Implication of fibroblast growth factors in epileptogenesis-associated circuit rearrangements

Frontiers in Cellular Neuroscience

Volumn , Issue SEP, 2013, Pages

  Paradiso, Beatrice ^a,b   Zucchini, Silvia ^a,c   Simonato, Michele ^a,c  

^a UNIVERSITY OF FERRARA   (Italy)

^b Azienda Ospedaliero Universitaria di Ferrara   (Italy)

^c Technopole of Ferrara   (Italy)

Author keywords

Cell death; Epilepsy; Fibroblast growth factors; Neurogenesis; Synaptogenesis

Indexed keywords

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 14; FIBROBLAST GROWTH FACTOR 17; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 5; FIBROBLAST GROWTH FACTOR 8; FIBROBLAST GROWTH FACTOR RECEPTOR; KERATINOCYTE GROWTH FACTOR; KLOTHO PROTEIN; NEUROTROPHIC FACTOR; UNCLASSIFIED DRUG;

BINDING SITE; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; EPILEPSY; EPILEPTOGENESIS; HIPPOCAMPAL CA3 REGION; HUMAN; MACROCEPHALY; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL NECROSIS; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SEIZURE; SIGNAL TRANSDUCTION; SKELETON MALFORMATION; SYNAPTOGENESIS;

EID: 84885052644     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00152     Document Type: Review

References (94)

