Synapse number and synaptic efficacy are regulated by presynaptic cAMP and protein kinase A

Journal of Neuroscience

Volumn 23, Issue 10, 2003, Pages 4146-4155

  Munno, David W ^a   Prince, David J ^a   Syed, Naweed I ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

cAMP; Cell culture; Lymnaea; PKA; Synapse formation; Synaptic plasticity; Trophic factors

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; ISOQUINOLINE DERIVATIVE; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; NERVE GROWTH FACTOR; SULFONAMIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL FUNCTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME MECHANISM; INNERVATION; LYMNAEA; NERVE CELL CULTURE; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN FUNCTION; SYNAPSE; SYNAPTOGENESIS; ANIMAL; BRAIN; CELL COMMUNICATION; CELL CULTURE; CELL SEPARATION; CULTURE MEDIUM; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; GROWTH, DEVELOPMENT AND AGING; HIPPOCAMPUS; LONG TERM POTENTIATION; METABOLISM; NERVE CELL INHIBITION; NERVE TRACT; PHYSIOLOGY; SYNAPTIC TRANSMISSION; SYNAPTOSOME;

ANIMALS; BRAIN; CELL COMMUNICATION; CELL SEPARATION; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; ISOQUINOLINES; LONG-TERM POTENTIATION; LYMNAEA; NERVE GROWTH FACTORS; NEURAL INHIBITION; NEURAL PATHWAYS; NEURONAL PLASTICITY; NEUROTRANSMITTER AGENTS; PRESYNAPTIC TERMINALS; SULFONAMIDES; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 0038718782     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-10-04146.2003     Document Type: Article

References (56)

