2002. Activity-dependent mapping in the retinotectal projection. Curr Opin Neurobiol 12:93-99.
21. De La Monte SM, Federoff HJ, Ng S-C, Grabczyk E, Fishman MC. 1989. GAP-43 gene expression during development: Persistence in a distinctive set of neurons in the mature central nervous system. Dev Brain Res 46:161-168.
22. Dent EW, Tang F, Kalil K. 2003. Axon guidance by growth cones and branches: Common cytoskeletal and signaling mechanisms. Neuroscientist 9:343-353.
23. Dickson BJ, Cline H, Polleux F, Ghosh A. 2001. Making connections. Meeting: Axon guidance and neural plasticity. EMBO Rep 2:182-186.
24. Dillon C, Goda Y. 2005. The actin cytoskeleton: Integrating form and function at the synapse. Annu Rev Neurosci 28: 25-55.
25. Dumuis A, Sebben M, Haynes L, Pin JP, Bockaert J. 1988. NMDA receptors activate the arachidonic acid cascade system in striatal neurons. Nature 336:68-70.
26. Easter SS, Nicola GN. 1996. The development of vision in the zebrafish (Danio rerio). Dev Biol 180:646-663.
27. Harris WA, Holt CE, Bonhoeffer F. 1987. Retinal axons with and without their somata growing to and arborizing within the tectum of Xenopus embryos: A time-lapse video study of single fibers in vivo. Development 101:123-133.
28. He Q, Dent EW, Meiri KF. 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.
29. Hioki H, Kuramoto E, Konno M, Kameda H, Takahashi Y, Nakano T, Nakamura KC, Kaneko T. 2009. High-level transgene expression in neurons by lentivirus with Tet-Off system. Neurosci Res 63:149-154.
30. Holder N, Klein R. 1999. Eph receptors and ephrins: Effectors of morphogenesis. Development 126:2033-2044.
31. Hu B, Nikolapoulou AM, Cohen-Cory S. 2005. BDNF stabilizes synapses and maintains the structural complexity of optic axons in vivo. Development 132:4285-4298.
32. Hua JY, Smear MC, Baier H, Smith SJ. 2005. Regulation of axon growth in vivo by activity-based competition. Nature 434:1022-1026.
33. Hulo S, Alberi S, Laux T, Muller D, Caroni P. 2002. A point mutation of GAP-43 induces enhanced short-term and long-term hippocampal plasticity. Eur J Neurosci 15:1976-1982.
34. Igarishi M, Li WW, Sudo Y, Fishman MC. 1995. Ligandinduced growth cone collapse: Amplification and blockade by variant GAP-43 peptides. J Neurosci 15:5660-5667.
35. Kato H, Allen ND, Emson PC, Kiyama H. 2000. GAP-43 N-terminal translocation signal targets b-galactosidase to developing axons in a pan-neuronal transgenic mouse line. Dev Brain Res 121:109-112.
36. Kim C-H, Lisman JE. 1999. A role of actin filament in synaptic transmission and long-term potentiation. J Neurosci 19:4314-4324.
37. Klein R. 2001. Excitatory Eph receptors and adhesive ephrin ligands. Curr Opin Cell Biol 13:196-203.
38. Laux T, Fukami K, Thelen M, Golub T, Frey D, Caroni P. 2000. GAP43. MARCKS, and CAP23 modulate PI(4,5) P(2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J Cell Biol 149:1455-1472.
39. Leahy JC, Luo Y, Kent CS, Meiri KF, Vallano ML. 1993. Demonstration of presynaptic protein kinase C activation following long-term potentiation in hippocampal slices. Neuroscience 52:563-574.
40. Leu BH, Schmidt JT. 2008. Arachidonic acid as a retrograde signal controlling growth and dynamics of retinotectal arbors. Dev Neurobiol 68:18-30.
41. Li Z, Sacks DB. 2003. Elucidation of the interaction of calmodulin with the IQ motifs of IQGAP1. J Biol Chem 278:4347-4352.
42. Livet J, Weissman TA, Kang H, Draft RW, Lu J, Bennis RA, Sanes JR, et al. 2007. Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450:56-62.
43. Lom B, Hoepker V, McFarlane S. Bixby JL, Holt CE. 1998. Fibroblast growth factor receptor signaling in xenopus retinal axon extension. J Neurobiol 33:633-641.
44. Luo Y, Vallano ML. 1995. Arachidonic acid, but not sodium nitroprusside, stimulates presynaptic protein kinase C and phosphorylation of GAP-43 in rat hippocampal slices and synaptosomes. J Neurochem 64:1808-1818.
