Rapid induction by kainic acid of both axonal growth and F1/GAP-43 protein in the adult rat hippocampal granule cells

Journal of Comparative Neurology

Volumn 366, Issue 2, 1996, Pages 303-319

  Cantallops, Isabel ^a   Routtenberg, Aryeh ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

hippocampus; mossy fibers; plasticity; sprouting; Timm's staining

Indexed keywords

KAINIC ACID;

ANIMAL CELL; ARTICLE; GENE INDUCTION; GRANULE CELL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MOSSY FIBER; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE SPROUTING; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTOGENESIS;

ANIMALS; ANTIBODIES, MONOCLONAL; AXONS; COLORING AGENTS; DENDRITES; EXCITATORY AMINO ACID AGONISTS; GAP-43 PROTEIN; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; KAINIC ACID; MALE; MEMBRANE GLYCOPROTEINS; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER;

EID: 0030039640     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960304)366:2<303::AID-CNE9>3.0.CO;2-9     Document Type: Article

References (103)

1. Aigner, L., S. Arber, J.P. Kapfhammer, T. Laux, C. Schneider, F. Botteri, H.-R. Brenner, and P. Caroni (1995) Overexpression of the neuronal growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell 83:269-278.
2. Aigner, L., and P. Caroni (1993) Depletion of 43-kD growth associated protein in primary sensory neurons leads to diminished formation and spreading of growth cones. J. Cell Biol. 123:417-429.
3. Amaral, D.G. (1978) A Golgi study of cell types in the hilar region of the hippocampus in the rat. J. Comp. Neurol. 152:851-914.
4. Babb, T.L., W.J. Brown, J. Pretorius, C. Davenport, J. Lieb, and P.H. Crandall (1984) Temporal lobe volumetric cell densities in temporal lobe epilepsy. Epilepsia 25:729-740.
5. Ben-Ari, Y (1985) Limbic seizure and brain damage produced by kainic acid: Mechanisms and relevance to human lobe epilepsy. Neuroscience 14:375-403.
6. Ben-Ari, Y., and M. Gho (1988) Long-lasting modification of the synaptic properties of rat CA3 hippocampal neurones induced by kainic acid. J. Phys. 404:365-384
7. Ben-Ari, Y., and A. Represa (1990) Brief seizure episodes induce long-term potentiation and mossy fiber sprouting in the hippocampus. T I N.S. 13:312-318.
8. Ben-Ari, Y., E. Tremblay, D. Riche, G. Ghilini, and R. Naquet (1981) Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: Metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience 6:1361-1391.
9. Bendotti, C., S. Baldessari, R. Samanin, and S. De Biasi (1994a) Ultrastructural immunolocalization of GAP-43 in the sprouted mossy fibres of kainic acid lesioned rats. NeuroReport 5:2645-2648.
10. Bendotti, C., M. Pende, and R. Samanin (1994b) Expression of GAP-43 in the granule cells of rat hippocampus after seizure-induced sprouting of mossy fibres: In situ hybridization and immunocytochemical studies. Eur. J. Neurosci. 6:509-515.
11. Bendotti, C., A. Vezzani, G Tarizzo, and R Samanin (1993) Increased expression of GAP-43, somatostatin and neuropeptide Y mRNA in hippocampus during development of hippocampal kindling in rats. Eur. J. Neurosci. 5.1312-1320.
12. Benowitz, L.I., and A. Routtenberg (1987) A membrane phosphoprotein associated with neural development, axonal regeneration, phospholipid metabolism and synaptic plasticity. T I.N.S. 10:527-531.