1. Ahmari SE, Smith SJ (2002) Knowing a nascent synapse when you see it. Neuron 34:333-336.
2. Casadio A, Martin KC, Giustetto M, Zhu H, Chen M, Bartsch D, Bailey CH, Kandel ER (1999) A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 99:221-237.
3. Colledge M, Dean RA, Scott GK, Langeberg LK, Huganir RL, Scott JD (2000) Targeting of PKA to glutamate receptors through a MAGUK-AKAP complex. Neuron 27:107-119.
4. Colman H, Nabekura J, Lichtman JW (1997) Alterations in synaptic strength preceding axon withdrawal. Science 275:356-361.
5. Davis GW, Bezprozvanny I (2001) Maintaining the stability of neural function: a homeostatic hypothesis. Annu Rev Physiol 63:847-869.
6. Davis GW, Goodman CS (1998a) Synapse-specific control of synaptic efficacy at the terminals of a single neuron. Nature 392:82-86.
7. Davis GW, Goodman CS (1998b) Genetic analysis of synaptic development and plasticity: homeostatic regulation of synaptic efficacy. Curr Opin Neurobiol 8:149-156.
8. Davis GW, DiAntonio A, Petersen SA, Goodman CS (1998) Postsynaptic PKA controls quantal size and reveals a retrograde signal that regulates presynaptic transmitter release in Drosophila. Neuron 20:305-315.
9. Desai NS, Cudmore RH, Nelson SB, Turrigiano GG (2002) Critical periods for experience-dependent synaptic scaling in visual cortex. Nat Neurosci 5:783-789.
10. Diefenbach TJ, Guthrie PB, Kater SB (2000) Stimulus history alters behavioral response of neuronal growth cortes. J Neurosci 20:1484-1494.
11. Fainzilber M, Smit AB, Syed NI, Wildering WC, Hermann PM, van der Schors RC, Jimenez C, Li KW, van Minnen J, Bulloch AG, Ibanez CF, Geraerts WP (1996) CRNF, a molluscan neurotrophic factor that interacts with the p75 neurotrophin receptor. Science 274:1540-1543.
12. Feng ZP, Klumperman J, Lukowiak K, Syed NI (1997) In vitro synaptogenesis between the somata of identified Lymnaea neurons requires protein synthesis but not extrinsic growth factors or substrate adhesion molecules. J Neurosci 17:7839-7849.
13. Garner CC, Zhai RG, Gundelfinger ED, Ziv NE (2002) Molecular mechanisms of CNS synaptogenesis. Trends Neurosci 25:243-251.
14. Hamakawa T, Woodin MA, Bjorgum MC, Painter SD, Takasaki M, Lukowiak K, Nagle GT, Syed NI (1999) Excitatory synaptogenesis between identified Lymnaea neurons requires extrinsic trophic factors and is mediated by receptor tyrosine kinases. J Neurosci 19:9306-9312.
15. Hermann PM, van Kesteren RE, Wildering WC, Painter SD, Reno JM, Smith JS, Kumar SB, Geraerts WP, Ericsson LH, Smit AB, Bulloch AG, Nagle GT (2000) Neurotrophic actions of a novel molluscan epidermal growth factor. J Neurosci 20:6355-6364.
16. Hilfiker S, Czernik AJ, Greengard P, Augustine GJ (2001) Tonically active protein kinase A regulates neurotransmitter release at the squid giant synapse. J Physiol (Lond) 531:141-146.
17. Huang YY, Li XC, Kandel ER (1994) cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell 79:69-79.
18. Ichise T, Kano M, Hashimoto K, Yanagihara D, Nakao K, Shigemoto R, Katsuki M, Aiba A (2000) mGluR1 in cerebellar Purkinje cells essential for long-term depression, synapse elimination, and motor coordination. Science 288:1832-1835.
19. Kim JH, Huganir RL (1999) Organization and regulation of proteins at synapses. Curr Opin Cell Biol 11:248-254.
20. Kimura S, Uchiyama S, Takahashi HE, Shibuki K (1998) cAMP-dependent long-term potentiation of nitric oxide release from cerebellar parallel fibers in rats. J Neurosci 18:8551-8558.
21. Leslie KR, Nelson SB, Turrigiano GG (2001) Postsynaptic depolarization scales quantal amplitude in cortical pyramidal neurons. J Neurosci 21:RC170(1-6).
22. Lissin DV, Gomperts SN, Carroll RC, Christine CW, Kalman D, Kitamura M, Hardy S, Nicoll RA, Malenka RC, von Zastrow M (1998) Activity differentially regulates the surface expression of synaptic AMPA and NMDA glutamate receptors. Proc Natl Acad Sci USA 95:7097-7102.
23. Liu Y, Fields RD, Festoff BW, Nelson PG (1994a) Proteolytic action of thrombin is required for electrical activity-dependent synapse reduction. Proc Natl Acad Sci USA 91:10300-10304.
24. Liu Y, Fields RD, Fitzgerald S, Festoff BW, Nelson PG (1994b) Proteolytic activity, synapse elimination, and the Hebb synapse. J Neurobiol 25:325-335.
25. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
26. Marek KW, Ng N, Fetter R, Smolik S, Goodman CS, Davis GW (2000) A genetic analysis of synaptic development: pre- and postsynaptic dCBP control transmitter release at the Drosophila NMJ. Neuron 25:537-547.
27. Martin KC, Kandel ER (1996) Cell adhesion molecules, CREB and the formation of new synaptic connections. Neuron 17:567-570.
