Transient expression of GAP-43 within the hippocampus after global brain ischemia in rat

Cell and Tissue Research

Volumn 288, Issue 2, 1997, Pages 225-238

  Schmidt Kastner, R ^a,b   Bedard, A ^b   Hakim, A ^b  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Cerebral ischemia; GAP 43; Hippocampus; Immunohistochemistry; mRNA; Plasticity; Rat (Wistar)

Indexed keywords

MESSENGER RNA; NEUROMODULIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AXOPLASM FLOW; BRAIN ISCHEMIA; CONTROLLED STUDY; DENTATE GYRUS; FOREBRAIN; GRANULE CELL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SEIZURE;

ANIMALIA; RODENTIA;

EID: 0030945122     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s004410050808     Document Type: Article

References (87)

1. Aigner L, Arber S, Kapfhammer JP, Laux T, Schneider C, Botteri F, Brenner HR, 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. Amaral DG (1978) A Golgi study of cell types in the hilar region of the hippocampus in the rat. J Comp Neurol 182: 851-914
3. Bendotti C, Pende M, Sanumin R (1994) 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
4. Benowitz LI, Perrone-Bizzozero NI (1991) The expression of GAP-43 in relation to neuronal growth and plasticity: when, where, how, and why? Prog Brain Res 89: 69-87
5. Benowitz, LI, Apostolides PJ, Perrone-Bizzozero N, Finklestein SP, Zwiers H (1988) Anatomical distribution of the growth-associated protein GAP-43/B-50 in the adult rat brain. J Neurosci 8: 339-352
6. Benowitz LI, Rodriguez WR, Neve RL (1990) The pattern of GAP-43 immunostaining changes in the rat hippocampal formation during reactive synaptogenesis. Brain Res Mol Brain Res 8: 17-23
7. 45Ca accumulation in rat dentate hilus. J Cereb Blood Flow Metab 8: 713-719
8. Bliss TV, Collingridge CL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39
9. Brierley JB, Graham DI (1984) Hypoxia and vascular disorders of the central nervous system. In: Adams JH, Corsellis JAN, Duchen LW (eds) Greenfield's Neuropathology, 4th edn. Edward Arnold, London, pp 125-207
10. Burry BW, Perrone-Bizzozero NI (1993) Nerve growth factor stimulates GAP-43 expression in PC12 cell clones independently of neurite outgrowth. J Neurosci Res 36: 241-251
11. Coggins PJ, Zwiers H (1991) B-50 (GAP-43): biochemistry and functional neurochemistry of a neuron-specific phosphoprotein. J Neurochem 56: 1095-1106
12. Costello B, Meymandi A, Freeman JA (1990) Factors influencing GAP-43 gene expression in PC12 pheochromocytoma cells. J Neurosci 10: 1398-1406
13. Curtis R, Hardy R, Reynolds R, Spruce BA, Wilkin GP (1991) Down-regulation of GAP-43 during oligodendrocyte development and lack of expression by astrocytes in vivo: implications for macroglial differentiation. Eur J Neurosci 3: 876-886
14. Curtis R, Averill S, Priestley JV, Wilkin GP (1993a) The distribution of GAP-43 in normal rat spinal cord. J Neurocytol 22: 39-50
15. Curtis R, Green D, Lindsay RM, Wilkin GP (1993b) Up-regulation of GAP-43 and growth of axons in rat spinal cord after compression injury. J Neurocytol 22: 51-64
16. Dalby NO, Rondouin G, Lerner-Natoli M (1995) Increase in GAP-43 and GFAP immunoreactivity in the rat hippocampus subsequent to perforant path kindling. J Neurosci Res 41: 613-619
17. Davenport CJ, Brown WJ, Babb TL (1990) Sprouting of GABAergic and mossy fiber axons in dentate gyrus following intrahippocampal kainate in the rat. Exp Neurol 109: 180-190
