Early induction of mRNA for calbindin-D(28k) and BDNF but not NT-3 in rat hippocampus after kainic acid treatment

Molecular Brain Research

Volumn 47, Issue 1-2, 1997, Pages 183-194

  Lee, S ^a   Williamson, J ^b   Lothman, E W ^b   Szele, F G ^c   Chesselet, M F ^a,c   Von Hagen, S ^a   Sapolsky, R M ^d   Mattson, M P ^e   Christakos, S ^a,f  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d STANFORD UNIVERSITY   (United States)

^e UNIVERSITY OF KENTUCKY   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN PROTEIN; CALBINDIN; CALCIUM BINDING PROTEIN; KAINIC ACID; MESSENGER RNA; NEUROTROPHIN 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; DENTATE GYRUS; EARLY RESPONSE GENE; EPILEPTIC STATE; GENE EXPRESSION REGULATION; GENE INDUCTION; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; NERVE CELL; NONHUMAN; NORTHERN BLOTTING; ONCOGENE C FOS; PRIORITY JOURNAL; RAT; SEIZURE;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; HIPPOCAMPUS; IN SITU HYBRIDIZATION; KAINIC ACID; MALE; NERVE GROWTH FACTORS; NEUROTROPHIN 3; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; TIME FACTORS;

EID: 0031009080     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-328X(97)00043-0     Document Type: Article

References (78)