28. Martin KC, Casadio A, Zhu H, Yaping E, Rose JC, Chen M, Bailey CH, Kandel ER (1997a) Synapse-specific, long-term facilitation of Aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91:927-938.
29. Martin KC, Michael D, Rose JC, Barad M, Casadio A, Zhu H, Kandel ER (1997b) MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron 18:899-912.
30. McAllister AK, Katz LC, Lo DC (1999) Neurotrophins and synaptic plasticity. Annu Rev Neurosci 22:295-318.
31. Meems R, Munno DW, van Minnen J, Syed NI (2003) Synapse formation between isolated axons requires presynaptic soma and re-distribution of postsynaptic AChRs. J Neurophysiol, in press.
32. Mellor J, Nicoll RA, Schmitz D (2002) Mediation of hippocampal mossy fiber long-term potentiation by presynaptic Ih channels. Science 295:143-147.
33. Murthy VN, Schikorski T, Stevens CF, Zhu Y (2001) Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32:673-682.
34. Nguyen QT, Lichtman JW (1996) Mechanism of synapse disassembly at the developing neuromuscular junction. Curr Opin Neurobiol 6:104-112.
35. Nguyen QT, Parsadanian AS, Snider WD, Lichtman JW (1998) Hyperinnervation of neuromuscular junctions caused by GDNF overexpression in muscle. Science 279:1725-1729.
36. Okada M, Nutt DJ, Murakami T, Zhu G, Kamata A, Kawata Y, Kaneko S (2001) Adenosine receptor subtypes modulate two major functional pathways for hippocampal serotonin release. J Neurosci 21:628-640.
37. Rico B, Xu B, Reichardt LF (2002) TrkB receptor signaling is required for establishment of GABAergic synapses in the cerebellum. Nat Neurosci 5:225-233.
38. Salin PA, Malenka RC, Nicoll RA (1996) Cyclic AMP mediates a presynaptic form of LTP at cerebellar parallel fiber synapses. Neuron 16:797-803.
39. Sanes JR, Lichtman JW (1999) Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22:389-442.
40. Schinder AF, Poo M (2000) The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci 23:639-645.
41. Smit AB, Syed NI, Schaap D, van Minnen J, Klumperman J, Kits KS, Lodder H, van der Schors RC, van Elk R, Sorgedrager B, Brejc K, Sixma TK, Geraerts WP (2001) A glia-derived acetylcholine-binding protein that modulates synaptic transmission. Nature 411:261-268.
42. Stellwagen D, Shatz CJ (2002) An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron 33:357-367.
43. Syed NI, Winlow W (1991) Coordination of locomotor and cardiorespiratory networks of Lymnaea stagnalis by a pair of identified interneurones. J Exp Biol 158:37-62.
44. Syed NI, Bulloch AG, Lukowiak K (1990) In vitro reconstruction of the respiratory central pattern generator of the mollusk Lymnaea. Science 250:282-285.
45. Syed NI, Ridgway RL, Lukowiak K, Bulloch AG (1992) Transplantation and functional integration of an identified respiratory interneuron in Lymnaea stagnalis. Neuron 8:767-774.
46. Syed NI, Zaidi H, Lovell P (1999) In vitro reconstruction of neuronal networks: a simple model system approach. In: Modern techniques in neuroscience research (Windhurst U, Johansson H, eds), pp 361-377. Berlin: Springer.
47. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391:892-896.
48. Vicario-Abejon C, Collin C, McKay RD, Segal M (1998) Neurotrophins induce formation of functional excitatory and inhibitory synapses between cultured hippocampal neurons. J Neurosci 18:7256-7271.
49. Watt AJ, van Rossum MC, MacLeod KM, Nelson SB, Turrigiano GG (2000) Activity coregulates quantal AMPA and NMDA currents at neocortical synapses. Neuron 26:659-670.
50. Weisskopf MG, Castillo PE, Zalutsky RA, Nicoll RA (1994) Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. Science 265:1878-1882.
51. Woodin MA, Hamakawa T, Takasaki M, Lukowiak K, Syed NI (1999) Trophic factor-induced plasticity of synaptic connections between identified Lymnaea neurons. Learn Mem 6:307-316.
52. Woodin MA, Munno DW, Syed NI (2002) Trophic factor-induced excitatory synaptogenesis involves postsynaptic modulation of nicotinic acetyl-choline receptors. J Neurosci 22:505-514.
53. Yoshihara M, Suzuki K, Kidokoro Y (2000) Two independent pathways mediated by cAMP and protein kinase A enhance spontaneous transmitter release at Drosophila neuromuscular junctions. J Neurosci 20:8315-8322.
54. Zhang JM, Li H, Liu B, Brull SJ (2002) Acute topical application of tumor necrosis factor alpha evokes protein kinase A-dependent responses in rat sensory neurons. J Neurophysiol 88:1387-1392.
55. Ziv NE, Garner CC (2001) Principles of glutamatergic synapse formation: seeing the forest for the trees. Curr Opin Neurobiol 11:536-543.
56. Zoubine MN, Ma JY, Smirnova IV, Citron BA, Festoff BW (1996) A molecular mechanism for synapse elimination: novel inhibition of locally generated thrombin delays synapse loss in neonatal mouse muscle. Dev Biol 179:447-457.