18. De la Monte SM, Federoff HJ, Ng SC, Grabczyk E, Fishman MC (1989) GAP-43 gene expression during development: persistence in a distinctive set of neurons in the mature central nervous system. Brain Res Dev Brain Res 46: 161-168
19. Doster SK, Lozano AM, Aguayo AJ, Willard MB (1991) Expression of the growth-associated protein GAP-43 in adult rat retinal ganglion cells following axon injury. Neuron 6: 635-647
20. Elmer E, Kokaia M, Kokaia Z, Ferencz I, Lindvall O (1996) Delayed kindling development after rapidly recurring seizures: relation to mossy fiber sprouting and neurotrophin, GAP-43 and dynorphin gene expression. Brain Res 712: 19-34
21. Federoff HJ, Grabczyk E, Fishman MC (1988) Dual regulation of GAP-43 gene expression by nerve growth factor and glucocorticoids. J Biol Chem 263: 19290-19295
22. Figueiredo BC, Skup M, Bedard AM, Tetzlaff W, Cuello AC (1995) Differential expression of p140trk, p75NGFR and growth-associated phosphoprotein-43 genes in nucleus basalis magnocellularis, thalamus and adjacent cortex following neocortical infarction and nerve growth factor treatment. Neuroscience 68: 29-45
23. Freund TF, Magloczky Z (1993) Early degeneration of calretinin-containing neurons in the rat hippocampus after ischemia. Neuroscience 56: 581-596
24. Gall CM (1993) Seizure-induced changes in neurotrophin expression: implications for epilepsy. Exp Neurol 124: 150-166
25. Goto S, Yamada K, Inoue N, Nagahiro S, Ushio Y (1994) Increased expression of growth-associated protein GAP-43/B-50 following cerebral hemitransection or striatal ischemic injury in the substantia nigra of adult rats. Brain Res 647: 333-339
26. Holtzman DM, Lowenstein DH (1995) Selective inhibition of axon outgrowth by antibodies to NGF in a model of temporal lobe epilepsy. J Neurosci 15: 7062-7070
27. Houser CR, Miyashiro JE, Swartz BE, Walsh GO, Rich JR, Delgado-Escueta AV (1990) Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J Neurosci 10: 267-282
28. Jap Tjoen San ER, Schmidt-Michels M, Oestreicher AB, Gispen WH, Schotman P (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 Commun 187: 839-846
29. Johansen FF, Zimmer J, Diemer NH (1987) Early loss of somatostatin neurons in dentate hilus after cerebral ischemia in the rat precedes CA-1 pyramidal cell loss. Acta Neuropathol (Berl) 73: 110-114
30. Karns LR, Ng S-C, Freeman JA, Fishman MC (1987) Cloning of complementary DNA for GAP-43, a neuronal growth-related protein. Science 236: 597-600
31. Kohn DT, Tsai K-C, Cansino VV, Neve RL, Perrone-Bizzozero NI (1996) Role of highly conserved pyrimidine-rich sequences in the 3' untranslated region of GAP-43 mRNA in mRNA stability and RNA-protein interactions. Brain Res Mol Brain Res 36: 240-250
32. Kruger L, Bendotti C, Rivolta R, Samanin R (1992) GAP-43 mRNA localization in the rat hippocampus CA3 field. Brain Res Mol Brain Res 13: 267-272
33. Kruger L, Bendotti C, Rivolta R, Samanin R (1993) Distribution of GAP-43 mRNA in the adult rat brain. J Comp Neurol 333: 417-434
34. Lin LH, Bock S, Carpenter K, Rose M, Norden JJ (1992) Synthesis and transport of GAP-43 in entorhinal cortex neurons and perforant pathway during lesion-induced sprouting and reactive synaptogenesis. Brain Res Mol Brain Res 14: 147-153
