Null mutation of c-fos impairs structural and functional plasticities in the kindling model of epilepsy

Journal of Neuroscience

Volumn 16, Issue 12, 1996, Pages 3827-3836

  Watanabe, Yoshinori ^a   Johnson, Randall S ^b   Butler, Linda S ^a   Binder, Devin K ^a   Spiegelman, Bruce M ^b   Papaioannou, Virginia E ^c   McNamara, James O ^a,d  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c The New York Presbyterian Hospital   (United States)

^d DURHAM VA MEDICAL CENTER   (United States)

Author keywords

axonal reorganization; c fos; epilepsy; immediate early genes; kindling; plasticity

Indexed keywords

EPILEPSY; GENE MUTATION; GRANULE CELL; HIPPOCAMPUS; HISTOCHEMISTRY; IMMEDIATE EARLY GENE; MORPHOMETRICS; MOSSY FIBER; ONCOGENE C FOS; PLASTICITY; PRIORITY JOURNAL; REVIEW;

EID: 0029922536     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-12-03827.1996     Document Type: Review

References (54)

1. Aigner L, Arber S, Kapfhammer JP, Laux T, Schneider C, Botteri F, Brenner H-R, Caroni P (1995) Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell 83:269-278.
2. Alcantara AA, Greenough WT (1993) Developmental regulation of Fos and Fos-related antigens in cerebral cortex, striatum, hippocampus, cerebellum of the rat. J Comp Neurol 334:75-85.
3. Angevine JB (1965) Time of neuron origin in the hippocampal region. Exp Neurol [Suppl] 2:1-70.
4. Bartel DP, Sheng M, Lau LF, Greenberg ME (1989) Growth factors and membrane depolarization activate distinct programs of early response gene expression: dissociation of fos and jun induction. Genes Dev 3:304-313.
5. Bayer SA, Altman J (1974) Hippocampal development in the rat. Cytogenesis and morphogenesis examined with autoradiography and low-level X-irradiation. J Comp Neurol 158:55-80.
6. Bendotti C, Vezzani A, Tarizzo G, Samanin R (1993) Increased expression of GAP-43, somatostatin and neuropeptide Y mRNA in the hippocampus during development of hippocampal kindling in rats. Eur J Neurosci 5:1312-1320.
7. Bengzon J, Kokaia Z, Ernfors P, Kokaia M, Leanza G, Nilsson OG, Persson H, Lindvall O (1993) Regulation of neurotrophin and trkA and trkC tyrosine kinase receptor messenger RNA expression in kindling. Neuroscience 53:433-436.
8. Bertram EH, Lothman EW (1993) Morphometric effects of intermittent kindled seizures and limbic status epilepticus in the dentate gyrus of the rat. Brain Res 603:25-31.
9. Bertram EH, Lothman EW, Lenn NJ (1990) The hippocampus in experimental chronic epilepsy: a morphometric analysis. Ann Neurol 27:43-48.
10. Bugra K, Pollard H, Charton G, Moreau J, Ben-Ari Y, Khrestchatisky M (1994) aFGF, bFGF and flg mRNAs show distinct patterns of induction in the hippocampus following kainate-induced seizures. Eur J Neurosci 6:58-66.
11. Cavazos JE, Sutula TP (1990) Progressive neuronal loss induced by kindling: a possible mechanism for mossy fiber synaptic reorganization and hippocampal sclerosis. Brain Res 527:1-6.
12. Cavazos JE, Das I, Sutula TP (1994) Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures. J Neurosci 14:3106-3121.
13. Cavazos JE, Golarai G, Sutula T (1991) Mossy fiber sprouting reorganization induced by kindling: time course of development, progression, and permanence. J Neurosci 11:2795-2803.
14. Cline HT, Constantine-Paton M (1990) NMDA receptor agonists and antagonists alter retinal ganglion cell arbor structure in the developing frog retinotectal projection. J Neurosci 10:1197-1216.
15. Collazo D, Takahashi H, McKay RDG (1992) Cellular targets and trophic functions of neurotrophin-3 in the developing rat hippocampus. Neuron 9:643-656.
16. Cronin J, Obenaus A, Houser CR, Dudek FE (1992) Electrophysiology of dentate granule cells after kainate-induced synaptic reorganization of the mossy fibers. Brain Res 573:305-310.
17. Danscher G (1981) Histochemical demonstration of heavy metals: a revised version of the silver sulphide method suitable for both light and electron microscopy. Histochemistry 71:1-16.
18. Dasheiff RM, McNamara JO (1982) Intradentate colchicine retards the development of amygdala kindling. Ann Neurol 11:347-352.
19. Ernfors P, Bengzon J, Kokaia Z, Persson H, Lindvall O (1991) Increased levels of messenger RNAs for neurotrophic factors in the brain during kindling epileptogenesis. Neuron 7:165-176.
20. Frotscher M, Zimmer J (1983) Lesion-induced mossy fibers to the molecular layer of the rat fascia dentata: identification of post-synaptic granule cells by the Golgi-EM technique. J Comp Neurol 215:299-311.
21. Gall CM (1993) Seizure-induced changes in neurotrophin expression: implications for epilepsy. Exp Neurol 124:150-166.
22. Gall CM, Isackson PJ (1989) Limbic seizures increase neuronal production of messenger RNA for nerve growth factor. Science 245:758-761.
23. Gall CM, Berschauer R, Isackson PJ (1994) Seizures increase basic fibroblast growth factor mRNA in adult rat forebrain neurons and glia. Mol Brain Res 21:190-205.