13. Benowitz, L.I., P.J. Apostolides, N.I Perrone-Bizzozero, S.P Finklestein, and H. Zwiers (1988) Anatomical distribution of the growth-associated protein GAP-43/B-50 in the adult rat brain. J. Neurosci. 5:339-352.
14. Benowitz, L.I., N I Perrone-Bizzozero, S.P. Finklestein, and E.D. Bird (1989) Localization of the growth-associated phosphoprotein GAP-43 (B-50, F1) in the human cerebral cortex. J. Neurosci. 5:990-995.
15. Benowitz, L.I., W.R. Rodriguez, and R.L. Neve (1990) The pattern of GAP-43 immunostaining changes in the rat hippocampal formation during reactive synaptogenesis. Mol. Brain Res. 8:17-23.
16. Biffo. S., J. Verhaagen, L H. Schrama, W. Danho, and F.L. Margolis (1990) B-50/GAP43 expression correlates with process outgrowth in the embryonic mouse nervous system. Eur. J. Neurosci. 2:487-499.
17. Bisby, M.A. (1988) Dependence of GAP43 (B50, F1) transport on axonal regeneration in rat dorsal root ganglion neurons. Brain Res. 455:157-161
18. Campbell, G., P.N. Anderson, M. Turmaine, and A.R. Lieberman (1991) GAP-43 in the axons of mammalian CNS neurons regenerating into peripheral nerve grafts. Exp. Brain Res. 87:67-74.
19. Cavazos, J.E., G. Golarai, and T.P. Sutula (1992) Septotemporal variation of the supragranular projection of mossy fiber pathway in the dentate gyrus of normal and kindled rats. Hippocampus 2:363-372.
20. Chong, M.S., M.L. Reynolds, N. Irwin, R.E. Coggeshall, P.C. Emson, L.J. Benowitz, and C.J. Woolf (1994) GAP-43 expression in primary sensory neurons following central axotomy J. Neurosci. 14:4375-4384.
21. Coreoran, M.E., R.K. McNamara, R.K. Gilbert, and A. Routtenberg (1993) Induction of F1/GAP-43 mRNA in dentate granule cells after perforant path kindling. Soc. Neurosci. Abstr. 19:606.
22. Cotman, C W. (1979) Specificity of synaptic growth in brain: remodeling induced by kainic acid. Prog. Brain Res. 51:203-215.
23. Coyle, J.T., M.E. Molliver, and M.J. Kuhar (1978) In situ injection of kainic acid. A new method for selectively Iesioning neuronal cell bodies while sparing axons of passage. J. Comp. Neurol. 180:301-324.
24. Cronin, J., and F.E. Dudek (1988) Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res. 474:181-184.
25. Curtis, R., D. Green, R.M. Lindsay, and G.P. Wilkin (1993) Up-regulation of GAP-43 and growth of axons in rat spinal cord after compression injury. J. Neurocytology 22:51-64.
26. Dam, A.M. (1980) Epilepsy and neuron loss in the hippocampus. Epilepsia 21:617-629.
27. Dani, J.W., D.M. Armstrong, and L.I. Benowitz (1991) Mapping the development of the rat brain by GAP-43 immunocytochemistry. Neuroscience 40:277-288.
28. Davenport, C. J., W.J. Brown, and T.L. Babb (1990b) Sprouting of GABAergic and mossy fiber axons in dentate gyrus following intrahippocampal kainate in the rat. Exp. Neurol. 109:180-190.
29. DeGraan, P.N.E., C.O.M. van Hoof, B.C. Tilly, A.B. Oestreicher, P. Schotman, and W.H. Gispen (1985) Phosphoprotein B-50 in nerve growth cones from fetal rat brain. Neurosci. Lett. 61:235-241.
30. Doster, S.K., A.M. Lozano, A J. Aguayo, and M.B. Willard (1991) Expression of the growth-associated protein GAP-43 in adult rat retinal ganglion cells following axon injury. Neuron 6:635-647.
31. Dunn-Meynell, A.A., L I Benowitz, and B.E Levin (1992) Vibrissectomy induced changes in GAP-43 immunoreactivity in the adult rat barrel cortex. J Comp. Neurol 315.160-170.