1. Abe, K., Aoyagi, A., and 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. doi: 10. 1016/s0197-0186(00)00093-0
2. Acharya, M. M., Hattiangady, B., and Shetty, A. K. (2008). Progress in neuroprotective strategies for preventing epilepsy. Prog. Neurobiol.84, 363-404. doi: 10.1016/j.pneurobio. 2007.10.010
3. Allerstorfer, S., Sonvilla, G., Fischer, H., Spiegl-Kreinecker, S., Gauglhofer, C., and Setinek, U. (2008). FGF5 as an oncogenic factor in human glioblastoma multiforme: autocrine and paracrine activities. Oncogene 27, 4180-4190. doi: 10.1038/onc. 2008.61
4. Aoyagi, A., Nishikawa, K., Saito, H., and Abe, K. (1994). Characterization of basic fibroblast growth factor-mediated acceleration of axonal branching in cultured rat hippocampal neurons. Brain Res. 661, 117-126. doi: 10.1016/0006-8993(94)91188-6
5. Ballabriga, J., Pozas, E., Planas, A. M., and Ferrer, I. (1997). bFGF and FGFR-3 immunoreactivity in the rat brain following systemic kainic acid administration at convulsant doses: localization of bFGF and FGFR-3 in reactive astrocytes, and FGFR-3 in reactive microglia. Brain Res. 752, 315-318. doi: 10.1016/s0006-8993(96)01308-x
6. Beenken, A., and Mohammadi, M. (2009). The FGF family: biology, pathophysiology and therapy. Nat. Rev. Drug Discov. 8, 235-253. doi: 10.1038/nrd2792
7. Bikfalvi, A., Klein, S., Pintucci, G., and Rifkin, D. B. (1997). Biological roles of fibroblast growth factor-2. Endocr. Rev. 18, 26-45. doi: 10. 1210/er.18.1.26
8. Bovolenta, R., Zucchini, S., Paradiso, B., Rodi, D., Merigo, F., Navarro Mora, G., et al. (2010). Hippocampal FGF-2 and BDNF overexpression attenuates epileptogenesisassociated neuroinflammation and reduces spontaneous recurrent seizures.J. Neuroinflammation 7:81. doi: 10.1186/1742-2094-7-81
9. Bregola, G., Frigati, L., Zucchini, S., and Simonato, M. (2000). Different patterns of induction of fibroblast growth factor-2 and brain derived neurotrophic factor messenger RNAs during kindling epileptogenesis, and development of a herpes simplex vector for fibroblast growth factor-2 gene transfer in vivo. Epilepsia 41(Suppl. 6), S122-S126. doi: 10.1111/j.1528-1157.2000.tb01570.x
10. Bugra, K., Pollard, H., Charton, G., Moreau, J., Ben-Ari, Y., and Khrestchatisky, M. (1994). aFGF, bFGF and flg mRNAs show distinct patterns of induction in the hippocampus following kainateinduced seizures. Eur. J. Neurosci. 6, 58-66. doi: 10.1111/j.1460-9568. 1994.tb00247.x
11. Caday, C. G., Klagsbrun, M., Fanning, P. J., Mirzabegian, A., and Finklestein, S. P. (1990). Fibroblast growth factor (FGF) levels in the developing rat brain. Brain Res. Dev. Brain Res. 52, 241-246. doi: 10. 1016/0165-3806(90)90240-y
12. Cheng, Y., Black, I. B., and DiCiccoBloom, E. (2002). Hippocampal granule neuron production and population size are regulated by levels of bFGF. Eur. J. Neurosci. 15, 3-12. doi: 10.1046/j.0953-816x.2001. 01832.x
13. Coffin, J. D., Florkiewicz, R. Z., Neumann, J., Mort-Hopkins, T., Dorn, G. W. 2nd., Lightfoot, P., et al. (1995). Abnormal bone growth and selective translational regulation in basic fibroblast growth factor (FGF-2) transgenic mice. Mol. Biol. Cell 6, 1861-1873. doi: 10.1091/mbc.6.12. 1861
14. Cuevas, P., and Giménez-Gallego, G. (1996). Antiepileptic effects of acidic fibroblast growth factor examined in kainic acid-mediated seizures in the rat. Neurosci. Lett. 203, 66-68. doi: 10.1016/0304-3940(95)12254-0
15. Ernfors, P., Lonnerberg, P., AyerLeLievre, C., and Persson, H. (1990). Developmental and regional expression of basic FGF mRNA in the rat central nervous system. J. Neurosci. Res. 27, 10-15. doi: 10. 1002/jnr.490270103