1. Baimbridge, K.G., Mody, I. and Miller, J.J. Reduction of rat hippocampal calcium binding protein following commissural, amygdala, septal, perforant path and olfactory bulb kindling, Epilepsia, 26 (1985) 460-465.
2. Ballarin, M., Ernfors, P., Lindefors, N. and Persson, H., Hippocampal damage and kainic acid injection induce a rapid increase in mRNA for BDNF and NGF in the rat brain, Exp. Neurol., 114 (1991) 35-43.
3. Ben-Ari, Y., Limbic seizures and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy, Neuroscience, 14 (1985) 375-403.
4. Bengzon, J., Kokaia, Z., Ernfors, P., Kokaia, M., Leanza, G., Nilsson, O.G., Persson, H. and Lindvall, O., Regulation of neurotrophin and trkA, trkB and trkC tyrosine kinase receptor messenger RNA expression in kindling, Neuroscience, 53 (1993) 433-446.
5. 28k immunostaining, following developmental hypoxic-ischemic injury, Neuroscience, 56 (1993) 305-315.
6. Celio, M.R., Calbindin and parvalbumin in the rat nervous system, Neuroscience, 35 (1990) 375-475.
7. Changelian, P.S., Feng, P., King, T.C. and Milbrandt, J., Structure of the NGFI-A gene and detection of upstream sequences responsible for its transcriptional induction by nerve growth factor, Proc. Natl. Acad. Sci. USA, 86 (1989), 377-381.
8. 28k and parvalbumin in rat sensory neurons, J. Physiol., 472 (1993) 341-357.
9. Cheng, B., Christakos, S. and Mattson, M., Tumor necrosis factors protect against metabolic excitotoxic insults and promote maintenance of calcium homeostasis, Neuron, 12 (1994) 139-153.
10. Cheng, B. and Mattson, M.P., NGF and bFGF protect rat hippocampal and human cortical neurons against hypoglycemic damage by stabilizing calcium homestasis, Neuron, 7 (1991) 1031-1041.
11. Cheng, B. and Mattson, M.P., NT-3 and BDNF protect against metabolic/excitotoxic insults, Brain Res., 640 (1994) 56-67.
12. Chesselet, M.F., Weiss, L., Wuenschell, C., Tobin, A.J. and Affolter, H.-U., Comparative distribution of mRNAs for glutamic acid decarboxylase, tyrosine hydroxylase, and tachykinins in basal ganglia: an in situ hybridization study in the rodent brain, J. Comp. Neurol., 262 (1987) 125-140.
13. Chomczynski, P. and Sacchi, N., Single-step method of RNA isolation by acid guanidinium thiocyanate phenol-chloroform extraction, Anal. Biochem., 162 (1987) 156-159.
14. Christakos, S., Vitamin D-dependent calcium binding proteins: chemistry distribution, functional considerations and molecular biology: update 1995, Endocr. Rev. Monogr., 4 (1995) 108-110.
15. Christakos, S., Gabrielides, C. and Rhoten, W.B., Vitamin D-dependent calcium binding proteins: chemistry, distribution, functional considerations and molecular biology, Endocr. Rev., 10 (1989) 3-16.
16. 28k: purification, quantitation, immunocytochemical localization and comparative aspects, Methods Enzymol., 139 (1987) 543-551.
17. Cleveland, D.W., Lopata, M.A., MacDonald, R.J., Cowan, N.J., Rutter, W.J. and Kirschner, M.W., Number and evolutionary conservation of α and β tubulin and cytoplasmic α and γ actin genes using specific cDNA probes, Cell, 20 (1980) 95-105.
18. Cole, A.J., Saffen, D.W., Baraban, J.M. and Worley, P.F. Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation, Nature, 340 (1989) 474-476
19. Collazo, D., Takahashi, H. and McKay, R.D.G., Cellular targets and trophic functions of neurotrophin-3 in the developing hippocampus, Neuron, 9 (1992) 643-656.
20. Cornish, S.M. and Wheal, H.V., Long term loss of paired pulse inhibition in the kainic acid lesioned hippocampus of the rat, Neuroscience, 28 (1989) 563-571.
21. Curran, T. and Franga, B.R., Fos and Jun: the AP-1 connection, Cell, 55 (1988) 395-397.
22. Curran, T., Gordon, M.B., Rubino, K.L. and Sambucetii, L.C., Isolation and charcterization of the c-fos (rat) cDNA and analysis of post-translation modifications in vitro, Oncogene, 2 (1987) 74-87.
23. Dugich-Djordjevic, M.M., Tocco, G., Willoughby, D.A., Najm, I., Pasinetti, G., Thompson, R.F., Baudry, M., Lapchak, P.A. and Hefti, F., BDNF mRNA expression in the developing rat brain following kainic acid induced seizure activity, Neuron, 8 (1992) 1127-1138.
24. Dugich-Djordjevic, M.M., Tocco, G., Lapchak, P.A., Pasinetti, G.M., Najm, I., Baudry, M. and Hefti, F., Regionally specific and rapid increases in brain-derived neurotrophic factor messenger RNA in the adult rat brain following seizures induced by systemic administration of kainic acid, Neuroscience, 47 (1992) 303-315.
25. Elliott, E., Mattson, M.P., Vanderklish, P., Lynch, G., Chang, I. and Sapolsky, R.M., Corticosterone exacerbates kainate-induced alterations in hippocampal tau immunoreactivity and spectrin proteolysis in vivo, J. Neurochem., 61 (1993) 57-67.
26. Ernfors, P., Bengzon, J., Kokaia, Z., Persson, H. and Lindvall, O., Increased levels of messenger RNAs for neurotrophic factors in the brain during kindling epileptogenesis, Neuron, 7 (1991) 165-176.
27. Feinberg, A.P. and Vogelstein, B.A., Technique for radiolabeling DNA restriction endonuclease fragments to high specific activity, Anal. Biochem., 137 (1984) 266-267.
28. Gall, C.M., Seizure induced changes in neurotrophin expression: implications for epilepsy, Exp. Neurol., 124 (1990) 150-166.
29. Ghosh, A. and Greenberg, M.E., Calcium signaling in neurons: molecular mechanisms and cellular consequences, Science, 268 (1995) 239-247.
30. 3 and butyrate inducible responses, Proc. Natl. Acad. Sci USA, 90 (1993) 2984-2988.
31. 28k immunoractivity and selective vulnerability to ischemia in the dentate gyrus of the developing rat brain, Brain Res., 606 (1993) 309-314.