45. Marshak S, Nikolapoulou AM, Dirks R, Martens GJ, Cohen-Cory S. 2007. Cell-autonomous TrkB signaling in presynaptic retinal ganglion cells mediates axon arbor growth and synapse maturation during the establishment of retinotectal synaptic connectivity. J Neurosci 27:2444-2456.
46. McLaughlin T, Hindges R, O'Leary DD. 2003. Regulation of axial patterning of the retina and its topographic mapping in the brain. Curr Opin Neurobiol 13:57-69.
47. Meiri KF, Saffell JL, Walsh SF, Doherty P. 1998. Neurite outgrowth stimulated by neural cell adhesion molecules (NCAM) requires growth associated protein-43 (GAP43) function and is associated with GAP-43 phosphorylation in growth cones. J Neurosci 18:10429-10437.
48. Meyer MP, Smith SJ. 2006. Evidence from in vivo imaging that synaptogenesis guides the growth and branching of axonal arbors by two distinct mechanisms. J Neurosci 26:3604-3613.
49. Moss DJ, Fernyhough P, Chapman K, Baizer L, Bray D, Allsopp T. 1990. Chicken growth-associated protein GAP-43 is tightly bound to the actin-rich neuronal membrane skeleton. J Neurochem 54:729-736.
50. Muzzio IA, Gandhi CC, Manyam U, Pesnell A, Matzel LD. 2001. Receptor-stimulated phospholipase A(2) liberates arachidonic acid and regulates neuronal excitability through protein kinase C. J Neurophysiol 85:1639-1647.
51. Nielander HB, Schrama LH, van Rozen AJ, Kasperaitis M, Oestreicher AB, Gispen WH, Schotman P. 1990. Mutation of serine 41 in the neuron-specific protein B-50 (GAP-43) prohibits phosphorylation by protein kinase C. J Neurochem 55:1442-1445.
52. Nishizaki T, Nomura T, Matsuoka T, Enikolopov G, Sumikawa K. 1999. Arachidonic acid induces a long-lasting facilitation of hippocampal synaptic transmission by modulating PKC activity and nicotinic ACh receptors. Mol Brain Res 69:263-272.
53. Oestreicher AB, De Graan PN, Gispen WH, Verhaagen J, Schrama LH. 1997. B-50, the growth associated protein-43: Modulation of cell morphology and communication in the nervous system. Prog Neurobiol 53:627-686.
54. Okamoto K-I, Nagai T, Miyawaki A, Hayashi Y. 2004. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat Neurosci 7:1104-1112.
55. Pascale A, Amadio M, Scapagnini G, Lanni C, Racchi M, Provenzani A, Govoni S, et al. 2005. Neuronal ELAV proteins enhance mRNA stability by a PKCalpha-dependent pathway. PNASUSA 102:12065-12070.
56. Pascale A, Gusev PA, Amadio M, Dottorini T, Govoni S, Alkon D, Quattrone, A. 2004. Increase of the RNA-binding protein HuD and posttranscriptional up-regulation of the GAP-43 gene during spatial memory. PNASUSA 101:1217-1222.
57. Pavlidis P, Montgomery J, Madison DV. 2000. Presynaptic protein kinase C activity supports long-term potentiation at synapses between individual hippocampal neurons. J Neurosci 20:4497-4505.
58. Perrone-Bizzozero N, Bolognani F. 2002. Role of HuD and other RNA-binding proteins in neural development and plasticity. J Neurosci Res 68:121-126.
59. Rajan I, Witte S, Cline HT. 1999. NMDA receptor activity stabilizes presynaptic retinotectal axons and postsynaptic optic tectal cell dendrites in vivo. J Neurobiol 38:357-368.
60. Rekart JL, Meiri K, Routtenberg A. 2004. Hippocampal-dependent memory is impaired in heterozygous GAP-43 knockout mice. Hippocampus 15:1-7.
61. Rico B, Beggs HE, Schahin-Reed D, Kimes N, Schmidt A, Reichardt LF. 2004. Control of axonal branching and synapse formation by focal adhesion kinase. Nat Neurosci 7:1059-1069.
62. Roskies AL, O'Leary DD. 1994. Control of topographic retinal axon branching by inhibitory membrane-bound molecules. Science 265:799-803.
63. Routtenberg A, Cantallops I, Zaffuto S, Serano P, Namgung U. 2000. Enhanced learning after genetic overexpression of a brain growth protein. Proc Natl Acad Sci USA 97:7657-7662.
