Excitatory synaptogenesis between identified Lymnaea neurons requires extrinsic trophic factors and is mediated by receptor tyrosine kinases

Journal of Neuroscience

Volumn 19, Issue 21, 1999, Pages 9306-9312

  Hamakawa, Toshiro ^a,b   Woodin, Melanie A ^a   Bjorgum, Micki C ^a   Painter, Sherry D ^c   Takasaki, Mayumi ^b   Lukowiak, Ken ^a   Nagle, Gregg T ^c   Syed, Naweed I ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF MIYAZAKI   (Japan)

^c UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

EGF; Lymnaea; Protein synthesis; Soma soma synapses; Synapse formation; Trk receptors; Trophic factors

Indexed keywords

EPIDERMAL GROWTH FACTOR; GENISTIN; LAVENDUSTIN A; NEUROTROPHIC FACTOR; PROTEIN TYROSINE KINASE;

ARTICLE; BRAIN SLICE; CELL PROLIFERATION; LYMNAEA; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NERVE FIBER GROWTH; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; RECEPTOR DENSITY; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS;

EID: 0033232536     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-21-09306.1999     Document Type: Article

References (53)

1. Berninger B, Poo M-M (1996) Fast actions of neurotrophic factors. Curr Opin Neurobiol 6:324-330.
2. Bjorgum MC, Hamakawa T, Takasaki M, Syed NI (1998) Brain-conditioned medium induced excitatory synaptogenesis between identified Lymnaea neurons may require activity dependent mechanisms. Soc Neurosci Abstr 24:791.
3. Boulanger L, Poo M-M (1999) Presynaptic depolarization facilitates neurotrophin-induced synaptic potentiation. Nat Neurosci 2:345-351.
4. Cohen-Corey S, Fraser SE (1995) Effects of brain-derived neurotrophic factor on optic axon branching and remodeling in vivo. Nature 378:192-196.
5. Fainzilber M, Smit AB, Syed NI, Wildering WC, Hermann PM, van der Schors RC, Jiménez C, Li KW, van Minnen J, Bulloch AGM, Ibán̄ez CF, Geraerts WPM (1996) CRNF, a molluscan neurotrophic factor that interacts with the p75 neurotrophin receptor. Science 274:1540-1543.
6. Feng Z-P, 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 sustrate adhesion molecules. J Neurosci 17:7839-7849.
7. Funakoshi H, Bellurado N, Arenas E, Yamamoto Y, Casabona A, Persson H, Ibanez CF (1995) Muscle-derived neurotrophin-4 as an activity-dependent trophic signal for adult motor neurons. Science 268:1459-1499.
8. Hermann PM, Wildering WC, Painter SD, Nagle GT, Bulloch AGM (1998) Molluscan epidermal growth factor: neurotrophic actions. Soc Neurosci Abstr 24:106.
9. Janse C, van der Wilt CJ, van der Plas J, van der Roest M (1985) Central and peripheral neurons involved in oxygen perception in the pulmonate snail Lymnaea stagnalis (Mollusca Gastropoda). Comp Biochem Physiol 82A:459-467.
10. Kang H, Schuman EM (1995) Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267:1658-1662.
11. Kim HG, Wang T, Olafsson P, Lu B (1994) Neurotrophin-3 potentiates neuronal activity and inhibits G-aminobutyratergic synaptic transmission in cortical neurons. Proc Natl Acad Sci USA 91:12341-12345.
12. Landis SC (1990) Target regulation of neurotransmitter phenotype. Trends Neurosci 13:344-350.
13. Leßmann V, Gottmann K, Heumann R (1994) BDNF and NT-4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurones. NeuroReport 6:21-25.
14. Levine ES, Dreyfus CF, Black IB, Plummer MR (1995) Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc Natl Acad Sci USA 92:8074-8077.
15. Li YX, Zhang Y, Lester HA, Schuman EM, Davidson N (1998) Enhancement of neurotransmitter release induced by brain-derived neurotrophic factor in cultured hippocampal neurons. J Neurosci 18:10231-10240.
16. Liou JC, Yang RS, Fu WM (1997) Regulation of quantal secretion by neurotrophic factors at developing motoneurons in Xenopus cell cultures. J Physiol (Lond) 503:129-139.
17. Lohof AM, Ip NY, Poo M-M (1993) Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 363:350-353.
18. Magoski NS, Bulloch AGM (1997) Localization, physiology, and modulation of a molluskan dopaminergic synapse. J Neurobiol 33:247-264.
19. Magoski NS, Bauce LG, Syed NI, Bulloch AGM (1995) Dopaminergic transmission between identified neurons from the mollusc Lymnaea stagnalis. J Neurophysiol 74:1287-1300.
20. McAllister AK, Lo DC, Katz LC (1995) Neurotrophins regulate dendritic growth in developing visual cortex, Neuron 15:323-331.
21. McAllister AK, Katz LC, Lo DC (1996) Neurotrophin regulation of cortical dendritic growth requires activity. Neuron 18:767-778.
22. McCaman MW, Ono JK, McCaman RE (1979) Dopamine measurements in molluscan ganglia and neurons using a new, sensitive assay. J Neurochem 32:1111-1113.
23. McCrohan CR, Benjamin PR (1980) Synaptic relationships of the cerebral giant cells with motorneurones in the feeding system of Lymnaea stagnalis. J Exp Biol 85:169-186.