16. Follesa, P., Gale, K., and Mocchetti, I. (1994). Regional and temporal pattern of expression of nerve growth factor and basic fibroblast growth factor mRNA in rat brain following electroconvulsive shock. Exp. Neurol. 127, 37-44. doi: 10.1006/exnr. 1994.1077
17. Fulgham, D. L., Widhalm, S. R., Martin, S., and Coffin, J. D. (1999). FGF-2 dependent angiogenesis is a latent phenotype in basic fibroblast growth factor transgenic mice. Endothelium 6, 185-195. doi: 10. 3109/10623329909053409
18. Galanopoulou, A. S., Buckmaster, P. S., Staley, K. J., Moshé, S.L., Perucca, E., Engel, J. Jr., et al. (2012). Identification of new epilepsy treatments: issues in preclinical methodology. Epilepsia 53, 571-582. doi: 10.1111/j.1528-1167.2011. 03391.x
19. Gall, C. M., Berschauer, R., and Isackson, P. J. (1994). Seizures increase basic fibroblast growth factor mRNA in adult rat forebrain neurons and glia. Brain Res. Mol. Brain Res. 21, 190-205. doi: 10. 1016/0169-328x(94)90250-x
20. Goldfarb, M., Schoorlemmer, J., Williams, A., Diwakar, S., Wang, Q., Huang, X., et al. (2007). Fibroblast growth factor homologous factors control neuronal excitability through modulation of voltagegated sodium channels. Neuron 55, 449-463. doi: 10.1016/j.neuron. 2007.07.006
21. Gomez-Pinilla, F., Lee, J. W.-K., and Cotman, C. W. (1992). Basic FGF in adult rat brain: cellular distribution and response to enthorinal lesion and fimbria-fornix transection.J. Neurosci. 12, 345-355.
22. Gómez-Pinilla, F., van der Wal, E. A., and Cotman, C. W. (1995). Possible coordinated gene expression for FGF receptor, FGF-5, and FGF-2 following seizures. Exp. Neurol. 133, 164-174. doi: 10.1006/exnr. 1995.1019
23. Gremo, F., and Presta, M. (2000). Role of fibroblast growth factor-2 in human brain: a focus on development. Int. J. Dev. Neurosci. 18, 271-279. doi: 10.1016/s0736-5748(99)00095-7
24. Gwinn, R. P., Kondratyev, A., and Gale, K. (2002). Time-dependent increase in basic fibroblast growth factor protein in limbic regions following electroshock seizures. Neuroscience 114, 403-409. doi: 10.1016/s0306-4522(02)00265-8
25. Hattiangady, B., and Shetty, A. K. (2010). Decreased neuronal differentiation of newly generated cells underlies reduced hippocampal neurogenesis in chronic temporal lobe epilepsy. Hippocampus 20, 97-112. doi: 10.1002/hipo. 20594
26. Hefti, F. (1997). Pharmacology of neurotrophic factors. Ann. Rev. Pharmacol. Toxicol. 37, 239-267. doi: 10. 1146/annurev.pharmtox.37.1.239
27. Hu, X. L., Cheng, X., Cai, L., Tan, G. H., Xu, L., Feng, X. Y., et al. (2011). Conditional deletion of NRSF in forebrain neurons accelerates epileptogenesis in the kindling model. Cereb. Cortex 21, 2158-2165. doi: 10.1093/cercor/bhq284
28. Humpel, C., Lippoldt, A., Chadi, G., Ganten, D., Olson, L., and Fuxe, K. (1993). Fast and widespread increase of basic fibroblast growth factor messenger RNA and protein in the forebrain after kainateinduced seizures. Neuroscience 57, 913-922. doi: 10.1016/0306-4522(93)90037-g
29. Itoh, N. (2010). Hormone-like (endocrine) FGFs: their evolutionary history and roles in development, metabolism, and disease. Cell Tissue Res. 342, 1-11. doi: 10.1007/s00441-010-1024-2
30. Itoh, N., and Ornitz, D. M. (2011). Fibroblast growth factors: from molecular evolution to roles in development, metabolism and disease. J. Biochem. 149, 121-130. doi: 10.1093/jb/mvq121
31. Jones, K., and Basson, M. A. (2010). FGF ligands emerge as potential specifiers of synaptic identity. Cellscience 7, 33-42.