64. Saffell JL, Williams EJ, Mason IJ, Walsh FS, Doherty P. 1997. Expression of a dominant negative FGF receptor inhibits axonal outgrowth and FGF receptor phosphorylation stimulated by CAMs. Neuron 18:231-242.
65. Sanfeliu C, Hunt A, Patel AJ. 1990. Exposure to N-methyl-D-aspartate increases release of arachidonic acid in primary cultures of rat hippocampal neurons and not in astrocytes. Brain Res 526:241-248.
66. Schaechter JD, Benowitz LI. 1993. Activation of protein kinase C by arachidonic acid selectively enhances the phosphorylation of GAP-43 in nerve terminal membranes. J Neurosci 13:4361-4371.
67. Schmidt JT. 1990. Long-term potentiation and activity-dependent retinotopic sharpening in the regenerating retinotectal projection of goldfish: common sensitive period and sensitivity to NMDA blockers. J Neurosci 10:233-246.
68. Schmidt JT. 2004. Activity-driven sharpening of the retinotectal projection: The search for retrograde synaptic signaling pathways. J Neurobiol 59:114-133.
69. Schmidt JT, Buzzard M, Borress R, Dhillon S. 2000. MK801 increases retinotectal arbor size in developing zebrafish without affecting kinetics of branch elimination and addition. J Neurobiol 42:303-314.
70. Schmidt JT, Fleming MR, Leu B. 2004. Presynaptic protein kinase C controls maturation and branch dynamics of developing retinotectal arbors: Possible role in activitydriven sharpening. J Neurobiol 58:328-340.
71. Slemmon JR, Martzen MR. 1994. Neuromodulin (GAP-43) can regulate a calmodulin-dependent target in vitro. Biochem 33:5653-5660.
72. Smith CL, Afroz R, Bassell GJ, Furneaux HM, Perrone-Bizzozero N, Burry RW. 2004. GAP-43 mRNA in growth cones is associated with HuD and ribosomes. J Neurobiol 61:222-235.
73. Stella N, Pellerin L, Magistretti PJ. 1995. Modulation of the glutamate-evoked release of arachidonic acid from mouse cortical neurons: Involvement of a pH-sensitive membrane phospholipase A2. J Neurosci 15:3307-3317.
74. Strittmatter SM, Igarishi M, Fishman MC. 1994. GAP-43 amino terminal peptides modulate growth cone morphology and neurite outgrowth. J Neurosci 14:5503-5513.
75. Strittmatter SM, Valenzuela D, Fishman MC. 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(Part 1):195-204.
76. Szebenyi G, Callaway JL, Dent EW, Kalil K. 1998. Interstitial branches develop from active regions of the axon demarcated by the primary growth cone during pausing behaviors. J Neurosci 18:7930-7940.
77. Tejero-Diez P, Rodriguez-Sanchez P, Martin-Cofreces NB, Diez-Guerra FJ. 2000. bFGF stimulates GAP-43 phosphorylation at ser41 and modifies its intracellular localization in cultured hippocampal neurons. Mol Cell Neurosci 16:766-780.
78. Wahl S, Barth H, Ciossek T, Aktories K, Mueller BK. 2000. Ephrin-A5 induces collapse of growth cones by activating Rho and Rho kinase. J Cell Biol 149:263-270.
79. Wiederkehr A, Staple J, 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.
80. Williams EJ, Furness J, Walsh FS, Doherty P. 1994. Characterization of the second messenger pathway underlying neurite outgrowth stimulated by FGF. Development 120:1685-1693.
81. Williams JH, Errington ML, Lynch MA, Bliss TVP. 1989. Arachidonic acid induces a long-term activity-dependent enhancement of synaptic transmission in the hippocampus. Nature 341:739-742.
82. Xiao T, Roeser T, Staub W, Baier H. 2005. A GFP-based genetic screen reveals mutations that disrupt the architecture of the zebrafish retinotectal projection. Development 132:2955-2967.
83. Yates PA, Roskies AL, McLaughlin T, O'Leary DD. 2001. Topographic-specific axon branching controlled by ephrin-As is the critical event in retinotectal map development. J Neurosci 21:8548-8563.
84. Zhang W, Benson DL. 2001. Stages of synapse development by dependence on F-actin. J Neurosci 21:5169-5181.
85. Zhu Q, Julien JP. 1999. A key role for GAP-43 in retinotectal topographic organization. Exp Neurol 155:228-242.