Fibroblast growth factor-2 increases functional excitatory synapses on hippocampal neurons

European Journal of Neuroscience

Volumn 16, Issue 7, 2002, Pages 1313-1324

  Li, Ai Jun ^a   Suzuki, Seigo ^a   Suzuki, Masashi ^a   Mizukoshi, Eiichi ^a,b   Imamura, Toru ^a,b  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

FM4 64; Neuron culture; Neurotrophins; Rat; Synaptogenesis

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 3; FLUORESCENT DYE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; NERVE PROTEIN;

ANIMAL CELL; ARTICLE; CELL VACUOLE; CONTROLLED STUDY; DENDRITE; DRUG EFFECT; DRUG MECHANISM; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GROWTH CONE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; NERVE CELL CULTURE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE; NERVE FUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; QUANTITATIVE ASSAY; RAT; RECEPTOR DENSITY; STATISTICAL SIGNIFICANCE; SYNAPSE; SYNAPTOGENESIS;

ANIMALS; CELLS, CULTURED; EMBRYO; FIBROBLAST GROWTH FACTOR 2; HIPPOCAMPUS; MITOGEN-ACTIVATED PROTEIN KINASES; NEURONS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, FIBROBLAST GROWTH FACTOR; SYNAPSES; SYNAPSINS; SYNAPTOPHYSIN;

EID: 0036430039     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.02193.x     Document Type: Article

References (51)