35. Lindsay RM, Wiegand SJ, Altar CA, DiStefano PS (1994) Neurotrophic factors: from molecule to man. Trends Neurosci 17: 182-190
36. Lindvall O, Ernfors P, Bengzon J, Kokaia Z, Smith M-L, Siesjö BK, Persson H (1992) Differential regulation of mRNAs for nerve growth factor, brain derived neurotrophic factor, and neurotrophin 3 in the adult rat brain following cerebral ischemia and hypoglycemic coma. Proc Natl Acad Sci USA 89: 648-652
37. Lindvall O, Kokaia Z, Bengzon J, Elmer E, Kokaia M, (1994) Neurotrophins and brain insults. Trends Neurosci 17: 490-496
38. Masliah E, Fagan AM, Terry RD, DeTeresa R, Mallory M, Gage FH (1991) Reactive synaptogenesis assessed by synaptophysin immunoreactivity is associated with GAP-43 in the dentate gyrus of the adult rat. Exp Neurol 113: 131-142
39. Matsuyama T, Tsuchiyama M, Nakamura H, Mutsumoto M, Sugita M (1993) Hilar somatostatin neurons are more vulnerable to an ischemic insult than CA1 pyramidal neurons. J Cereb Blood Flow Metab 13: 229-234
40. Mattson MP, Cheng B, Smith-Swintosky VL (1993) Mechanisms of neurotrophic factor protection against calcium- and free radical-mediated excitotoxic injury: implications for treating neurodegenerative disorders. Exp Neurol 124: 89-95
41. Meberg PJ, Routtenberg A (1991) Selective expression of protein F1/(GAP-43) mRNA in pyramidal but not granule cells of the hippocampus. Neuroscience 45: 721-733
42. Meberg PJ, Barnes CA, McNaughton BL, Routtenberg A (1993a) Protein kinase C and F1/GAP-43 gene expression in hippocampus inversely related to synaptic enhancement lasting 3 days. Proc Natl Acad Sci USA 90: 12050-12054
43. Meberg PJ, Gall CM, Routtenberg A (1993b) Induction of F1/GAP-43 gene expression in hippocampal granule cells after seizures. Brain Res Mol Brain Res 17: 295-297
44. Meberg PJ, Jarrard LE, Routtenberg A (1996) Is the lack of protein F1/GAP-43 mRNA in granule cells target-dependent? Brain Res Mol Brain Res 17: 217-226
45. Mohiuddin L, Fernandez K, Tomlinson DR, Fernyhough P (1995) Nerve growth factor and neurotrophin-3 enhance neurite outgrowth and up-regulate the levels of messenger RNA for growth-associated protein GAP-43 and T alpha 1 alpha-tubulin in cultured adult rat sensory neurones. Neurosci Lett 185: 20-23
46. Mugnaini E, Oertel WH (1985) An atlas of the distribution of GABAergic neurons and terminals in the rat CNS as revealed by GAD immunohistochemistry. In: Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy, Vol 4: GABA and neuropeptides in the CNS, part I, Elsevier, Amsterdam, pp 430-608
47. Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116: 201-211
48. Ng SC, Monte SM de la, Conboy GL, Karns LR, Fishman MC (1988) Cloning of human GAP-43: growth association and ischemic resurgence. Neuron 1: 133-139
49. Nishizawa K (1994) NGF-induced stabilization of GAP-43 mRNA is mediated by both 3′ untranslated region and a segment encoding the carboxy-terminus peptide. Biochem Biophys Res Commun 200: 789-796
50. Nishizawa K, Okamoto H (1994) Mutation analysis of the role for the carboxy-terminus encoding region in NGF-induced stabilization of GAP-43 mRNA. Biochem Biophys Res Commun 205: 1380-1385
51. Oestreicher AB, Gispen WH (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
52. Pazos AJ, Orezzoli SL, McCabe PM, Dietrich WD, Green EJ (1995) Recovery of vibrissae-dependent behavioral responses following barrelfield damage is not dependent upon the remaining somatosensory cortical tissue. Brain Res 689: 224-232