32. Frotscher, M., and J. Zimmer (1983) Lesion-induced mossy fibers to the molecular layer of the rat fascia dentata: Identification of postsynaptic granule cells by the Golgi-EM technique. J. Comp. Neurol. 215:299-311.
33. Gaarskjaer, F.B. (1978) Organization of the mossy fiber system of the rat studied in extended hippocampi. J. Comp. Neurol. 178:49-72.
34. Goslin, K., D. Schreyer, J.H.P. Skene, and G. Banker (1988) Development of neuronal polarity: GAP-43 distinguishes axonal from dendritic growth cones Nature 336:672-674
35. Haug, F.-M.S. (1973) Heavy metals in the brain. A light microscope study of the rat with Timm's sulphide silver method. Methodological considerations and cytological and regional staining patterns. Advanc. Anat. Embryol. Cell. Biol. 47:1-71
36. Haug, F.-M.S. (1974) Light microscopical mapping of the hippocampal region, the pyriform cortex and the corticomedial amygdaloid nuclei of the rat with Timm's sulphide silver method I. Area dentata, hippocampus and subiculum. Z. Anat. Entwickl.-Gesch. 145:1-27.
37. Hjorth-Simonsen, A., and S. Laurberg (1977) Commissural connections of the dentate area in the rat. J. Comp. Neurol. 174:591-606.
38. Jacobson, R.D., I. Virag, and P. Skene (1986) A protein associated with axon growth, GAP-43, is widely distributed and developmentally regulated in rat CNS. J. Neurosci. 6:1843-1855.
39. Jap Tjoen San, E.R.A., M. Schmidt-Michels, A.B. Oestreicher, W.H. Gispen, and P. Schotman (1992) Inhibition of nerve growth factor-induced B-50/GAP-43 expression by antisense oligomers interferes with neurite outgrowth of PC12 cells. Biochem. Biophys. Res. Comm. 187:839-846.
40. 5-Enkephalin and the level of dynorphin A in the rat hippocampus. J. Neurosci. 6:3094-3102.
41. Kugamai-Tohda, C , M. Tohda, and Y Nomura (1993) Increase in neurite formation and acetylcholine release by transfection of growth-associated protein-43 cDNA into NG108-15 cells. J. Neurochem. 61:526-532.
42. Laurberg, S. (1979) Commissural and intrinsic connections of the rat hippocampus. J. Comp. Neurol. 184:685-708.
43. Laurberg, S., and J. Zimmer (1981) Lesion-induced sprouting of hippocampal mossy fiber collaterals to the fascia dentata in developing and adult rats J. Comp Neurol 200:433-459
44. Lee, P.H.K., J. Obie, and J.S. Hong (1989) Opioids induce convulsions and wet dog shakes in rats. Brain Res 441:381-385.
45. Lee, P.H.K., C.W. Xie, D V. Lewis, W.A. Wilson, C.L. Mitchell, and J.S. Hong (1990) Opioid-induced epileptiform bursting in hippocampal slices. Higher susceptibility in ventral than dorsal hippocampus. J. Pharmac. Exp. Ther. 253:545-551
46. Lin, L -H., S. Bock, K. Carpenter, M. Rose, and J.J. Norden (1992) Synthesis and transport of GAP-43 in entorhinal cortex neurons and perforant pathway during lesion-induced sprouting and reactive synaptogenesis. Mol. Brain Res. 14.147-153.
47. Lothman, F.W., and R. C. Collins (1981) Kainic acid induced limbic seizures: Metabolic, behavioral, electroencephalographic and neuropathological correlates. Brain Res. 218:299-318.
48. Mansour, A., H. Khachaturian, M.E. Lewis, H. Akil, and S.J. Watson (1987) Autoradiographic differentiation of mu. delta, and kappa opioid receptors in the rat forebrain and midbrain. J. Neurosci. 7:2445-2464.
49. McGuire, C.B., G.J. Snipes, and J.J. Norden (1988) Light-microscopic immunolocalization of the growth- and plasticity-associated protein GAP-43 in the developing rat brain. Dev. Brain Res. 41:277-271.
