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

Hippocampal granule cells do not normally express the axonal growth and plasticity‐associated protein F1/GAP‐43 in the adult rat. Using three different methods that lead to hypersynchronous activity in limbic circuits, expression of F1/GAP‐43 mRNA can be induced in granule cells which is followed by sprouting in mossy fibers, the axons of granule cells.

[1]  J. Kapfhammer,et al.  Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice , 1995, Cell.

[2]  J. Freeman,et al.  A protein induced during nerve growth (GAP-43) is a major component of growth-cone membranes , 1986, Science.

[3]  E. Nedivi,et al.  A protein associated with axon growth, GAP-43, is widely distributed and developmentally regulated in rat CNS , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  J. Schwob,et al.  Monoclonal antibodies show that kinase C phosphorylation of GAP-43 during axonogenesis is both spatially and temporally restricted in vivo , 1991, The Journal of cell biology.

[5]  J. Freeman,et al.  Changes in axonally transported proteins during axon regeneration in toad retinal ganglion cells , 1981, The Journal of cell biology.

[6]  C. Woolf,et al.  Partial denervation of the medial gastrocnemius muscle results in growth-associated protein-43 immunoreactivity in sprouting axons and schwann cells , 1993, Neuroscience.

[7]  M. Reynolds,et al.  GAP-43 expression in primary sensory neurons following central axotomy , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  S. Biffo,et al.  B‐50/GAP43 Expression Correlates with Process Outgrowth in the Embryonic Mouse Nervous System , 1990, The European journal of neuroscience.

[9]  G. Wilkin,et al.  Up-regulation of GAP-43 and growth of axons in rat spinal cord after compression injury , 1993, Journal of neurocytology.

[10]  P. Caroni,et al.  Depletion of 43-kD growth-associated protein in primary sensory neurons leads to diminished formation and spreading of growth cones , 1993, The Journal of cell biology.

[11]  Jau-Shyong Hong,et al.  Intrahippocampal injections of a specific μ-receptor ligand PL017 produce generalized convulsions in rats , 1988, Brain Research.

[12]  A. Vezzani,et al.  Increased Expression of GAP‐43, Somatostatin and Neuropeptide Y mRNA in the Hippocampus During Development of Hippocampal Kindling in Rats , 1993, The European journal of neuroscience.

[13]  W. Penfield,et al.  Memory deficit produced by bilateral lesions in the hippocampal zone. , 1958, A.M.A. archives of neurology and psychiatry.

[14]  M. Pende,et al.  Expression of GAP‐43 in the Granule Cells of Rat Hippocampus After Seizure‐induced Sprouting of Mossy Fibres: In Situ Hybridization and Immunocytochemical Studies , 1994, The European journal of neuroscience.

[15]  W. Gispen,et al.  Inhibition of nerve growth factor-induced B-50/GAP-43 expression by antisense oligomers interferes with neurite outgrowth of PC12 cells. , 1992, Biochemical and biophysical research communications.

[16]  J. Norden,et al.  Light-microscopic immunolocalization of the growth- and plasticity-associated protein GAP-43 in the developing rat brain. , 1988, Brain research.

[17]  L. Benowitz,et al.  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 , 1990, Neuroscience.

[18]  A. Routtenberg,et al.  Selective expression of protein F1/(GAP-43) mRNA in pyramidal but not granule cells of the hippocampus , 1991, Neuroscience.

[19]  W. J. Brown,et al.  Temporal Lobe Volumetric Cell Densities in Temporal Lobe Epilepsy , 1984, Epilepsia.

[20]  M. Tohda,et al.  Increase in Neurite Formation and Acetylene line Release by Transfection of Growth‐Associated Protein‐43 cDNA into NG108–15 Cells , 1993, Journal of neurochemistry.

[21]  G. Banker,et al.  Development of neuronal polarity: GAP-43 distinguishes axonal from dendritic growth cones , 1988, Nature.

[22]  M. Frotscher,et al.  Lesion‐induced mossy fibers to the molecular layer of the rat fascia dentata: Identification of postsynaptic granule cells by the Golgi‐EM technique , 1983, The Journal of comparative neurology.

[23]  D. Amaral.  A golgi study of cell types in the hilar region of the hippocampus in the rat , 1978, The Journal of comparative neurology.

[24]  H. Akil,et al.  Autoradiographic differentiation of mu, delta, and kappa opioid receptors in the rat forebrain and midbrain , 1987 .

[25]  N. Perrone-Bizzozero,et al.  Phospholipid-mediated delivery of anti-GAP-43 antibodies into neuroblastoma cells prevents neuritogenesis , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  D. Perry,et al.  Administration of kainic acid and colchicine alters μ and λ opiate binding in rat hippocampus , 1989, Brain Research.

[27]  J. Skene.  Axonal growth-associated proteins. , 1989, Annual review of neuroscience.

