Synapse formation in the absence of cell bodies requires protein synthesis

Journal of Neuroscience

Volumn 22, Issue 5, 2002, Pages 1831-1839

  Schacher, Samuel ^a   Wu, Fang ^a  

^a New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

Aplysia; Axon growth; Cell culture; Local protein synthesis; Neuritic mRNA; Synapse formation

Indexed keywords

ANISOMYCIN; MESSENGER RNA; PROTEIN;

APLYSIA; ARTICLE; CONTROLLED STUDY; MOTONEURON; NERVE CELL CULTURE; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SENSORY NERVE CELL; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS;

EID: 0036523035     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-05-01831.2002     Document Type: Article

References (35)

1. Ahmari SE, Buchanan J, Smith SJ (2000) Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 3:445-451.
2. Bailey CH, Chen M (1983) Morphological basis of long-term habituation and sensitization. Science 220:91-93.
3. Bailey CH, Chen M (1988) Long-term memory in Aplysia modulates the total number of varicosities of single identified sensory neurons. Proc Natl Acad Sci USA 85:2373-2377.
4. Bank M, Schacher S (1992) Segregation of presynaptic inputs on an identified target neuron in vitro: Structural remodeling visualized over time. J Neurosci 12:2960-2972.
5. Benbassat D, Spira ME (1994) The survival of transected axonal segments of cultured Aplysia neurons is prolonged by contact with intact nerve cells. Euro J Neurosci 6:1605-1614.
6. Bittner GD (1991) Long-term survival of anucleate axons and its implications for nerve regeneration. Trends Neurosci 14:188-193.
7. Casadio A, Martin KC, Bailey CH, Chen M, Zhu H, Kandel ER (1997) Molecular mechanisms underlying synapse-specific long-term facilitation of Aplysia sensory to motor synapses. Soc Neurosci Abstr 24:234.
8. Casadio A, Martin KC, Giustetto M, Zhu H, Chen M, Bartsch D, Bailey CH, Kandel ER (1999) A transient, neuron-wide form of crebmediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 99:221-237.
9. Chitwood R, Li Q, Glanzman D (2001) Serotonin facilitates AMPA-type responses in isolated siphon motor neurons of Aplysia in culture. J Physiol (Lond) 534:501-510.
10. Conrad P, Wu F, Schacher S (1999) Changes in functional glutamate receptors on a postsynaptic neuron accompany formation and maturation of an identified synapse. J Neurobiol 39:237-248.
11. Coulson RL, Klein M (1997) Rapid development of synaptic connections and plasticity between sensory neurons and motor neurons of Aplysia in cell culture: Implications for learning and regulation of synaptic strength. J Neurophysiol 77:2316-2327.
12. Crino PB, Eberwine J (1996) Molecular characterization of the dendritic growth cone: Regulated mRNA transport and local protein synthesis. Neuron 17:1173-1187.
13. 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.
14. Glanzman DL, Kandel ER, Schacher S (1989) Identified target motor neuron regulates neurite outgrowth and synapse formation of Aplysia sensory neurons in vitro. Neuron 3:441-450.
15. Hatada Y, Wu F, Silverman R, Schacher S, Goldberg DJ (1999) En passant synaptic varicosities form directly from growth cones by transient cessation of growth cone advance but not of actin-based motility. J Neurobiol 41:242-251.
16. Hatada Y, Wu F, Sun ZY, Schacher S, Goldberg DJ (2000) Presynaptic morphological changes associated with long-term synaptic facilitation are triggered by actin polymerization at pre-existing varicosities. J Neurosci 20:RC82(1-5).
17. Huber KM, Kayser MS, Bear MF (2000) Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288:1254-1257.
18. Kang H, Schuman EM (1996) A requirement for local protein synthesis in neutrophin-induced hippocampal synaptic plasticity. Science 273:1402-1406.
19. Martin KC, Casadio A, Zhu H, Yaping E, Rose JC, Chen M, Bailey CH, Kandel ER (1997) Synapse-specific, long-term facilitation of Aplysia sensory to motor synapses: A function for local protein synthesis in memory storage. Cell 91:927-938.
20. Nakata T, Terada S, Hirokawa N (1998) Visualization of the dynamics of synaptic vesicle and plasma membrane proteins in living neurons. J Cell Biol 140:659-674.
21. Rayport SG, Schacher (1986) Synaptic plasticity in vitro: Cell culture of identified Aplysia neurons mediating short-term habituation and sensitization. J Neurosci 6:759-763.
22. Santarelli L, Montarolo PG, Schacher S (1996) Neuropeptide localization in varicosities of Aplysia sensory neurons is regulated by target and neuromodulators evoking long-term synaptic plasticity. J Neurobiol 31:297-308.
23. Schacher S, Glanzman DL, Barzilai A, Dash P, Grant SGN, Keller F, Mayford M, Kandel ER (1990) Long-term facilitation inAplysia: Persistent phosphorylation and structural changes. Cold Spring Harbor Symp Quant Biol 55:187-202.
24. Schacher S, Wu F, Panyko JD, Sun ZY, Wang D (1999) Expression and branch-specific export of mRNA are regulated by synapse formation and interaction with specific postsynaptic targets. J Neurosci 19:6338-6347.
25. Sheetz AJ, Nairn AC, Constantine-Paton M (2000) NMDA receptormediated control of protein synthesis at developing synapses. Nat Neurosci 3:211-216.
26. Sherff CM, Carew TJ (1999) Coincident induction of long-term facilitation in Aplysia: Cooperativity between cell bodies and remote synapses. Science 285:1911-1914.
27. Sherff CM, Carew TJ (2000) Induction of long-term facilitation atAplysia sensorimotor synapses by coincident 5-HT exposure requires postsynaptic protein synthesis. Soc Neurosci Abstr 26:1523.
28. Spencer GE, Syed NI, van Kesteren E, Lukowiak K, Geraerts WP, van Minnen J (2000) Synthesis and functional integration of a neurotransmitter receptor in isolated invertebrate axons. J Neurobiol 44:72-81.
29. Steward O, Schuman EM (2001) Protein synthesis at synaptic sites on dendrites. Annu Rev Neurosci 24:299-325.
30. Steward O, Wallace CS, Lyford GL, Worley PF (1998) Synaptic activation causes the mRNA for the IEG Arc to localized selectively near activated postsynaptic sites on dendrites. Neuron 21:741-751.
31. Sun ZY, Wu F, Schacher S (2001) Rapid bidirectional modulation of mRNA expression and export accompany long-term facilitation and depression of Aplysia synapses. J Neurobiol 46:41-47.
32. Trudeau LE, Castellucci VF (1995) Postsynaptic modifications in longterm facilitation: Upregulation of excitatory amino acid receptors. J Neurosci 15:1275-1284.
33. Wu L, Wells D, Tay J, Mendis D, Abbott MA, Barnitt A, Quinlan E, Heynen A, Fallon JR, Richter JD (1998) CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of alpha-CaMKII mRNA at synapses. Neuron 21:1129-1139.
34. Zhu H, Wu F, Schacher S (1994) Aplysia cell adhesion molecules and serotonin regulate sensory cell-motor cell interactions during early stages of synapse formation in vitro. J Neurosci 14:6886-6900.
35. Zhu H, Wu F, Schacher S (1997) Site-specific and sensory neurondependent increases in postsynaptic glutamate sensitivity accompany serotonin-induced long-term facilitation at Aplysia sensorimotor synapses. J Neurosci 17:4976-4986.