32. Jung, K. H., Chu, K., Lee, S. T., Kim, J. H., Kang, K. M., Song, E. C., et al. (2009). Region-specific plasticity in the epileptic rat brain: a hippocampal and extrahippocampal analysis. Epilepsia 50, 537-549. doi: 10. 1111/j.1528-1167.2008.01718.x
33. Kalinina, J., Dutta, K., Ilghari, D., Beenken, A., Goetz, R., Eliseenkova, A. V., et al. (2012). The alternatively spliced acid box region plays a key role in FGF receptor autoinhibition. Structure 20, 77-88. doi: 10.1016/j. str.2011.10.022
34. Katoh, Y., and Katoh, M. (2005). Comparative genomics on FGF7, FGF10, FGF22 orthologs, and identification of fgf25. Int. J. Mol. Med. 16, 767-770. doi: 10.1007/11554714_6
35. Kelly, M. E., and McIntyre, D. C. (1994). Hippocampal kindling protects several structures from the neuronal damage resulting from kainic acid-induced status epilepticus. Brain Res.634, 245-256. doi: 10. 1016/0006-8993(94)91927-5
36. Kim, S. Y., Buckwalter, M., Soreq, H., Vezzani, A., and Kaufer, D. (2012). Blood-brain barrier dysfunctioninduced inflammatory signaling in brain pathology and epileptogenesis. Epilepsia 53(Suppl. 6), 37-44. doi: 10.1111/j.1528-1167.2012. 03701.x
37. Kim, J., Gale, K., and Kondratyev, A. (2010). Effects of repeated minimal electroshock seizures on NGF, BDNF and FGF-2 protein in the rat brain during postnatal development. Int. J. Dev. Neurosci. 28, 227-232. doi: 10.1016/j.ijdevneu.2010. 02.003
38. Kondratyev, A., Sahibzada, N., and Gale, K. (2001). Electroconvulsive shock exposure prevents neuronal apoptosis after kainic acid-evoked status epilepticus. Brain Res. Mol. Brain Res. 91, 1-13. doi: 10. 1016/s0169-328x(01)00099-7
39. Kondratyev, A., Ved, R., and Gale, K. (2002). The effects of repeated minimal electroconvulsive shock exposure on levels of mRNA encoding fibroblast growth factor-2 and nerve growth factor in limbic regions. Neuroscience 114, 411-416. doi: 10. 1016/s0306-4522(02)00266-x
40. Lee, C. H., Javed, D., Althaus, A. L., Parent, J. M., and Umemori, H. (2012). Neurogenesis is enhanced and mossy fiber sprouting arises in FGF7-deficient mice during development. Mol. Cell. Neurosci. 51, 61-67. doi: 10.1016/j.mcn.2012.07.010
41. Lee, C. H., and Umemori, H. (2013). Suppression of epileptogenesisassociated changes in response to seizures in FGF22-deficient mice. Front. Cell. Neurosci. 7:43. doi: 10. 3389/fncel.2013.00043
42. Li, Q., and Stephenson, D. (2002). Postischemic administration of basic fibroblast growth factor improves sensorimotor function and reduces infarct size following permanent focal cerebral ischemia in the rat. Exp. Neurol.177, 531-537. doi: 10.1006/exnr.2002.7994
43. Li, A. J., Suzuki, S., Suzuki, M., Mizukoshi, E., and Imamura, T. (2002). Fibroblast growth factor-2 increases functional excitatory synapses on hippocampal neurons. Eur. J. Neurosci. 16, 1313-1324. doi: 10.1046/j.1460-9568.2002. 02193.x
44. Liu, Z., D'Amore, P. A., Mikati, M., Gatt, A., and Holmes, G. L. (1993). Neuroprotective effect of chronic infusion of basic fibroblast growth factor on seizure-associated hippocampal damage. Brain Res. 626, 335-338. doi: 10.1016/0006-8993(93)90598-h
45. Liu, Z., and Holmes, G. L. (1997a). Basic fibroblast growth factor is highly neuroprotective against seizure-induced long-term behavioural deficits. Neuroscience 76, 1129-1138. doi: 10.1016/s0306-4522(96)00412-5
46. Liu, Z., and Holmes, G. L. (1997b). Basic fibroblast growth-induced seizures in rats. Neurosci. Lett. 233, 85-88. doi: 10.1016/s0304-3940(97)00627-7
