Temporal specific patterns of semaphorin gene expression in rat brain after kainic acid-induced status epilepticus

Hippocampus

Volumn 13, Issue 1, 2003, Pages 1-20

  Barnes, Gregory ^a   Puranam, Ram S ^a   Luo, Yuling ^b   McNamara, James O ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b NONE

Author keywords

CA1 region; Cerebral cortex; Epilepsy; Kainic acid; Semaphorin; Synaptic reorganization

Indexed keywords

BIOLOGICAL MARKER; COMPLEMENTARY DNA; KAINIC ACID; MESSENGER RNA; PENTOBARBITAL; SEMAPHORIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AXOPLASM FLOW; BRAIN CORTEX; BRAIN INJURY; BRAIN NERVE CELL; CONTROLLED STUDY; EPILEPTIC STATE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE LOCATION; GENOMIC IN SITU HYBRIDIZATION; HIPPOCAMPUS; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REVIEW; RNA PROBE; SYNAPSE;

ANIMALS; BRAIN; CEREBRAL CORTEX; EPILEPSY; GENE EXPRESSION REGULATION; GROWTH CONES; HIPPOCAMPUS; MALE; NEURAL PATHWAYS; NEURONAL PLASTICITY; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; RNA, MESSENGER; SEMAPHORINS; STATUS EPILEPTICUS; TIME FACTORS;

EID: 0037222764     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/hipo.10041     Document Type: Review

References (91)