1. Abe, K., Aoyagi, A. & Saito, H. (2001) Sustained phosphorylation of mitogen-activated protein kinase is required for basic fibroblast growth factor-mediated axonal branch formation in cultured rat hippocampal neurons. Neurochem. Int., 38, 309-315.
2. Anderson, K.J., Dam, D., Lee, S. & Cotman, C.W. (1988) Basic fibroblast growth factor prevents death of lesioned cholinergic neurons in vivo. Nature, 332, 360-361.
3. Aoyagi, A., Nishikawa, K., Saito, H. & Abe, K. (1994) Characterization of basic fibroblast growth factor-mediated acceleration of axonal branching in cultured rat hippocampal neurons. Brain Res., 661, 117-126.
4. Bailey, C.H., Kaang, B.K., Chen, M., Martin, K.C., Lim, C.S., Casadio, A. & Kandel, E.R. (1997) Mutation in the phosphorylation sites of MAP kinase blocks learning-related internalization of apCAM in Aplysia sensory neurons. Neuron, 18, 913-924.
5. Baird, A. & Walicke, P.A. (1989) Fibroblast growth factors. Br. Med. Bull., 45, 438-452.
6. Becherer, U., Angleson, J.K. & Betz, W.J. (2000) Imaging synaptic vesicle dynamics at the frog neuromuscular junction with the styryl dye FM1-43. In Yeste, R., Lanni, F. & Konnerth, A. (eds), Imaging Neurons. Cold Spring. Harbour Laboratory Press, New York, pp. 53.1-53.11.
7. Boyer, C., Schikorski, T. & Stevens, C.F. (1998) Comparison of hippocampal dendritic spines in culture and in brain. J. Neurosci., 18, 5294-5300.
8. Causing, C.G., Gloster, A., Aloyz, R., Bamji, S.X., Chang, E., Fawcett, J., Kuchel, G. & Miller, F.D. (1997) Synaptic innervation density is regulated by neuron-derived BDNF. Neuron, 18, 257-267.
9. Cheng, B., Furukawa, K., O'Keefe, J.A., Goodman, Y., Kihiko, M., Fabian, T. & Mattson, M.P. (1995) Basic fibroblast growth factor selectively increases AMPA-receptor subunit GluR1 protein level and differentially modulates Ca2+ responses to AMPA and NMDA in hippocampal neurons. J. Neurochem., 65, 2525-2536.
10. Cohen-Cory, S. & Fraser, S.E. (1995) Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature, 378, 192-196.
11. Collin, C., Vicario-Abejon, C., Rubio, M.E., Wenthold, R.J., McKay, R.D. & Segal, M. (2001) Neurotrophins act at presynaptic terminals to activate synapses among cultured hippocampal neurons. Eur. J. Neurosci., 13, 1273-1282.
12. Di Cristo, G., Berardi, N., Cancedda, L., Pizzorusso, T., Putignano, E., Ratto, G.M. & Maffei, L. (2001) Requirement of ERK activation for visual cortical plasticity. Science, 292, 2337-2340.
13. Durand, G.M., Kovalchuk, Y. & Konnerth, A. (1996) Long-term potentiation and functional synapse induction in developing hippocampus. Nature, 381, 71-75.
14. English, A.W. & Schwartz, G. (1995) Both basic fibroblast growth factor and ciliary neurotrophic factor promote the retention of polyneuronal innervation of developing skeletal muscle fibers. Dev. Biol., 169, 57-64.
15. Ferguson, I.A. & Johnson, E.M. Jr (1991) Fibroblast growth factor receptor-bearing neurons in the CNS: Identification by receptor-mediated retrograde transport. J. Comp. Neurol., 313, 693-706.
16. Fletcher, T.L., Cameron, P., De Camilli, P. & Banker, G. (1991) The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture. J. Neurosci., 11, 1617-1626.
17. Gomez-Pinilla, F., Lee, J.W. & Cotman, C.W. (1994) Distribution of basic fibroblast growth factor in the developing rat brain. Neuroscience, 61, 911-923.
18. Grothe, C., Zachmann, K. & Unsicker, K. (1991) Basic FGF-like immunoreactivity in the developing and adult rat brainstem. J. Comp. Neurol., 305, 328-336.
19. Huang, Y.Y., Martin, K.C. & Kandel, E.R. (2000) Both protein kinase A and mitogen-activated protein kinase are required in theamygdala for the macromolecular synthesis-dependent late phase of long-term potentiation. J. Neurosci., 20, 6317-6325.
20. Jovanovic, J.N., Benfenati, F., Siow, Y.L., Sihra, T.S., Sanghera, J.S., Pelech, S.L., Greengard, P. & Czernik, A.J. (1996) Neurotrophins stimulate phosphorylation of synapsin I by MAP kinase and regulate synapsin I-actin interactions. Proc. Natl. Acad. Sci. USA., 93, 3679-3683.
21. Kannenberg, K., Sieghart, W. & Reuter, H. (1999) Clusters of GABAA receptors on cultured hippocampal cells correlate only partially with functional synapses. Eur. J. Neurosci., 11, 1256-1264.
22. Kawakami, N., Kashiwagi, S., Kitahara, T., Yamashita, T. & Ito, H. (1995) Effect of local administration of basic fibroblast growth factor against neuronal damage caused by transient intracerebral mass lesion in rats. Brain Res., 697, 104-111.
23. Kim, D. & Thayer, S.A. (2001) Cannabinoids inhibit the formation of new synapses between hippocampal neurons in culture. J. Neurosci., 21, RC146.
24. Koketsu, N., Berlove, D.J., Moskowitz, M.A., Kowall, N.W., Caday, C.G. & Finklestein, S.P. (1994) Pretreatment with intraventricular basic fibroblast growth factor decreases infarct size following focal cerebral ischemia in rats. Ann. Neurol., 35, 451-457.
25. Lowenstein, D.H. & Arsenault, L. (1996) The effects of growth factors on the survival and differentiation of cultured dentate gyrus neurons. J. Neurosci., 26, 1759-1769.