[28]  D. Lovinger,et al.  Selective increase in phosphorylation of a 47-kDa protein (F1) directly related to long-term potentiation. , 1985, Behavioral and neural biology.

[29]  J. McGinty,et al.  Kainic acid alters the metabolism of Met5-enkephalin and the level of dynorphin A in the rat hippocampus , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  A. Morton,et al.  Accelerated Differentiation in Response to Retinoic Acid After Retrovirally Mediated Gene Transfer of GAP‐43 into Mouse Neuroblastoma Cells , 1992, The European journal of neuroscience.

[31]  S. Finklestein,et al.  Anatomical distribution of the growth-associated protein GAP-43/B-50 in the adult rat brain , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  F. Gaarskjaer.  Organization of the mossy fiber system of the rat studied in extended hippocampi. I. Terminal area related to number of granule and pyramidal cells , 1978, The Journal of comparative neurology.

[33]  R. C. Collins,et al.  Kainic acid induced limbic seizures: metabolic, behavioral, electroencephalographic and neuropathological correlates , 1981, Brain Research.

[34]  W. Tetzlaff,et al.  Response of facial and rubrospinal neurons to axotomy: changes in mRNA expression for cytoskeletal proteins and GAP-43 , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  M. Tohyama,et al.  GAP-43 mRNA expression in facial motoneurons during regeneration: in situ hybridization histochemistry study using an alkaline phosphatase-labelled probe. , 1993, Acta oto-laryngologica. Supplementum.

[36]  T. Babb,et al.  Sprouting of GABAergic and mossy fiber axons in dentate gyrus following intrahippocampal kainate in the rat , 1990, Experimental Neurology.

[37]  D. Linden,et al.  The two major phosphoproteins in growth cones are probably identical to two protein kinase C substrates correlated with persistence of long- term potentiation , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  X. Qiao,et al.  Developmental analysis of hippocampal mossy fiber outgrowth in a mutant mouse with inherited spike-wave seizures , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  W. Gispen,et al.  Comparison of the immunocytochemical distribution of the phosphoprotein B-50 in the cerebellum and hippocampus of immature and adult rat brain , 1986, Brain Research.

[40]  R. Racine,et al.  Modification of seizure activity by electrical stimulation. II. Motor seizure. , 1972, Electroencephalography and clinical neurophysiology.

[41]  J. Coyle,et al.  In situ injection of kainic acid: A new method for selectively lesioning neuronal cell bodies while sparing axons of passage , 1978, The Journal of comparative neurology.

[42]  M. Fishman,et al.  The neuronal growth-associated protein GAP-43 induces filopodia in non-neuronal cells. , 1989, Science.

[43]  A. Routtenberg,et al.  Evidence for the coidentification of GAP-43, a growth-associated protein, and F1, a plasticity-associated protein , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  S. Laurberg,et al.  Commissural connections of the dentate area in the rat , 1977, The Journal of comparative neurology.

[45]  Robert B. Nelson,et al.  Gradients of protein kinase C substrate phosphorylation in primate visual system peak in visual memory storage areas , 1987, Brain Research.

[46]  W. Gispen,et al.  Expression of growth-associated protein B-50 (GAP43) in dorsal root ganglia and sciatic nerve during regenerative sprouting , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  W. Gispen,et al.  Phosphoprotein B-50 in nerve growth cones from fetal rat brain , 1985, Neuroscience Letters.

[48]  M. Fishman,et al.  Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43 , 1995, Cell.

[49]  C. Cotman,et al.  Specificity of synaptic growth in brain: remodeling induced by kainic acid lesions. , 1979, Progress in brain research.

[50]  S. Laurberg,et al.  Commissural and intrinsic connections of the rat hippocampus , 1979, The Journal of comparative neurology.

[51]  B. Grafstein,et al.  Effect of target removal on goldfish optic nerve regeneration: analysis of fast axonally transported proteins , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  D. Tauck,et al.  Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  Y. Ben-Ari,et al.  Limbic seizure and brain damage produced by kainic acid: Mechanisms and relevance to human temporal lobe epilepsy , 1985, Neuroscience.

[54]  F. Dudek,et al.  Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats , 1988, Brain Research.

[55]  J. Price,et al.  Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: A histological study , 1980, Neuroscience.

[56]  J. Olney,et al.  Acute dendrotoxic changes in the hippocampus of kainate treated rats , 1979, Brain Research.

[57]  E. Bird,et al.  Localization of the growth-associated phosphoprotein GAP-43 (B-50, F1) in the human cerebral cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  A. Routtenberg,et al.  Induction of F1/GAP-43 gene expression in hippocampal granule cells after seizures [corrected]. , 1993, Brain research. Molecular brain research.

[59]  R. Neve,et al.  The pattern of GAP-43 immunostaining changes in the rat hippocampal formation during reactive synaptogenesis. , 1990, Brain research. Molecular brain research.