1. Adams B, Sazgar M, Osehobo P, Van der Zee ZE, Diamond J, Fahnest M, Racine RJ. 1997. Nerve growth factor accelerates seizure development, enhances mossy fiber sprouting, and alters seizures induced decreased neuronal density in the kindling model of epilepsy. J Neurosci 17: 5288-5296.
2. Amaral DG, Witter MP. 1995. Hippocampal formation. In: Paxinos G, editor. The rat nervous system. New York: Academic Press. p 443-493.
3. Bagnard D, Lohrum M, Uziel D, Puschel AW, Bolz J. 1998. Semaphorins act as attractive and repulsive guidance signals during the development of cortical projections. Development 125:5043-5053.
4. Bagnard D, Thomasset N, Lohrum M, Puschel AW, Bolz J. 2000. Spatial distribution of guidance molecules regulate chemorepulsion and chemoattraction of growth cones. J Neurosci 20:1030-1035.
5. Barnes GN, Luo YL, McNamara JO. 2000. Status epilepticus is necessary but not sufficient to regulate neuropilin gene expression in mouse hippocampus after kainic acid status epilepticus. Epilepsia 41 (suppl 7):41.
6. Bausch S, McNamara JO. 2000. Synaptic connections from multiple hippocampal subfields contribute to hyperexcitiability of dentate granule cells in long-term organotypic hippocampal slice cultures. J Neurophysiol 84:2918-2932.
7. Ben-Ari Y. 1985. Limbic seizures and brain damage produced by kainic acid: mechanism and relevance to human temporal lobe epilepsy. Neuroscience 14:375-403.
8. Cabelli RJ, Hohn A, Shatz CJ. 1995. Inhibition of ocular dominance column formation by infusion of NT4/5 or BDNF. Science 267: 1662-1666.
9. Cabelli RJ, Shelton DL, Segal RA, Shatz CJ. 1997. Blockade of endogenous ligands of trkB inhibits formation of ocular dominance columns. Neuron 19:63-76.
10. Castellani V, Yue Y, Gao PP, Zhou R, Bolz J. 1998. Dual action of a ligand for Eph receptor tyrosine kinases on specific populations of axons during the development of cortical circuits. J Neurosci 18:4663-4672.
11. Chedotal A, Del Rio JA, Ruiz M, He Z, Borrell V, de Castro F, Ezan F, Goodman CS, Tessier-Lavigne M, Sotelo C, Soriano E. 1998. Semaphorins III and IV repel hippocampal axons via two distinct receptors. Development 125:4313-4323.
12. Chen H, Chedotal A, He Z, Goodman CS, Tessier-Lavigne M. 1997. Neuropilin 2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins E and semaphorin IV but not semaphorin III. Neuron 19:547-559.
13. Chen H, Bagri A, Zupicich JA, Zou Y, Stoeckli E, Pleasure SJ, Lowenstein DH, Skarnes WC, Chedotal A, Tessier-Lavigne M. 2000. Neuropilin 2 regulates the development of select cranial and sensory nerves and hippocampal mossy fiber projections. Neuron 25:43-56.
14. Chen LS, Wong JG, Banerjee PK, Snead OC III. 1996. Kainic acid-induced focal cortical seizure is associated with an increase of synaptophysin immunoreactivity in the cortex. Exp Neurol 141:25-31.
15. Chirgwin JJ, Przbyla AE, MacDonald RJ, Rutter WJ. 1979. Isolation of biologically active RNA from sources enriched in ribonuclease. Biochemistry 18:5294.
16. Cline HT, Constatine-Paton M. 1990. NMDA receptor agonists and antagonists after retinal ganglion cell arbor structure in developing frog retinotectal projections. J Neurosci 38:248-258.
17. Darin-Smith C, Gilbert CD. 1994. Axonal sprouting accompanies functional reorganization in adult cat striate cortex. Nature 368:737-740.
18. de Castro F, Hu L, Drabkin H, Sotelo C, Chedotal A. 1999. Chemoattraction and chemorepulsion of olfactory bulb axons by different secreted semaphorins. J Neurosci 19:4428-4436.
19. Dellar T, Frotscher M. 1997. Lesion-induced plasticity of central neurons; sprouting of single fibers in the rat hippocampus after unilateral entorhinal cortex lesion. Prog Neurobiol 53:687-727.
20. Esclapez M, Hirsch J, Ben-Ari Y, Bernard C. 1999. Newly formed excitatory pathways provide a substrate for hyperexcitability in experimental temporal lobe epilepsy. J Comp Neurol 408:449-460.
21. Giger RJ, Pasterkamp RJ, Heijnen S, Holtmaat JGD, Verhaagen J. 1998a. Anatomical distribution of the chemorepellant semaphorin III/D in adult rat and human brain: predominant expression in structures of the olfactory-hippocampal pathway and the motor system. J Neurosci Res 52:27-42.