50. McNamara, J.O. (1994) Cellular and molecular basis of epilepsy. J. Neurosci. 14:3413-3425.
51. McNamara, R.K., P.J. Meberg, and A. Routtenberg (1993) Kainic acid elicits a transient induction of F1/GAP-43 mRNA in dentate gyrus granule cells: Role of seizures and opioids. Soc. Neurosci. Abtrs. 19:805.
52. McNamara, R.K., and A. Routtenberg (1995) NMDA receptor blockade prevents kainate induction of protein F1/GAP-43 mRNA in hippocampal granule cells and subsequent mossy fiber sprouting in the rat. Mol. Brain. Res. 35:22-28.
53. Meberg, P.J., and A. Routtenberg (1991) Selective expression of protein F1/(GAP-43) mRNA in pyramidal but not granule cells of the hippocampus. Neuroscience 45:721-733.
54. Meberg, P.J., and A. Routtenberg (1993) Induction of F1/GAP-43 gene expression in hippocampal granule cells after seizures. Mol. Brain Res. 17:295-299.
55. Meberg, P.J., L.E. Jarrard, and A. Routtenberg (1996) Is the lack of protein F1/GAP-43 mRNA in granule cells target-dependent? Brain Res. (in press).
56. Mehta, A., M.L. Reynolds, and C.J. Woolf (1993) Partial denervation of the medial gastrocnemius muscle results in growth-associated protein-43 immunoreactivity in sprouting axons and Schwann cells. Neuroscience 57:433-442
57. Meiri, K.F., L.E. Bickerstaff, and J.E. Schwob (1991) Monoclonal antibodies show that kinase C phosphorylation of GAP-43 during axonogenesis is both spatially and temporally restricted in vivo. J. Cell Biol. 112:991-1005.
58. Morton, A.J., and T.N. Buss (1992) Accelerated differentiation in response to retinoic acid after retrovirally mediated gene transfer of GAP-43 into mouse neuroblastoma cells. Eur. J. Neurosci. 4:910-916.
59. Nadler, J.V., B.W. Perry, and C.W. Cotman (1978) Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature 271:676-677.
60. Nadler, J V., B.W Perry, and C.W Cotman (1980) Selective reinnervation of hippocampal area CA1 and fascia dentata after destruction of CA3-CA4 afferents with kainic acid. Brain Res. 182:1-9.
61. Nelson, R.B., D.P. Friedman, J.B. O'Neill, M. Mishkin, and A. Routtenberg (1987) Gradients of protein kinase C substrate phosphorylation in primate visual system peak in visual memory storage areas. Brain Res. 416:387-392.
62. Nelson, R.B., D.J. Linden, C. Hyman, K.H Pfenninger, and A Routtenberg (1989) The two major phosphoproteins in growth cones are probably identical to two protein kinase C substrates correlated with persistance of long-term potentiation. J. Neurosci. 9 381-389.
63. Nilges, R.G. (1944) The arteries of the mammalian cornu ammonis. J. Comp. Neurol. 80:177-190.
64. Oestreicher, A B., and W.H. Gispen (1986) Comparison of the immunocytochemical distribution of the phosphoprotein B-50 in the cerebellum and hippocampus of immature and adult rat brain. Brain Res. 375:267-279.
65. Olney, J.W., T. Fuller, and T. De Gubareff (1979) Acute dendrotoxic changes in the hippocampus of kainate treated rats. Brain Res. 176:91-100.
66. Penfield, W., and B. Milner (1958) Memory deficit produced by bilateral lesions in the hippocampal zone. Arch. Neurol. Psychiatry 79:475-497.
67. Perry, D.C., and L.M. Grimes (1989) Administration of kainic acid and colchicine alters mu and lambda opiate binding in rat hippocampus. Brain Res. 477:100-108.