24. Goddard GV, McIntyre DC, Leech CK (1969) A permanent change in brain function resulting from daily electrical stimulation. Exp Neurol 25:295-330.
25. Hosford DA, Simonato M, Cao Z, Garcia-Cairasco N, Silver JM, Butler L, Shin C, McNamara JO (1995) Differences in the anatomic distribution of immediate-early gene expression in amygdala and angular bundle kindling development. J Neurosci 15:2513-2523.
26. Hubel DH, Wiesel TN (1965) Binocular interaction in striate cortex of kittens raised with artificial squint. Science 28:1041-1059.
27. Ip YN, Li Y, Yancopoulos GD, Lindsay RM (1993) Cultured hippocampal neurons show responses to BDNF, NT3, and NT-4, but not NGF. J Neurosci 13:3394-3405.
28. Johnson RS, Spiegelman BM, Papaioannou V (1992) Pleiotropic effects of a null mutation in the c-fos proto-oncogene. Cell 71:577-586.
29. Kiessling M, Gass P (1993) Immediate early gene expression in experimental epilepsy. Brain Pathol 3:381-393.
30. Labiner DM, Butler LS, Cao Z, Hosford DA, Shin C, McNamara JO (1993) Induction of c-fos mRNA by kindled seizures: complex relationship with neuronal burst firing. J Neurosci 13:744-751.
31. Laurberg S, Zimmer J (1981) Lesion-induced sprouting of hippocampal mossy fiber collaterals to the fascia dentata in developing and adult rats. J Comp Neurol 200:433-459.
32. Lowenstein DH. Arsenault L (1996) The effects of growth factors on the survival and differentiation of cultured dentate gyrus neurons. J Neurosci 16:1759-1769.
33. Mattson MP, Murrain M, Guthrie PB, Kater SB (1989) Fibroblast growth factor and glutamate: opposing roles in the generation and degeneration of hippocampal neuroarchitecture. J Neurosci 9:3728-3740.
34. McNamara JO, Bonhaus DW, Shin C (1993) The kindling model of epilepsy. In: Epilepsy: models, mechanisms, and concepts (Schwartzkroin PA, ed), pp 27-47. Cambridge, UK: Cambridge UP.
35. Meberg PJ, Gall CM, Routtenberg A (1993) Induction of F1/GAP-43 gene: expression in hippocampal granule cells after seizures. Mol Brain Res 17:295-297.
36. Morgan JI, Cohen DR, Hempstead JL, Curran T 1987 Mapping patterns of c-fos expression in the central nervous system after seizure. Science 237:192-197.
37. Morgan JI, Curran T (1991) Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu Rev Neurosci 14:421-451.
38. Nedivi E, Basi OS, Akey IV, Skene JH (1992) A neural-specific GAP-43 core promoter located between unusual DNA elements that interact to regulate its activity. J Neurosci 12:691-704.
39. Okazaki MM, Evenson DA, Nadler JV (1995) Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: visualization after retrograde transport of biocytin. J Comp Neurol 352:515-534.
40. Patel MM, McNamara JO (1995) Selective enhancement of axonal branching of cultured dentate gyrus neurons by neurotrophic factors. Neuroscience 69:763-770.
41. Pennypacker KR, Hong J-S, McMillian MK (1995) Implications of prolonged expression of Fos-related antigens. Trends Pharmacol Sci 16:317-321.
42. Purves D (1994) Neural activity and the growth of the brain. Cambridge, UK: Cambridge UP.
43. Racine RJ (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294.
44. Represa A, Jorquera I, Le Gal La Salle G, Ben-Ari Y (1993) Epilepsy induced collateral sprouting of hippocampal mossy fibers: does it induce the development of ectopic synapses with granule cell dendrites? Hippocampus 3:257-268.
45. Schreiber SS, Tocco G, Najm I, Finch CE, Johnson SA, Baudry M (1992) Absence of c-fos induction in neonatal brain after seizures. Neurosci Lett 136:31-35.
46. Shatz CJ (1990) Impulse activity and the patterning of connections during CNS development. Neuron 5:745-756.
47. Shibata F, Baird A, Florkiewicz RZ (1991) Functional characterization of the human basic fibroblast growth factor gene promoter. Growth Factors 4:277-287.
48. Sloviter RS (1992) Possible functional consequences of synaptic reorganization in the dentate gyrus of kainate-treated rats. Neurosci Lett 137:91-96.
49. Sperber EF, Haas KZ, Stanton PK, Moshe SL (1991) Resistance of the immature hippocampus to seizure-induced synaptic reorganization. Dev Brain Res 60:88-93.
50. Sutula T, He XX, Cavazos J, Scott G (1988) Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science 239:1147-1150.
51. Sutula TP, He XX, Hurtenbach C (1987) Facilitation of kindling by CA3/CA4 lesions: evidence for epileptogenic potential of lesion-induced sprouting and synaptic reorganization. Epilepsia 28:947.
52. Tauck DL, Nadler JV (1985) Evidence for functional mossy fiber sprouting in hippocampal formation of kainic acid treated rats. J Neurosci 5:1016-1022.
53. Walicke P, Cowan WM, 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.
54. Wang ZQ, Ovitt C, Grigoriadis AE (1992) Bone and haematopoietic defects in mice lacking c-fos. Nature 360:741-745.