22. Giger RJ, Urquhart ER, Gillespie SK, Levengood DV, Ginty DD, Kolodkin AL. 1998b. Neuropilin 2 is a receptor form semaphorin IV: insight into the structural basis of receptor function and specificity. Neuron 21:1079-1092.
23. Giger RJ, Cloutier J-F, Sahay A, Prinjha RK, Levengood DV, Moore SE, Pickering S, Simmons D, Rastan S, Walsh FS, Kolodkin AL, Ginty DD, Geppert M. 2000. Neuropilin-2 is required in vivo for selective axon guidance responses to secreted semaphorins. Neuron 25:29-41.
24. He Z, Tessier-Lavigne M. 1997. Neuropilin is a receptor for the axonal chemorepellant semaphorin III. Cell 90:739-751.
25. Holmes GL, Ben-Ari Y. 1998. Seizures in the developing brain: perhaps not so benign after all. Neuron 21:1231-1234.
26. Holtmaat JA, Gorter J, DeWit GMJ, DeWit J, Giger RJ, Lopes-deSilva FH, Verhaagen J. 1998. Transient down-regulation of semaphorin III/collapsin I expression in a rat model for temporal lobe epilepsy. Soc Neurosci Abs 24:541.
27. Hubel DH, Wiesel TN. 1965. Binocular interaction in striate cortex of kittens reared with artificial squint. J Neurophysiol 28:1041-1059.
28. Isbister CM, Tsai A, Wong ST, Kolodkin AL, O'Connor TP. 1999. Discrete roles for secreted and transmembrane semaphorins in neuronal growth cone guidance in vivo. Development 126:2007-2019.
29. Isokawa M, Levesque MF, Babb TL, Engel J Jr. 1993. Single mossy fiber axonal systems of human dentate granule cells in hippocampal slices from patients with temporal lobe epilepsy. J Neurosci 13:1511-1522.
30. Jones TA. 1999. Multiple synapse formation in the motor cortex opposite unilateral sensorimotor cortex lesions in adult rats. J Comp Neurol 414:57-66.
31. Kawakami A, Kitsukawa T, Takagi S, Fujisawa H. 1996. Developmentally regulated expression of a cell surface protein, neuropilin, in the mouse nervous system. J Neurobiol 29:1-17.
32. Kobayashi H, Koppel AM, Luo Y, Raper A. 1997. A role for collapsin I in olfactory and cranial sensory axon guidance. J Neurosci 17:8339-8352.
33. Kokaia M, Ernsfors P, Kokaia Z, Elmers E, Jaenisch R, Lindvall O. 1995. Suppressed epileptogenesis in BDNF mutant mice. Exp Neurol 133: 215-224.
34. Kolodkin A, Levengood DV, Rowe EG, Tai YT, Giger RJ, Ginty DD. 1997. Neuropilin is a semaphorin III receptor. Cell 90:753-762.
35. Le Gal La Salle G, Rougon G, Valin A. 1992. The embryonic form of neural cell surface molecules (E-NCAM) in the hippocampus and its reexpression on glial cells following kainic SCID status epilepticus. J Neurosci 12:872-882.
36. Lerea LS, McNamara JO. 1993. Inotropic glutatmate receptor subtypes activate c-fos transcription by distinct calcium-requiring intracellular signaling pathways. Neuron 10:31-41.
37. 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.
38. Luo Y, Shepard I, Li J, Renzi MJ, Chang S, Raper J. 1995. A family of molecules related to collapsin in the embryonic chick nervous system. Neuron 14:1131-1140.
39. Maffei L, Beradi N, Domenici L, Parisi V, Pizzorusso T. 1992. Nerve growth factor (NGF) prevents the shift in ocular dominance columns distribution of visual cortical neurons in monocularly deprived rats. J Neurosci 12:4651-4662.
40. Mathern GW, Babb T, Mischel PS, Vinters HV, Pretorius JK, Leite JP, Peacock WJ. 1996. Childhood generalized and mesial temporal epilepsies demonstrate different amounts and patterns of hippocampal neuron loss and mossy fiber synaptic reorganization. Brain 119:965-987.
41. Mathern GW, Pretorius JK, Manedoza D, Lozada A, Kornblum HI. 1998a. Hippocampal AMPA and NMDA mRNA levels correlate with aberrant facia dentate mossy fiber spouting in the pilocarpine model of spontaneous limbic epilepsy. J Neurosci Res 54:734-753.
42. Mathern GW, Price G, Rosales C, Pretorius JK, Lozada A, Mendoza D. 1998b. Anoxia during kainate status epilepticus shortens behavioral convulsions but generates hippocampal neuron loss and supragranular mossy finer sprouting. Epilepsy Res 30:133-151.
43. Matthes DJ, Sink H, Kolodkin A, Goodman CS. 1995. Semaphorin II can function as a selective inhibitor of specific synaptic arborizations. Cell 81:631-639.
44. McNamara JO. 1999. Emerging insights into the genesis of epilepsy. Nature 399(suppl):A15-A22.