68. Perry, G.W., D.W. Burmeister, and B. Grafstein (1990) Effect of target removal on goldfish optic nerve regeneration. Analysis of fast axonally transported proteins. J Neurosci. 10:3439-3448.
69. Qiao, X., and J.L. Noebels (1993) Developmental analysis of hippocampal mossy fiber outgrowth in a mutant mouse with inherited spike-wave seizures J. Neurosci. 13:4622-4635.
70. Racine, R. (1972) Modification of seizure activity by electrical stimulation II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32:281-296.
71. Ramón y Cajal. S. (1901) Trabajos del Laboratorio de Investigaciones Biológicas de la Universidad de Madrid, Tomo I. Imprenta y Libreria de Nicolás Moya. Madrid.
72. Represa, A., I. Jorquera, G. Le Gal La Salle, and Y. Ben-Ari (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.
73. Represa, A., E. Tremblay, and Y. Ben-Ari (1987) Kainate binding sites in the hippocampal mossy fibers: localization and plasticity. Neuroscience 50:739-748
74. Rosenthal, A., S.Y. Chan, W. Henzel, C. Haskell, W.-J. Kuang, E. Chen, J.N. Wilcox, A. Ullrich, D.V. Goeddel, and A. Routtenberg (1987) Primary structure and mRNA localization of protein F1, a growth-related protein kinase C substrate, associated with synaptic plasticity. E.M.B O.J. 6:3641-3646.
75. Routtenberg, A. (1995) Knockout mouse fault lines. Nature 374:314-315
76. Routtenberg, A., D M. Lovinger, and O. Steward (1985) Selective increase in phosphorylation state of a 47kD protein (F1) directly related to long-term potentiation. Behav. Neural Biol. 43:3-11.
77. Saika, T., H. Kiyama, M. Tohyama, and T. Matsunaga (1993) GAP-43 mRNA expression in facial motoneurons during regeneration: In situ hybridization histochemistry study using an alkaline phosphatase-labelled probe. Acta Otolaryngol. Suppl. 501:80-84.
78. Schmidt-Michels, M., P.M Edwards, A.B. Oestreicher, and W.H Gispen (1989) Colchicine effect on B-50/GAP43 phosphoprotein localization in rat dorsal root ganglion explants. Neurosci. Lett. 97:285-290.
79. Schreyer, D.J., and J.H. Skene (1991) Fate of GAP-43 in ascending spinal axons of DRG neurons after peripheral nerve injury: Delayed accumulation and correlation with regenerative potential. J. Neurosci. 11:3738-3751.
80. Schwegler, H., and H.P. Lipp (1983) Hereditary covariations of neuronal circuitry and behavior correlations between the proportions of hippocampal synaptic fields in the regio inferior and two-way avoidance in mice and rats. Behav. Brain Res 7:1-38.
81. Schwob, J.E., T. Fuller, J.L. Price, and J.W. Olney (1980) Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: A histological study. Neuroscience 5:991-1014.
82. Seress, L., and J. Pokorny (1981) Structure of the granular layer of the rat dentate gyrus. A light microscopic and Golgi study. J. Anat. 133:181-195.
83. Serrano, P.A., I. Cantallops, R.L. Neve, and A. Routtenberg (1995) HSV-mediated F1 (GAP-43) gene transfer Evidence for F1-mRNA induction and knockdown of kainate-induced F1-mRNA Soc Neurosci. Abst 21:1317.
84. Shea, T.B , N.I. Perrone-Bizzozero, M.L. Beermann, and L.I. Benowitz (1991) Phospholipid-mediated delivery of anti-GAP-43 antibodies into neuroblastoma cells prevents neuritogenesis. J Neurosci. 11:1685-1690.
85. Skene, J.H.P. (1989) Axonal growth-associated proteins. Annu. Rev. Neurosci. 12:127-156.
86. Skene, J H.P., and M. Willard (1981a) Changes in axonally transported proteins during axon regeneration in toad retinal ganglion cells. J Cell Biol. 89:86-95.
