Presynaptic Protein Kinase C Controls Maturation and Branch Dynamics of Developing Retinotectal Arbors: Possible Role in Activity-Driven Sharpening

Journal of Neurobiology

Volumn 58, Issue 3, 2004, Pages 328-340

  Schmidt, John T ^a   Fleming, Matthew R ^a   Leu, Byunghee ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Bisindolylmaleimide; C kinase; Calphostin C; DAG lipase; DiO; NMDA receptor; Retinotopic map; Synaptic plasticity; Videomicroscopy

Indexed keywords

1,6 HEXAMETHYLENEDICARBAMIC ACID BIS(CYCLOHEXANONE OXIME) ESTER; ARACHIDONIC ACID; BISINDOLYLMALEIMIDE; CALPHOSTIN C; DIZOCILPINE; F ACTIN; LIPOPROTEIN LIPASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NERVE CELL ADHESION MOLECULE; PROTEIN KINASE C INHIBITOR; RINGER SOLUTION;

ANIMAL EXPERIMENT; ARACHIDONIC ACID METABOLISM; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVE FIBER GROWTH; NONHUMAN; OPTIC TRACT; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RETINA GANGLION CELL; RETINOTECTAL PROJECTION; VISION; XENOPUS; ZEBRA FISH;

ACTINS; ACTION POTENTIALS; ANIMALS; ARACHIDONIC ACID; CELL DIFFERENTIATION; DIZOCILPINE MALEATE; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; GAP-43 PROTEIN; GROWTH CONES; LARVA; LIPOPROTEIN LIPASE; NEURAL CELL ADHESION MOLECULE L1; NEURONAL PLASTICITY; PRESYNAPTIC TERMINALS; PROTEIN KINASE C; RECEPTORS, N-METHYL-D-ASPARTATE; RETINA; RETINAL GANGLION CELLS; SUPERIOR COLLICULUS; SYNAPTIC TRANSMISSION; VISUAL PATHWAYS; ZEBRAFISH;

EID: 1042289723     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10286     Document Type: Article

References (50)