45. McNamara JO, Bonhaus DW, Shin C. 1993. The kindling model of epilepsy. In: Schwartzkroin PA, editor. Epilepsy: models, mechanisms, and concepts. Cambridge, UK: Cambridge University Press. p 27-47.
46. McNamara RK, Routtenberg A. 1995. NMDA receptor blockade kainate-induction of protein F1/GAP-43 mRNA in hippocampal granule cells and subsequent mossy fiber sprouting in rat. Brain Res Mol Brain Res 33:22-28.
47. Meier CL, Dudek FE. 1996. Spontaneous and stimulation-induced synchronized burst a afterdischarges in the isolated CA1 of kainate-treated rats. J Neurophysiol 76:2231-2239.
48. Morin F, Beaulieu C, Lacaille J-C. 1998. Selective loss of GABA neurons in area CA1 of the rat hippocampus after interventricular kainate. Epilepsy Res 32:363-369.
49. Nadler J, Perry B, Cotman C. 1980a. Selective reinnervation of hippocampal area CA1 and the fascia dentata after destruction of CA3-CA4 afferents. Brain Res 182:1-9.
50. Nadler JV, Perry BW, Gentry C, Cotman CW. 1980b. Loss and reacquisition of hippocampal synapses after selective destruction of CA3-CA4 afferents with kainic acid. Brain Res 191:387-403.
51. Naffah-Mazzacoratti MG, Arganaraz GA, Porcionatto MA, Scorza FA, Amado D, Silva R, Bellissimo MI, Nader HB, Cavalheiro, EA. 1999. Selective alterations of glycosaminoglycans synthesis and proteoglycan expression in rat cortex and hippocampus in pilocarpine-induced epilepsy. Brain Res Bull 50:229-239.
52. Naham WK, Noebels JL. 1998. Nonobligate role of early or sustained expression of immediate-early gene proteins c-fos, c-jun, and Zif/268 in hippocampal mossy fiber sprouting. J Neurosci 18:9245-9255.
53. O'Leary DDM, Yates PA, McLaughlin T. 1999. Molecular development of sensory maps: representing sights and smells in the brain. Cell 96: 255-269.
54. Pasterkamp RJ, Giger RJ, Verhaagen J. 1998. Regulation of semaphorin III/collapsin-1 gene expression during peripheral nerve regeneration. Exp Neurol 153:313-327.
55. Pasterkamp RJ, Giger RJ, Ruitenberg Holtmaat AJ, De Wit J, De Winter F, Verhaagen J. 1999. Expression of the gene encoding the chemorepellant Semaphorin III in induced in the fibroblast component of neural scar tissue formed following injuries of adult but not neonatal CNS. Mol Cell Neurosci 13:143-166.
56. Patel MN, McNamara JO. 1995. Selective enhancement of axonal branching of cultured dentate gyrus neurons by neurotrophic factors. Neuroscience 69:763-770.
57. Perez Y, Morin F, Beaulieu C, Lacaille J-C. 1996. Axonal sprouting of CA1 pyramidal cells in hyperexcitable hippocampal slices of kainate-treated rats. Eur J Neurosci 8:736-748.
58. Polleux F, Giger RJ, Ginty DD, Kolodkin AL, Ghosh A. 1998. Patterning of cortical efferent projections by semaphorin-neuropilin interactions. Science 282:1904-1906.
59. Puschel AW, Adams RH, Betz H. 1995. Murine semaphorin D/Collapsin is a member of a diverse gene family and creates domains inhibitory for axonal extension. Neuron 14:941-948.
60. Qiao X, Suri C, Knusel B, Noebels JL. 2001. Absence of hippocampal mossy fiber sprouting in transgenic mice overexpressing brain-derived neurotrophic factor. J Neurosci Res 64:268-276.
61. Racine RJ. 1972. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294.
62. Renzi MJ, Feiner L, Koppel AM, Raper JA. 1999. A dominant negative receptor for specific secreted semaphorins is generated by deleting an extracellular domain from neuropilin 1. J Neurosci 19:7870-7880.
63. Represa A, Pollard H, Moreau J, Ghilini G, Khrestchatisky M, Ben-Ari Y. 1993. Mossy fiber sprouting in epileptic rats is associated with a transient increased expression of alpha-tubulin. Neurosci Lett 156:149-152.
64. Routbort MJ, Bausch SB, McNamara JO. 1999. Seizures, cell death, and mossy fiber sprouting in kainic acid-treated organotypic hippocampal cultures. Neuroscience 94:755-765.
65. Roubort MJ, McNamara JO. 1996. Excitatory amino acids and use-dependent plasticity: epileptogenesis. In: Conti F, Hicks TP, editors. Excitatory amino acids and the cerebral cortex. Cambridge, MA: MIT Press. p 313-323.
66. Salin P, Tseng GF, Hoffman S, Parada I, Prince DA. 1995. Axonal sprouting in layer V pyramidal neurons of chronically injured cerebral cortex. J Neurosci 15:8234-8245.