47. Lowenstein, D. H., and Arsenault, L. (1996). The effects of growth factors on the survival and differentiation of cultured dentate gyrus neurons.J. Neurosci. 16, 1759-1769.
48. Ma, D. K., Jang, M. H., Guo, J. U., Kitabatake, Y., Chang, M. L., Pow-Anpongkul, N., et al. (2009). Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323, 1074-1077. doi: 10. 1126/science.1166859
49. Masco, D., Sahibzada, N., Switzer, R., and Gale, K. (1999). Electroshock seizures protect against apoptotic hippocampal cell death induced by adrenalectomy. Neuroscience 91, 1315-1319. doi: 10. 1016/s0306-4522(98)00636-8
50. Mattson, M. P. (2000). Activin to the rescue for overexcited neurons. Nat. Med.6, 739-741. doi: 10.1038/77453
51. McCabe, M. J., Gaston-Massuet, C., Tziaferi, V., Gregory, L. C., Alatzoglou, K. S., Signore, M., et al. (2011). Novel FGF8 mutations associated with recessive holoprosencephaly, craniofacial defects, and hypothalamo-pituitary dysfunction. J. Clin. Endocrinol. Metab. 96, E1709-E1718. doi: 10.1210/jc. 2011-0454
52. Naegele, J. (2009). Epilepsy and the plastic mind. Epilepsy Curr. 9, 166-169. doi: 10.1111/j.1535-7511.2009. 01331.x
53. Ortega, S., Ittmann, M., Tsang, S. H., Ehrlich, M., and Basilico, C. (1998). Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2. Proc. Natl. Acad. Sci. U S A 95, 5672-5677. doi: 10.1073/pnas.95. 10.5672
54. Paradiso, B., Marconi, P., Zucchini, S., Berto, E., Binaschi, A., Bozac, A., et al. (2009). Localized delivery of fibroblast growth factor-2 and brain-derived neurotrophic factor reduces spontaneous seizures in an epilepsy model. Proc. Natl. Acad. Sci. U S A 106, 7191-7196. doi: 10. 1073/pnas.0810710106
55. Paradiso, B., Zucchini, S., Su, T., Bovolenta, R., Berto, E., Marconi, P., et al. (2011). Localized overexpression of FGF-2 and BDNF in hippocampus reduces mossy fiber sprouting and spontaneous seizures up to 4 weeks after pilocarpine-induced status epilepticus. Epilepsia 52, 572-578. doi: 10.1111/j.1528-1167.2010. 02930.x
56. Parent, J. M. (2007). Adult neurogenesis in the intact and epileptic dentate gyrus. Prog. Brain Res. 163, 529-540. doi: 10.1016/s0079-6123(07) 63028-3
57. Park, J. W., Park, E. S., Choi, E. N., Park, H. Y., and Jung, S. C. (2009). Altered brain gene expression pro-files associated with the pathogenesis of phenylketonuria in a mouse model. Clin. Chim. Acta 401, 90-99. doi: 10.1016/j.cca.2008.11.019
58. Pitkänen, A., and Lukasiuk, K. (2009). Molecular and cellular basis of epileptogenesis in symptomatic epilepsy. Epil. Behav. 14(Suppl. 1), 16-25. doi: 10.1016/j.yebeh.2008. 09.023
59. Pitkänen, A., and Lukasiuk, K. (2011). Mechanisms of epileptogenesis and potential treatment targets. Lancet Neurol. 10, 173-186. doi: 10. 1016/s1474-4422(10)70310-0
60. Pitkänen, A., and Sutula, T. P. (2002). Is epilepsy a progressive disorder? Prospects for new therapeutic approaches in temporal-lobe epilepsy. Lancet Neurol. 1, 173-181. doi: 10.1016/s1474-4422(02) 00073-x
61. Qian, X., Davis, A. A., Goderie, S. K., and Temple, S. (1997). FGF2 concentration regulates the generation of neurons and glia from multipotent cortical stem cells. Neuron 18, 81-93. doi: 10.1016/s0896-6273(01)80048-9
62. Reuss, B., Dono, R., and Unsicker, K. (2003). Functions of Fibroblast Growth Factor (FGF)-2 and FGF-5 in astroglial differentiation and blood-brain barrier permeability: evidence from mouse mutants. J. Neurosci. 23, 6404-6412.