87. Skene, J.H P., and M. Willard (1981b) Axonally transported proteins associated with axon growth in rabbit central and peripheral nervous systems. J Cell Biol. 80:96-103.
88. Skene, J.H.P., R D. Jacobson, G.J. Snipes, C.B. McGuire, J.J. Norden, and J.A. Freeman (1986) A protein induced during nerve regeneration (GAP-43) is a major component of growth cone membranes Science 233:783-786.
89. Snipes, G.J., S.Y. Chan, C.B. McGuire, B R. Costello, J.J Norden, J A. Freeman, and A. Routtenberg (1987) Evidence for the coidentification of GAP43, a growth-associated protein and F1, a plasticity-associated protein. J. Neurosci. 7.4066-4075.
90. Sperk, G., H. Lassmann, H. Baran, S.J. Kish, F. Seitelberger, and O. Hornnykiewicz (1983) Kainic acid induced seizures: Neurochemical and histopathological changes. Neuroscience 20:1301-1315.
91. Strittmatter, S.M., C. Fankhauser, P.L. Huang, H. Mashimo, and M.C. Fishman (1995) Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43. Cell 80:445-452.
92. Swanson, L.W., J.M. Wyss, and W.M. Cowan (1978) An autoradiographic study of the organization of intrahippocampal association pathways. J. Comp. Neurol. 181:681-716.
93. Tauck, D.L., and J.V. Nadler (1985) Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J. Neurosci. 5:1016-1022.
94. Tetzlaff, W., S.W. Alexander, F.D Miller, and M.A. Bisby (1991) Response of facial and rubrospinal neurons to axotomy: Changes in mRNA expression for cytoskeletal proteins and GAP-43. J. Neurosci. 11:2528-2544.
95. Van der Zee, C.E.E.M., H.B. Nielander, J.P. Vos, S Lopes da Silva, J. Verhaagen, B. Oestreicher, L.H. Schrama, P. Schotman, and W.H Gispen (1989) Expression of growth-associated protein B-50 (GAP43) in dorsal root ganglia and sciatic nerve during regenerative sprouting. J. Neurosci. 9:3505-3512
96. Widmer, F., and P Caroni (1993) Phosphorylation-site mutagenesis of the growth-associated protein GAP-43 modulates its effects on cell spreading and morphology. J. Cell Biol. 120:503-512.
97. Willard, M., and J.H.P. Skene (1982) Molecular events in axonal regeneration In Nicholls, J.G. (ed): Repair and Regeneration of the Nervous System. New York. Springer Verlag, pp. 71-89.
98. Williamson, J.M., E.H. Bertram, and E.W. Lothman (1991) Rapid kindling indicates regional differences in epileptogenicity in the hippocampal formation. Epilepsia 32:40.
99. Woolf, C.J., M.L. Reynolds, C Molander, C. O'Brien, R.M. Lindsay, and L.I. Benowitz (1990) The growth-associated protein GAP-43 appears in dorsal root ganglion cells and in the dorsal horn of the rat spinal cord following peripheral nerve injury. Neuroscience 34:465-478.
100. Yanker, B.A., L.I. Benowitz, L. Villa-Komaroff, and R.L. Neve (1990) Transfection of PC12 cells with the human GAP-43 gene- Effects on neurite outgrowth and regeneration. Mol. Brain Res. 7:39-44.
101. Zimmer, J. (1973) Changes in the Timm sulfide silver staining pattern of the rat hippocampus and fascia dentata following early postnatal deafferentation Brain Res. 64:313-326.
102. Zimmer, J. (1971) Ipsilateral afferents to the commissural zone of the fascia dentata, demonstrated in decommissurated rats by silver impregnation. J. Comp. Neurol. 142:393-16.
103. Zuber, M.X , D.W. Goodman, L.R. Karns, and M.C. Fishman (1989) The neuronal growth-associated protein GAP-43 induces filopodia in non-neuronal cells Science 244:1193-1195.