67. Seeger MA, Beattie CE. 1999. Attraction versus repulsion: modular receptors make the difference in axon guidance. Cell 97:821-824.
68. Shatz C. 1990. Impulse activity and the patterning of connections during CNS development. Neuron 5:745-756.
69. Shirvan A, Ziv I, Fleminger G, Shina R, He Z, Brudo I, Melamed E, Barzilai A. 1999. Semaphorins as mediators of neuronal apoptosis. J Neurochem 73:961-971.
70. Skaliora I, Singer W, Betz H, Puschel AW. 1998. Differential patterns of semaphorin expression in the developing rat brain. Eur J Neurosci 10:1215-1229.
71. Sloviter RS. 1992. Possible functional consequences of synaptic reorganization in the dentate gyrus of kainate-treated rats. Neurosci Lett 137: 91-96.
72. Song H-J, Ming G-L, He Z, Lehmann M, McKerracher L, Tessier-Lavigne M, Poo M-M. 1998. Conversion of neuronal growth cones responses from repulsion to attraction by cyclic nucleotides. Science 281:1515-1518.
73. Sperry R. 1963. Chemoaffinity in the orderly growth of nerve fibers patterns and connections. Proc Natl Acad Sci USA 50:703-710.
74. Steup A, Lohrum M, Hamscho N, Savaskan NE, Ninnemann O, Nitsch R, Fujisawa H, Puschel AW, Skutella T. 2000. Semaphorin 3C and netrin-1 differentially affect axon growth in the hippocampal formation. Mol Cell Neurosci 15:141-155.
75. Steup A, Ninnemann O, Savaskan NE, Nitsch R, Puschel AW, Skutella T. 1999. Semaphorin D acts as a repulsive factor for entorhinal and hippocampal neurons. Eur J Neurosci 11: 729-734.
76. Sutula TP. 1990. Experimental models of temporal lobe epilepsy: New insights from the study of kindling and synaptic reorganization. Epilepsia 31 (suppl 3):S45-S54.
77. Sutula TP, Golarai G, Cavazos J. 1992. Assessing the functional significance of mossy fiber sprouting. Epilepsy Res 7(suppl):251-259.
78. Takahashi T, Nakamuri F, Jin Z, Kalb RG, Strittmatter SM. 1998. Semaphorins A and E act as antagonists of neuropilin 1 and agonists of neuropilin 2 receptors. Nature Neurosci 1:487-493.
79. Takahashi T, Fournier A, Nakamura F, Wang LH, Murakami Y, Kalb RG, Fujisawa H, Strittmatter SM. 1999. Plexin-Neuropilin 1 complexes form functional semaphorin 3A receptors. Cell 99:59-69.
80. Tanelian DL, Barry MA, Johnson SA, Le T, Smith GM. 1997. Semaphorin III can repulse and inhibit adult sensory afferents in vivo. Nat Med 3:1398-401.
81. Tamagnone L, Artigiani S, Chen H, He Z, Ming G-L, Song, H-J, Chedotal A, Winberg ML, Goodman CS, Poo M-M, Tessier-Lavigne M, Comoglio PM. 1999. Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99:71-80.
82. Taniguchi M, Yuasa S, Fujisawa H, Naruse I, Saga S, Mishina M, Yagi T. 1997. Disruption of semaphorin III/D gene causes severe abnormality in peripheral nerve projection. Neuron 19:519-530.
83. Tauck DL, Nadler JV. 1985. Evidence for functional mossy fiber sprouting in hippocampal formation of kainate-treated rats. J Neurosci 5:1066-1022.
84. Tessier-Lavigne M, Goodman CS. 1996. The molecular biology of axon guidance. Science 274:1123-1133.
85. Pyapali GK, Turner DA. 1994. Denervation-induced dendritic alterations in CA1 pyramidal cells following kainic acid hippocampal lesions in rats. Brain Res 652:279-290.
86. Tuttle R, O'Leary DDM. 1998. Neurotrophins rapidly modulate growth cone response to the axon guidance molecule, collapsin-1. Mol Cell Neurosci 11:1-8.
87. Varela-Echavarria A, Tucker A, Puschel AW, Guthrie S. 1997. Motor axons subpopulations differentially to the chemorepellants netrin 1 and semaphorin D. Neuron 18:193-207.
88. Wenzel HJ, Robbins CA, Tsai LH, Schwartzkroin PA. 2001. Abnormal morphological and functional organization of the hippocampus in p35 mutant model of cortical dysplasia associated with spontaneous seizures. J Neurosci 21:983-998.
89. Winberg ML, Mitchell KJ, Goodman CS. 1998. Genetic analysis of the mechanisms controlling target selection: complementary and combinatorial functions of netrins, semaphorins, and IgCAMs. Cell 93:581-591.
90. Wuarin JP, Dudek FE. 1996. Electrographic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slices from kainate-treated epileptic rats. J Neurosci 16:4438-4448.
91. Yamada T, Endo R, Gotoh M, Hirohashi S. 1997. Identification of semaphorin E as a non-MDR drug resistance gene of human cancers. Proc Natl Acad Sci USA 94:14713-14718.