63. Riva, M. A., Donati, E., Tascedda, F., Zolli, M., and Racagni, G. (1994). Short-and long-term induction of basic fibroblast growth factor gene expression in rat central nervous system following kainate injection. Neuroscience 59, 55-65. doi: 10. 1016/0306-4522(94)90098-1
64. Riva, M. A., Fumagalli, F., Blom, J. M., Donati, E., and Racagni, G. (1995). Adrenalectomy reduces FGF-1 and FGF-2 gene expression in specific rat brain regions and differently affects their induction by seizures. Brain Res. Mol. Brain Res. 34, 190-196. doi: 10.1016/0169-328x(95) 00157-n
65. Riva, M. A., Gale, K., and Mocchetti, I. (1992). Basic fibroblast growth factor mRNA increases in specific brain regions following convulsive seizures. Brain Res. Mol. Brain Res. 15, 311-318. doi: 10.1016/0169-328x(92)90123-s
66. Riva, M. A., and Mocchetti, I. (1991). Developmental expression of the basic fibroblast growth factor gene in rat brain. Brain Res. Mol. Brain Res. 62, 45-50. doi: 10.1016/0165-3806(91)90188-o
67. Schinder, A. F., and Poo, M. (2000). The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci. 23, 639-645. doi: 10.1016/s0166-2236(00)01672-6
68. Schmidt, D., and Sillanpää, M. (2012). Evidence-based review on the natural history of the epilepsies. Curr. Opin. Neurol. 25, 159-163. doi: 10. 1097/wco.0b013e3283507e73
69. Simonato, M., Bennett, J., Boulis, N. M., Castro, M. G., Fink, D. J., Goins, W. F., et al. (2013). Progress in gene therapy for neurological disorders. Nat. Rev. Neurol.9, 277-291. doi: 10. 1038/nrneurol.2013.56
70. Simonato, M., Molteni, R., Bregola, G., Muzzolini, A., Piffanelli, M., Beani, L., et al. (1998). Different patterns of induction of FGF-2, FGF-1 and BDNF mRNAs during kindling epileptogenesis in the rat. Eur. J. Neurosci. 10, 955-963. doi: 10. 1046/j.1460-9568.1998.00105.x
71. Simonato, M., Tongiorgi, E., and Kokaia, M. (2006). Angels and demons: neurotrophic factors and epilepsy. Trends Pharmacol. Sci. 27, 631-638. doi: 10.1016/j.tips.2006. 10.002
72. Simonato, M., and Zucchini, S. (2010). Are the neurotrophic factors a suitable therapeutic target for the prevention of epileptogenesis? Epilepsia 51(Suppl. 3), 48-51. doi: 10.1111/j. 1528-1167.2010.02609.x
73. Szebenyi, G., Dent, E. W., Callaway, J. L., Seys, C., Lueth, H., and 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.
74. Tao, Y., Black, I. B., and DiCiccoBloom, E. (1997). In vivo neurogenesis is inhibited by neutralizing antibodies to basic fibroblast growth factor. J. Neurobiol. 33, 289-296. doi: 10.1002/(sici)1097-4695(199709)33:3<289::aid-neu7> 3.0.co;2-y
75. Temkin, N. R. (2001). Antiepileptogenesis and seizure prevention trials with antiepileptic drugs: metaanalysis of controlled trials. Epilepsia 42, 515-524. doi: 10.1046/j.1528-1157.2001.28900.x
76. Teng, Y. D., Mocchetti, I., TaveiraDaSilva, A. M., Gillis, R. A., and Wrathall, J. R. (1999). Basic fibroblast growth factor increases long-term survival of spinal motor neurons and improves respiratory function after experimental spinal cord injury. J. Neurosci. 19, 7037-7047.
77. Terauchi, A., Johnson-Venkatesh, E. M., Toth, A. B., Javed, D., Sutton, M. A., and Umemori, H. (2010). Distinct FGFs promote differentiation of excitatory and inhibitory synapses. Nature 465, 783-787. doi: 10.1038/nature09041
78. Torelli, S., Dell'Era, P., Ennas, M. G., Sogos, V., Gremo, F., Ragnotti, G., et al. (1990). Basic fibroblast growth factor in neuronal cultures of human fetal brain. J. Neurosci. Res. 27, 78-83. doi: 10.1002/jnr. 490270112
79. Tretter, Y. P., Hertel, M., Munz, B., ten Bruggencate, G., Werner, S., and Alzheimer, C. (2000). Induction of activin A is essential for the neuroprotective action of basic fibroblast growth factor in vivo. Nat. Med. 6, 812-815. doi: 10.1038/77548