24. Nagle GT, Akalal D-BG, ter Maat A, de With ND, Painter SD (1998) Molluscan epidermal growth factor: purification and characterization of a neurotrophic factor in the pulmonate Lymnaea. Soc Neurosci Abstr 24:106.
25. Oberstar JV, Challacombe JF, Roche FK, Letourneau PC (1997) Concentration-dependent stimulation and inhibition of growth cone behavior and neurite elongation by protein kinase inhibitors. J Neurobiol 33:161-171.
26. Onoda T, Linuma H, Sasaki Y, Hamada M, Isshiki K, Naganawa H, Takeuchi T, Tatsuta K, Umezawa K (1989) Isolation of a novel tyrosine kinase inhibitor, lavendustin A, from Streptomyces griseolavendus. J Nat Prod 52:1252-1257.
27. Oppenheim RW (1991) Cell death during development of the nervous system. Annu Rev Neurosci 14:453-501.
28. Purves D, Lichtman JW (1985) Principles of neural development. Sunderland, MA: Sinauer.
29. Ridgway RL, Syed NI, Lukowiak K, Bulloch AGM (1991) Nerve growth factor (NGF) induces sprouting of specific neurons of the snail, Lymnaea stagnalis. J Neurobiol 22:377-390.
30. Schacher S, Proshansky E (1983) Neurite regeneration by Aplysia neurons in dissociated cell culture: modulation by Aplysia hemolymph and the presence of the initial axonal segment. J Neurosci 3:2403-2413.
31. Schacher S, Rayport G, Ambron RT (1985) Giant Aplysia neuron R2 reliable forms strong chemical connections in vitro. J Neurosci 5:2851-2865.
32. Schlessinger J, Ullrich A (1992) Growth factor signaling by receptor tyrosine kinases. Neuron 9:383-391.
33. Schuman EM (1997) Synapse specificity and long-term information storage. Neuron 18:339-342.
34. Simpson CS, Morris BJ (1995) Stimulation of zif/268 gene expression by basic fibroblast growth factor in primary rat striatal cultures. Neuropharmacology 34:515-520.
35. Stoop R, Poo M-M (1995) Potentiation of transmitter release by ciliary neurotrophic factors requires somatic signaling. Science 267:695-699.
36. Stoop R, Poo M-M (1996) Synaptic modulation by neurotrophic factors: differential and synergistic effects of brain-derived neurotrophic factor and ciliary neurotrophic factor. J Neurosci 16:3256-3264.
37. Syed NI (1988) Neural control of locomotion in Lymnaea. PhD Thesis, University of Leeds.
38. Syed NI, Winlow W (1989) Morphology and electrophysiology of neurons innervating ciliated locomotor epithelium in Lymnaea stagnalis (L). Comp Biochem Physiol 93A-633-644.
39. Syed NI, Winlow W (1991) Respiratory behaviour in the pond snail Lymnaea stagnalis. II. Neural elements of the central pattern generator (CPG). J Comp Physiol [A] 169:557-568.
40. Syed NI, Harrison D, Winlow W (1988) Locomotion in Lymnaea - role of serotonergic motorneurons controlling the pedal cilia. Symp Biol Hung 36:387-402.
41. Syed NI, Bulloch AGM, Lukowiak K (1990) In vitro reconstruction of the respiratory central pattern generator of the mollusk Lymnaea. Science 250:282-285.
42. Syed N, Richardson P, Bulloch AGM (1996) Ciliary neurotrophic factor unlike nerve growth factor, supports neurite outgrowth but not synapse formation by adult Lymnaea neurons. J Neurobiol 29:293-303.
43. A synaptic responses by brain-derived neurotrophic factor (BDNF) in rat hippocampus. J Neurosci 17:2959-2966.
44. Thoenen H (1991) The changing scene of neurotrophic factors. Trends Neurosci 14:165-170.
45. Thoenen H (1995) Neurotrophins and neuronal plasticity. Science 270:593-598.
46. van Kesteren RE, Fainzilber M, Hauser G, van Minnen J, Vreugdenhil E, Smit AB, Ibánez CF, Geraerts WPM, Bulloch AGM (1998) Early evolutionary origin of the neurotrophin receptor family. EMBO J 17:2534-2542.
47. Vicario-Abéjon C, Collin C, McKay RDG, Segal M (1998) Neurotrophins induce formation of functional excitatory and inhibitory synapses between cultured hippocampal neurons. J Neurosci 18:7256-7271.
48. Wang T, Xie K, Lu B (1995) Neurotrophins promote maturation of developing neuromuscular synapses. J Neurosci 15:4796-4805.
49. Wang XH, Poo M-M (1997) Potentiation of developing synapses by postsynaptic release of neurotrophin-4. Neuron 19:825-835.
50. Winlow W, Benjamin PR (1977) Postsynaptic effects of a multiaction giant interneurone on identified snail neurones. Nature 268:263-265.
51. Wong RG, Hadley RD, Kater SB, Hauser GC (1981) Neurite outgrowth in molluscan organ and cell cultures: the role of conditioning factor(s). J. Neurosci 1:1008-1021.
52. Yamada M, Ikeuchi T, Hatanaka H (1997) The neurotrophic action and signalling of epidermal growth factor. Prog Neurobiol 51:19-37.
53. Zhou J, Bradford HF (1997) Nerve growth factors and the control of neurotransmitter phenotype selection in the mammalian central nervous system. Prog Neurobiol 53:27-43.