53. Pulsinelli WA, Brierley JB (1979) A new model of bilateral hemispheric ischemia in the unanesthetized rat. Stroke 10: 267-272
54. Pulsinelli WA, Brierley JB, Plum F (1982) Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 11: 491-498
55. Rashid K, Van der Zee CE, Ross GM, Chapman CA, Stanisz J, Riopelle RJ, Racine RJ, Fahnestock M (1995) A nerve growth factor peptide retards seizure development and inhibits neuronal sprouting in a rat model of epilepsy. Proc Natl Acad Sci USA 92: 9495-9499
56. Represa A, Niquet J, Charriaut-Marlangue C, Ben-Ari Y (1993) Reactive astrocytes in the kainic acid-damaged hippocampus have the phenotypic features of type-2 astrocytes. J Neurocytol 22: 299-310
57. Scharfman HE, Schwartzkroin PA (1989) Protection of dentate hilar cells from prolonged stimulation by intracellular calcium chelation. Science 246: 257-260
58. Schauwecker PE, Cheng HW, Serquinia RM, Mori N, McNeill TH (1995) Lesion-induced sprouting of commissural/associational axons and induction of GAP-43 mRNA in hilar and CA3 pyramidal neurons in the hippocampus are diminished in aged rats. J Neurosci 15: 2462-2470
59. Schmidt-Kastner R, Freund TF (1991) Selective vulnerability of the hippocampus in brain ischemia. Neuroscience 40: 599-636
60. Schmidt-Kasiner R, Hakim A (1995) Glial cell line-derived neurotrophic factor (GDNF) and brain-derived neurotrophic factor (BDNF) mRNA expression in hippocampus after brain ischemia. Soc Neurosci Abstr 21: 228
61. Schmidt-Kastner R, Paschen W, Grosse Ophoff B, Hossmann K-A (1989) A modified four-vessel occlusion model for inducing incomplete forebrain ischemia in rat. Stroke 20: 938-946
62. Schmidt-Kastner R, Szymas J, Hossmann K-A (1990) Immunohistochemical study of glial reaction and serum-protein extravasation in relation to neuronal damage in rat hippocampus after ischemia. Neuroscience 38: 27-540
63. Schmidt-Kastner R, Meiler D, Bellander D-M, Strömberg I, Olson L, Ingvar M (1993) A one-step immunohistochemical method for detection of blood-brain barrier disturbances for immunoglobulins in lesioned rat brain with special reference to false-positive staining in immunohistochemistry. J Neurosci Meth 46: 121-132
64. Schmidt-Kastner R, Robertson GS, Hakim A (1995) Monoclonal antibody to NeuN as specific marker for neurons in immunohistochemical evaluation of global ischemic damage in rat. J Cereb Blood Flow Metab 15: S230
65. Schmidt-Kastner R, Humpel C, Wetmore C, Olson L (1996) Changes of BDNF-, trkB-, and NGF-mRNA and BDNF-like immunoreactivity in hippocampus and cortex after status epilepticus induced by pilocarpine in rats. Exp Brain Res 107: 331-347
66. Schreyer DJ, Skene JH (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
67. Skene JH (1989) Axonal growth-associated proteins. Annu Rev Neurosci 12: 127-156
68. Skene JHP, Virag I (1989) Posttranslational membrane attachment and dynamic fatty acylation of a neuronal growth cone protein. GAP-43. J Cell Biol 108: 613-624
69. Skene JH, Jacobson RD, Snipes GJ, McGuire CB, Norden JJ, Freeman JA (1986) A protein induced during nerve growth (GAP-43) is a major component of growth-cone membranes. Science 233: 783-786
70. Smith ML, Auer RN, Siesjö BK (1984) The density and distribution of ischemic brain injury in the rut following 2-10 min of forebrain ischemia. Acta Neuropathol (Berl) 64: 319-332