1. Balkowiec A, Katz DM. 2000. Activity-dependent release of endogenous Brain-Derived Neurotrophic Factor from primary sensory neurons detected by ELISA in Situ. J Neurosci 20:7417-7423.
2. Bernhardt RR, Tongiorgi E, Anzini P, Schachner M. 1996. Increased expression of specific recognition molecules by retinal ganglion cells and by optic pathway glia accompanies the successful regeneration of retinal axons in adult zebrafish. J Comp Neurol 376:253-264.
3. Bliss TVP, Collingridge GL. 1993. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361:31-39.
4. Bredt DS, Snyder SH. 1990. Isolation of nitric oxide synthetase, a calcium-calmodulin-requiring enzyme. Proc Natl Acad Sci USA 87:682-685.
5. Bruns RF, Miller FD, Merriman RL, Howbert JJ, Heath WF, Kobayashi E, Takahashi I, Tamaoki T, Nakano H. 1991. Inhibition of protein kinase C by calphostin C is light dependent. Biochem Biophys Res Commun 176: 288-293.
6. Cohen-Cory S. 2002. The developing synapse: Construction and modulation of synaptic structures and circuits. Science 298:770-776.
7. Colicos MA, Collins BE, Sailor MJ, Goda Y. 2001. Remodeling of synaptic actin induced by photoconductive stimulation. Cell 107:605-616.
8. Davis PD, Elliott LH, Harris WH, Hill CH, Hurst SA, Keech E, Kumar MK, Lawton G, Nixon JS, Wilkinson SE. 1992. Inhibitors of protein kinase C. 2. Substituted bisindolylmaleimide with improved potency and selectivity. J Med Chem 35:994-1001.
9. Doherty P, Walsh FS. 1994. Signal transduction events underlying neurite outgrowth stimulated by cell adhesion molecules. Curr Opin Neurobiol 4:49-55.
10. Dorman RV, Schwartz MA, Terrian DM. 1988. Depolarization induced [3H]arachidonic acid accumulation: Effects of external Ca++ and phospholipase inhibitors. Brain Res Bull 21:445-450.
11. Drapeau C, Pellerin L, Wolfe LS, Avoli M. 1990. Long-term changes of synaptic transmission induced by arachidonic acid in the CA1 subfield of the rat hippocampus. Neurosci Lett 115:286-292.
12. Dumuis A, Sebben M, Haynes L, Pin J-P, Bockaert J. 1988. NMDA receptors activate the arachidonic acid cascade system in striatal neurons. Nature 336:68-70.
13. Goodman CS, Shatz CJ. 1993. Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell/Neuron (Suppl) 72:77-98.
14. 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.
15. Haruta T, Takami N, Ohmura M, Misumi Y, Ikehara Y. 1997. Ca+ +-dependent interaction of the growth-associated protein GAP-43 with the synaptic core complex. Biochem J 325:455-463.
16. He Q, Dent EW, Meiri KF. 1997. Modulation of actin filament behavior by GAP-43 is dependent on the phosphorylation status of serine 41, the protein kinase C site. J Neurosci 17:3515-3524.
17. Jessel TM, Kandel ER. 1993. Synaptic transmission: a bidirectional and self-modifiable form of cell-cell communication. Cell/Neuron (Suppl) 72:1-30.
18. Kaethner RJ, Stuermer CAO. 1994. Growth behavior of retinotectal axons in live zebrafish embryos under TTX-induced neural impulse blockade. J Neurobiol 25:781-796.
19. Kobayashi E, Nakano H, Morimoto M, Tamaoki T. 1989. Calphostin C (UCN-1028C), a novel microbial compound, is a highly potent and specific inhibitor of protein kinase C. Biochem Biophys Res Commun 159:548-553.
20. 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.
21. Linden DJ, Sheu FS, Murakami K, Routtenberg A. 1987. Enhancement of long-term potentiation by cis-unsaturated fatty acid: Relation to protein kinase C and phospholipase A2. J Neurosci 7:3783-3792.
22. Lom B, Hopker V, McFarlane S, Bixby JL, Holt C. 1998. Fibroblast growth factor receptor signaling in Xenopus retinal axon extension. J Neurobiol 37:633-641.
23. 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.
24. Massicotte G, Oliver M, Lynch G, Baudry M. 1990. Effect of bromophenacyl bromide, a phospholipase A2 inhibitor, on the induction and maintenance of LTP in hippocampal slices. Brain Res 537:49-53.
25. Mayford M, Wang J, Kandel E, O'Dell TJ. 1995. CamKII regulates the frequency-response function of hippocampal synapses for the production of both LTD and LTP. Cell 81:891-904.
26. McGahon B, Lynch MA. 1996. The synergism between metabotropic glutamate receptor activation and arachidonic acid on glutamate release is occluded by induction of LTP in the dentate gyrus. Neuroscience 72:847-855.
27. McGahon B, Lynch MA. 1998. Analysis of the interaction between arachidonic acid and metabotropic glutamate receptor activation reveals that phospholipase C acts as a coincidence detector in the expression of long-term potentiation in the rat dentate gyrus. Hippocampus 8:48-56.
28. Meiri KF, Saffell JL, Walsh FS, Doherty P. 1998. Neurite outgrowth stimulated by neural cell adhesion molecules requires growth-associated protein-43 (GAP-43) function and is associated with GAP-43 phosphorylation in growth cones. J Neurosci 18:10429-10437.
29. Nishizaki T, Nomura T, Matsuoka T, Tsujishita Y. 1999. Arachidonic acid as a messenger for the expression of long term potentiation. Biochem Biophys Res Commun 254:446-449.
30. O'Rourke NA, Cline HT, Fraser SE. 1994. Rapid remodeling of retinal arbors in the tectum with and without blockade of synaptic transmission. Neuron 12:921-934.
31. 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.
32. Piomelli D, Greengard P. 1991. Bidirectional control of phospholipase A2 by Ca++/calmodulin-dependent protein kinase II, cAMP-dependent protein kinase, and casein kinase II. Proc Natl Acad Sci USA 88:6770-6774.
33. 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.
34. Renteria R, Constantine-Paton M. 1999. Nitric oxide in the retinotectal system: a signal but not a retrograde messenger during map refinement and segregation. J Neurosci 19:7066-7076.
35. Renteria RC, Constantine-Paton M. 1996. Exogenous nitric oxide causes collapse of retinal ganglion cell axonal growth cones. J Neurobiol 29:415-428.
36. Routtenberg A, Cantallops I, Zaffuto S, Serrano P, Namgung U. 2000. Enhanced learning after genetic overexpression of a brain growth protein. Proc Natl Acad Sci USA 97:7657-7662.
37. Sanfeliu C, Hunt A, Patel AJ. 1990. Exposure to NMDA increased release of arachidonic acid in primary cultures of rat hippocampal neurones and not in astrocytes. Brain Res 526:241-248.
38. 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.
39. Schmidt JT. 1994. C-kinase manipulations disrupt activity-driven retinotopic sharpening in regenerating goldfish retinotectal projection. J Neurobiol 25:555-570.
40. Schmidt JT. 1998. Up-regulation of protein kinase C in regenerating optic nerve fibers of goldfish: Immunohistochemistry and kinase activity assay. J Neurobiol 36: 315-324.
41. Schmidt JT, Buzzard M. 1990. Activity-driven sharpening of the regenerating retinotectal projection: Effects of blocking or synchronizing activity on the morphology of individual regenerating arbors. J Neurobiol 21:900-917.
42. Schmidt JT, Buzzard M. 1993. Activity-driven sharpening of the retinotectal projection in goldfish: Development under stroboscopic illumination prevents sharpening. J Neurobiol 24:384-399.
43. 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.
44. Schmidt JT, Fleming MR, Leu BH. 2002. Arachidonic acid controls developing retinotectal arbor structure and dynamics in zebrafish. Neurosci Abstr 28:130.16.
45. Toullec D, Pianetti P, Coste H, Bellevergue P, Grand-Perret T, Ajakane M, Baudet V, Boissin P, Boursier E, Loriolle F, et al. 1991. The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J Biol Chem 266:15771-15781.
46. Williams EJ, Mittal B, Walsh FS, Doherty P. 1995. A Ca++/calmodulin kinase inhibitor, KN-62, inhibits neurite outgrowth stimulated by CAMs and FGF. Mol Cell Neurosci 6:69-79.
47. Winer BJ. 1962. Statistical Principles in Experimental Design. New York: McGraw Hill. 672p.
48. Witte S, Stier H, Cline HT. 1996. In vivo observations of timecourse and distribution of morphological dynamics in Xenopus retinotectal axon arbors. J Neurobiol 31:219-234.
49. Zou DJ, Cline HT. 1996. Expression of constitutively active CamKII in target tissue modifies presynaptic axon arbor growth. Neuron 16:529-539.
50. Zou DJ, Cline HT. 1999. Postsynaptic calcium/calmodulin kinase II is required to limit elaboration of presynaptic and postsynaptic neuronal arbors. J Neurosci 19:9809-9818.