[60]  C. Cotman,et al.  Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells , 1978, Nature.

[61]  J. Skene,et al.  Axonally transported proteins associated with axon growth in rabbit central and peripheral nervous systems , 1981, The Journal of cell biology.

[62]  S. Kish,et al.  Kainic acid induced seizures: Neurochemical and histopathological changes , 1983, Neuroscience.

[63]  D. Schreyer,et al.  Fate of GAP-43 in ascending spinal axons of DRG neurons after peripheral nerve injury: delayed accumulation and correlation with regenerative potential , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[64]  A. Routtenberg.  Knockout mouse fault lines , 1995, Nature.

[65]  Y. Ben-Ari,et al.  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 , 1981, Neuroscience.

[66]  JO McNamara,et al.  Cellular and molecular basis of epilepsy , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[67]  P. Caroni,et al.  Phosphorylation-site mutagenesis of the growth-associated protein GAP- 43 modulates its effects on cell spreading and morphology , 1993, The Journal of cell biology.

[68]  B. Levin,et al.  Vibrissectomy induced changes in GAP‐43 immunoreactivity in the adult rat barrel cortex , 1992, The Journal of comparative neurology.

[69]  Richard G. Nilges,et al.  The arteries of the mammalian cornu ammonis , 1944 .

[70]  H. Lipp,et al.  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 , 1983, Behavioural Brain Research.

[71]  L. Benowitz,et al.  Mapping the development of the rat brain by GAP-43 immunocytochemistry , 1991, Neuroscience.

[72]  Carl W. Cotman,et al.  Selective reinnervation of hippocampal area CA1 and the fascia dentata after destruction of CA3-CA4 afferents with kainic acid , 1980, Brain Research.

[73]  S. Laurberg,et al.  Lesion‐induced sprouting of hippocampal mossy fiber collaterals to the fascia dentata in developing and adult rats , 1981, The Journal of comparative neurology.

[74]  A. M. Dam,et al.  Epilepsy and Neuron Loss in the Hippocampus , 1980, Epilepsia.

[75]  L. Seress,et al.  Structure of the granular layer of the rat dentate gyrus. A light microscopic and Golgi study. , 1981, Journal of anatomy.

[76]  Y. Ben-Ari,et al.  Epilepsy induced collateral sprouting of hippocampal mossy fibers: Does it induce the development of ectopic synapses with granule cell dendrites? , 1993, Hippocampus.

[77]  L. Villa-komaroff,et al.  Transfection of PC12 cells with the human GAP-43 gene: effects on neurite outgrowth and regeneration. , 1990, Brain research. Molecular brain research.

[78]  J. Zimmer.  Ipsilateral afferents to the commissural zone of the fascia dentata, demonstrated in decommissurated rats by silver impregnation , 1971, The Journal of comparative neurology.

[79]  A. Routtenberg,et al.  NMDA receptor blockade prevents kainate induction of protein F1/GAP-43 mRNA in hippocampal granule cells and subsequent mossy fiber sprouting in the rat. , 1995, Brain research. Molecular brain research.

[80]  J. Skene,et al.  Molecular Events in Axonal Regeneration , 1982 .

[81]  L. H. Lin,et al.  Synthesis and transport of GAP-43 in entorhinal cortex neurons and perforant pathway during lesion-induced sprouting and reactive synaptogenesis. , 1992, Brain research. Molecular brain research.

[82]  A. Lozano,et al.  Expression of the growth-associated protein GAP-43 in adult rat retinal ganglion cells following axon injury , 1991, Neuron.

[83]  J. Zimmer.  Changes in the Timm sulfide silver staining pattern of the rat hippocampus and fascia dentata following early postnatal deafferentation. , 1973, Brain research.

[84]  G. Golarai,et al.  Septotemporal variation of the supragranular projection of the mossy fiber pathway in the dentate gyrus of normal and kindled rats , 1992, Hippocampus.

[85]  Y. Ben-Ari,et al.  Kainate binding sites in the hippocampal mossy fibers: Localization and plasticity , 1987, Neuroscience.

[86]  C. Mitchell,et al.  Opioid-induced epileptiform bursting in hippocampal slices: higher susceptibility in ventral than dorsal hippocampus. , 1990, The Journal of pharmacology and experimental therapeutics.

[87]  M. Bisby.  Dependence of GAP43 (B50, F1) transport on axonal regeneration in rat dorsal root ganglion neurons , 1988, Brain Research.

[88]  W. Gispen,et al.  Colchicine effect on B-50/GAP43 phosphoprotein localization in rat dorsal root ganglion explants , 1989, Neuroscience Letters.

[89]  W. Cowan,et al.  An autoradiographic study of the organization of intrahippocampal association pathways in the rat , 1978, The Journal of comparative neurology.