71. Strittmatter SM, Vartanian T, Fishman MC (1992) GAP-43 as a plasticity protein in neuronal form and repair. J Neurobiol 23: 507-520
72. Strittmatter SM, Fankhauser C, Huang PL, Mashimo H, Fishman MC (1995) Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43. Cell 80: 445-452
73. Stroemer RP, Kent TA, Hulsebosch CE (1995) Neocortical neural sprouting, synaptogenesis, and behavioral recovery after neocortical infarction in rats. Stroke 26: 2135-2144
74. Sutula T, Xiao-Xian H, Cavazos J, Scott G (1988) Synaptic reorganisation in the hippocampus induced by abnormal functional activity. Science 239: 1147-1150
75. Tagaya M, Matsuyama T, Nakumura H, Hata R, Shimizu S, Kiyama H, Matsumoto M, Sugita M (1995) Increased F1/GAP-43 mRNA accumulation in gerbil hippocampus after brain ischemia. J Cereb Blood Flow Metab 15: 1132-1136
76. Takami K, Kiyota Y, Iwane M, Miyamoto M, Tsukuda R, Igarashi K, Shino A, Wanaka A, Shiosaka S, Tohyama M (1993) Up-regulation of fibroblast growth factor-receptor messenger RNA expression in rat brain following transient forebrain ischemia. Exp Brain Res 97: 185-194
77. Tauck DL, Nadler JV (1985) Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci 5: 1016-1022
78. Tetzlaff W, Zwiers H, Lederis K, Cassar L, Bisby MA (1989) Axonal transport and localization of B-50/GAP-43-like immunoreactivity in regenerating sciatic and facial nerves of the rat. J Neurosci 9: 1303-1313
79. Tetzlaff W, Alexander SW, Miller FD, Bisby MA (1991) Response of facial and rubrospinal neurons to axotomy: changes in mRNA expression for cytoskeletal proteins and GAP-43. J Neurosci 11: 2528-2544
80. Tetzlaff W, Kobayashi NR, Giehl KM, Tsui BJ, Cassar SL, Bedard AM (1994) Response of rubrospinal and corticospinal neurons to injury and neurotrophins. Prog Brain Res 103: 271-286
81. Thilmann R, Xie Y, Kleihues P, Kiessling M (1986) Persistent inhibition of protein synthesis precedes delayed neuronal death in postischemic gerbil hippocampus. Acta Neuropathol (Berl) 71: 88-93
82. Thoenen H (1995) Neurotrophins and neuronal plasticity. Science 270: 593-598
83. Van Hooff CO, Holthuis JC, Oestreicher AB, Boonstra J, De Graan PN, Gispen WH (1989) Nerve growth factor-induced changes in the intracellular localization of the protein kinase C substrate B-50 in pheochromocytoma PC12 cells. J Cell Biol 108: 1115-1125
84. Vaudano E, Campbell G, Anderson PN, Davies AP, Woolhead C, Sehreyer DJ, Lieberman AR (1995) The effects of a lesion or a peripheral nerve graft on GAP-43 upregulution in the adult rat brain: an in situ hybridization and immunocytochemical study. J Neurosci 15: 3594-3611
85. Woolf CJ, Reynolds ML, Molander C, O'Brien C, Lindsay RM, Benowitz LI (1990) The growth-associated protein GAP-43 appears in dorsal root ganglion cells and in the dorsal horn of the rut spinal cord following peripheral nerve injury. Neuroscience 34: 465-478
86. Yankner BA, Benowitz LI, Villa-Komaroff L, Neve RL (1990). Transfection of PC12 cells with the human GAP-43 gene: effects on neurite outgrowth and regeneration. Brain Res Mol Bruin Res 7: 39-44
87. Yao GL, Kiyama H, Tohyama M (1993) Distribution of GAP-43 (B50/F1) mRNA in the adult rat brain by in situ hybridization using an alkaline phosphatase labeled probe. Brain Res Mol Brain Res 18: 1-16