80. Turner, N., and Grose, R. (2010). Fibroblast growth factor signalling: from development to cancer. Nat. Rev. Cancer 10, 116-129. doi: 10. 1038/nrc2780
81. Ueda, M., Sugiura, C., Ohno, K., Kakita, A., Hori, A., Ohama, E., et al. (2011). Immunohistochemical expression of fibroblast growth factor-2 in developing human cerebrum and epilepsy-associated malformations of cortical development. Neuropathology 31, 589-598. doi: 10.1111/j.1440-1789.2011. 01205.x
82. Umemori, H., Linhoff, M. W., Ornitz, D. M., and Sanes, J. R. (2004). FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain. Cell 118, 257-270. doi: 10.1016/j.cell.2004. 06.025
83. Van Der Wal, E. A., Gomez-Pinilla, F., and Cotman, C. W. (1994). Seizureassociated induction of basic fibroblast growth factor and its receptor in the rat brain. Neuroscience 60, 311-323. doi: 10.1016/0306-4522(94)90245-3
84. Vescovi, A. L., Reynolds, B. A., Fraser, D. D., and Weiss, S. (1993). bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron 11, 951-966. doi: 10. 1016/0896-6273(93)90124-a
85. Vezzani, A., French, J., Bartfai, T., and Baram, T. Z. (2011). The role of inflammation in epilepsy. Nat. Rev. Neurol. 7, 31-40. doi: 10. 1038/nrneurol.2010.178
86. Vicario-Abejon, C., Johe, K. K., Hazel, T. G., Collazo, D., and McKay, R. D. (1995). Functions of basic fibroblast growth factor and neurotrophins in the differentiation of hippocampal neurons. Neuron 15, 105-114. doi: 10.1016/0896-6273(95) 90068-3
87. Wagner, J. P., Black, I. B., and DiCiccoBloom, E. (1999). Stimulation of neonatal and adult brain neurogenesis by subcutaneous injection of basic fibroblast growth factor. J. Neurosci. 19, 6006-6016.
88. Waliche, P. A. (1988). Interactions between basic fibroblast growth factor (FGF) and glycosoaminoglycans in promoting neurite outgrowth. Exp. Neurol. 102, 144-148. doi: 10. 1016/0014-4886(88)90087-8
89. Wang, Q., Bardgett, M. E., Wong, M., Wozniak, D. F., Lou, J., McNeil, B. D., et al. (2002). Ataxia and paroxysmal dyskinesia in mice lacking axonally transported FGF14. Neuron 35, 25-38. doi: 10.1016/s0896-6273(02)00744-4
90. Woodward, W. R., Nishi, R., Meshul, C. K., Williams, T. E., Coulombe, M., and Eckenstein, F. P. (1992). Nuclear and cytoplasmic localization of basic fibroblast growth factor in astrocytes and CA2 hippocampal neurons.J. Neurosci. 12, 142-152.
91. Yoshimura, S., Takagi, Y., Harada, J., Teramoto, T., Thomas, S. S., Waeber, C., et al. (2001). FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc. Natl. Acad. Sci. U S A 98, 5874-5879. doi: 10. 1073/pnas.101034998
92. Zanni, G., Barresi, S., Travaglini, L., Bernardini, L., Rizza, T., Digilio, M. C., et al. (2011). FGF17, a gene involved in cerebellar development, is downregulated in a patient with Dandy-Walker malformation carrying a de novo 8p deletion. Neurogenetics 12, 241-245. doi: 10. 1007/s10048-011-0283-8
93. Zucchini, S., Barbieri, M., and Simonato, M. (2005). Alterations in seizure susceptibility and in seizure-induced plasticity after pharmacologic and genetic manipulation of the fibroblast growth factor-2 system. Epilepsia 46(Suppl. 5), 52-58. doi: 10.1111/j.1528-1167. 2005.01009.x
94. Zucchini, S., Buzzi, A., Barbieri, M., Rodi, D., Paradiso, B., Binaschi, A., et al. (2008). FGF-2 overexpression increases excitability and seizure susceptibility but decreases seizure-induced cell loss. J. Neurosci. 28, 13112-13124. doi: 10. 1523/jneurosci.1472-08.2008