26. Martin, K.C., Michael, D., Rose, J.C., Barad, M., Casadio, A., Zhu, H. & Kande, 1, E.R. (1997) MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron, 18, 899-912.
27. Martinez, A., Alcantara, S., Borrell, V., Del Rio, J.A., Blasi, J., Otal, R., Campos, N., Boronat, A., Barbacid, M., Silos-Santiago, I. & Soriano, E. (1998) TrkB and TrkC signaling are required for maturation and synaptogenesis of hippocampal connections. J. Neurosci., 18, 7336-7350.
28. Mason, I.J. (1994) The ins and outs of fibroblast growth factors. Cell, 78, 547- 552.
29. Matsuo, A., Tooyama, I., Isobe, S., Oomura, Y., Akiguchi, I., Hanai, K., Kimura, J. & Kimura, H. (1994) Immunohistochemical localization in the rat brain of an epitope corresponding to the fibroblast growth factor receptor-1. Neuroscience, 60, 49-66.
30. Mattson, M.P., Kumar, K.N., Wang, H., Cheng, B. & Michaelis, E.K. (1993) Basic FGF regulates the expression of a functional 71 kDa NMDA receptor protein that mediates calcium influx and neurotoxicity in hippocampal neurons. J. Neurosci., 13, 4575-4588.
31. McAllister, A.K., Katz, L.C. & Lo, D.C. (1999) Neurotrophins and synaptic plasticity. Annu. Rev. Neurosci., 22, 295-318.
32. Miyagawa, T., Saito, H. & Nishiyama, N. (1993) Branching enhancement by basic fibroblast growth factor in cut neurite of hippocampal neurons. Neurosci. Lett., 153, 29-31.
33. Morrison, R.S., Sharma, A., de Vellis, J. & Bradshaw, R.A. (1986) Basic fibroblast growth factor supports the survival of cerebral cortical neurons in primary culture. Proc. Natl. Acad. Sci. USA., 83, 7537-7541.
34. Nakata, N., Kato, H. & Kogure, K. (1993) Protective effects of basic fibroblast growth factor against hippocampal neuronal damage following cerebral ischemia in the gerbil. Brain Res., 605, 354-356.
35. Ozawa, K., Uruno, T., Miyakawa, K., Seo, M. & Imamura, T. (1996) Expression of the fibroblast growth factor family and their receptor family genes during mouse brain development. Brain Res. Mol. Brain Res., 41, 279-288.
36. Papa, M., Bundman, M.C., Greenberger, V. & Segal, M. (1995) Morphological analysis of dendritic spine development in primary cultures of hippocampal neurons. J. Neurosci., 15, 1-11.
37. Peng, H.B., Baker, L.P. & Chen, Q. (1991) Induction of synaptic development in cultured muscle cells by basic fibroblast growth factor. Neuron, 6, 237- 246.
38. Pozzo-Miller, L.D., Gottschalk, W., Zhang, L., Du McDermott, K.J., Gopalakrishnan, R., Oho, C., Sheng, Z.H. & Lu, B. (1999) Impairments in high-frequency transmission, synaptic vesicle docking, and synaptic protein distribution in the hippocampus of BDNF knockout mice. J. Neurosci., 19, 4972-4983.
39. Rao, A., Kim, E., Sheng, M. & Craig, A.M. (1998) Heterogeneity in the molecular composition of excitatory postsynaptic sites during development of hippocampal neurons in culture. J. Neurosci., 18, 1217-1229.
40. Riva, M.A. & Mocchetti, I. (1991) Developmental expression of the basic fibroblast growth factor gene in rat brain. Brain Res. Dev. Brain Res., 62, 45-50.
41. Sasaki, K., Oomura, Y., Figurov, A. & Yagi, H. (1994) Acidic fibroblast growth factor facilitates generation of long-term potentiation in rat hippocampal slices. Brain Res. Bull., 33, 505-511.
42. Seil, F.J. & Drake-Baumann, R. (2000) TrkB receptor ligands promote activity-dependent inhibitory synaptogenesis. J. Neurosci., 20, 5367-5373.
43. Shimada, A., Mason, C.A. & Morrison, M.E. (1998) TrkB signaling modulates spine density and morphology independent of dendrite structure in cultured neonatal Purkinje cells. J. Neurosci., 18, 8559-8570.
44. Szebenyi, G., Dent, E.W., Callaway, J.L., Seys, C., Lueth, H. & Kalil, K. (2001) Fibroblast growth factor-2 promotes axon branching of cortical neurons by influencing morphology and behavior of the primary growth cone. J. Neurosci., 21, 3932-3941.
45. Vicario-Abejon, C., Collin, C., McKay, R.D. & Segal, M. (1998) Neurotrophins induce formation of functional excitatory and inhibitory synapses between cultured hippocampal neurons. J. Neurosci., 18, 7256- 7271.
46. Walicke, P.A. (1988) Basic and acidic fibroblast growth factors have trophic effects on neurons from multiple CNS regions. J. Neurosci., 8, 2618-2627.
47. Walicke, P., Cowan, W.M., Ueno, N., Baird, A. & Guillemin, R. (1986) Fibroblast growth factor promotes survival of dissociated hippocampal neurons and enhances neurite extension. Proc. Natl. Acad. Sci. USA, 83, 3012-3016.
48. Wang, T., Xie, K. & Lu, B. (1995) Neurotrophins promote maturation of developing neuromuscular synapses. J. Neurosci., 15, 4796-4805.
49. Wu, G.Y., Deisseroth, K. & Tsien, R.W. (2001) Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology. Nature Neurosci., 4, 151-158.
50. Yamashita, T., Yoshioka, M. & Itoh, N. (2000) Identification of a novel fibroblast growth factor, FGF-23, preferentially expressed in the ventrolateral thalamic nucleus of the brain. Biochem. Biophys. Res. Commun., 277, 494-498.
51. Ziv, N.E. & Smith, S.J. (1996) Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron, 17, 91-102.