32. 3 and dietary alteration, Mol. Endocr., 2 (1988) 928-936.
33. Humpel, C., Wetmore, C. and Olson, L., Regulation of brain-derived neurotrophic factor messenger RNA and protein at the cellular level in pentylenetetrazol-induced epileptic seizures, Neuroscience, 53 (1993) 909-918.
34. 28k mRNA and protein levels in rat hippocampus, J. Biol. Chem., 265 (1990) 10177-10180.
35. 28k) gene expression in aging and neurodegenerative diseases, Proc. Natl. Acad. Sci. USA, 87 (1990) 4078-4082.
36. Ip, N.Y., Li, Y., Yancopoulos, G.D. and Lindsay, R.M., Cultured hippocampal neurons show responses to BDNF, NT-3 and NT-4 but not NGF, J. Neurosci., 13 (1993) 3394-3405.
37. Ip, N.Y. and Yancopoulos, G.D., Receptors and signaling pathways of ciliary neurotrophic factor and neurotrophins, Semin. Neurosci., 5 (1993) 249-257.
38. Isackson, P.J., Huntsman, M.M., Murray, K.D. and Gall, C.M., BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: temporal patterns of induction distinct from NGF, Neuron, 6 (1991) 937-948.
39. 28k immunoreactivity in the rat hippocampus following adrenalectomy and corticosterone treatment, Brain Res., 696 (1995) 89-96.
40. Lauterborn, J.C., Isackson, P.J. and Gall, C.M., Seizure induced increases in NGF mRNA exhibit different time courses across forebrain regions and are biphasic in hippocampus, Exp. Neurol., 125 (1994) 22-40.
41. Lindsay, R.M., Wiegand, S.J., Altar, C.A. and DiStefano, P.S., Neurotrophic factors: from molecule to man, Trends Neurosci., 17, (1994) 182-190.
42. Lindvall, O., Ernfors, P., Bengzon, J., Kokaia, Z., Smith, M.L., Siesjo, B.K. and Persson, H., Differential regulation of mRNAs for nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 in the adult rat brain following cerebral ischemia and hypoglycemiv coma, Proc. Natl. Acad. Sci. USA, 89 (1992) 648-652.
43. Lindvall, O., Kokaia, Z., Bengzon, J., Elmer, E. and Kokaia, M., Neurotrophins and brain insults, Trends Neurosci., 17 (1994) 490-496.
44. Lothman, E.W., Bertram, E.H., Kapur, J. and Stringer, J.L., Recurrent spontaneous hippocampal seizures in the rat as a chronic sequela to limbic status epilepticus, Epilepsy Res., 6 (1990) 110-118.
45. 28k, the glucose regulated proteins, or the 72 kDa heat-shock protein in three models of acute CNS injury, Mol. Brain Res., 22 (1994) 299-308.
46. 28k in the rat hippocampus following focal stimulation of the perforant path, Neuron, 6 (1991) 627-622.
47. Lowenstein, D.H., Seren, M.S. and Longo, F.M., Prolonged increases in neurotrophic activity associated with kainate-induced hippocampal synaptic organization, Neuroscience, 56 (1993) 597-604.
48. Lu, B., Yokoyama, M., Dreyfus, C.F. and Black, I.B., Depolarizing stimuli regulate nerve growth factor gene expression in cultured hippocampal neurons, Proc. Natl Acad. Sci. USA, 88 (1991) 6289-6292.
49. Magloczky, Z. and Freund, T.F., Selective neuronal death in the contralateral hippocampus following unilateral kainate injections into the CA3 subfield, Neuroscience, 56 (1993) 317-336.
50. Maisonpierre, P.C., Belluscio, L., Friedman, B., Alderson, R.F., Weigand, S.J., Furth, M.E., Lindsay, R.M. and Yancopoulos, G.D., NT-3, BDNF and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression, Neuron, 5 (1990) 501-509.
51. Maisonpierre, P.C., LeBeau, M.M., Espinosa, R., Ip, N.Y., Belluscio, L., de la Monte, S.M., Squinto, S., Furth, M.E. and Yancopoulos, G.D., Human and rat brain derived neurotrophic factor and neurotrophin-3: gene structure, distribution and chromosomal localization, Genomics, 10 (1991) 558-568.
52. 28k in astrocytes: evidence for a cytoprotective response, J. Neurosci. Res., 42 (1995) 357-370.
53. 28k in cultured hippocampal neurons, Neuron, 6 (1991) 41-51.
54. Milbrandt, J., Nerve growth factor induces a gene homologous to the glucocorticoid receptor gene, Neuron, 1 (1988) 183-188.
55. Minami, M., Kuraishi, Y. and Satoh, M., Effects of kainic acid on messenger RNA levels of IL-IB, IL-6, TNFα and LIF in the rat brain, Biochem. Biophys. Res. Commun., 176 (1991) 593-598.
56. Nadler, J.V., Kainic acid as a tool for the study of temporal lobe epilepsy, Life Sci., 29 (1981) 2031-2042.
57. 28k, J. Neurosci. Res., 42 (1995) 371-376.
58. Olney, J.W., Rhee, V. and Ho, O.L., Kainic acid: a powerful neurotoxic analogue of glutamate, Brain Res., 77 (1974) 507-512.
59. Pellegrino, L.J., Pellegrino, A.S. and Cushman, A.J., A Stereotaxic Atlas of the Rat Brain, Plenum, New York, NY, 1979, 122 pp.
60. Persson, H., Neurotrophin production in the brain, Semin. Neurosci., 5 (1993) 227-237.
61. Popovici, T., Represa, A., Crepel, V., Barbin, G., Beaudoin, M. and Ben-Ari, Y., Effects of kainic acid-induced sizures and ishemia on c-fos like proteins in rat brain, Brain Res., 536 (1990) 183-194.
62. 28k and ischemic damage of pyramidal cells in rat hippocampus, J. Neurosci. Res., 31 (1992) 89-95.
63. Rocamora, N., Palacios, J.M. and Mengod, G., Limbic seizures induce a differential regulation of the expression of nerve growth factor, brain-derived neurotrophic factor and neurotrphin-3 in rat hippocampus, Mol. Brain Res., 13 (1992) 27-33.
64. Saffen, D.W., Cole, A.J., Worley, P.F., Christy, B.A., Ryder, K.A. and Baraban, J.M., Convulsant-induced increase in transcription factor mRNAs in rat brain, Proc. Natl. Acad. Sci. USA, 85 (1988) 7785-7799.
65. Schwob, J.E., Fuller, T., Price, J.L. and Olney, J.W., Widespread pattterns of neuronal damage following systemic or intracerebral injections of kainic acid: a histolgical study, Neuroscience, 5 (1980) 991-1014.
66. Sheng, M., McFadden, G. and Greenberg, M.E., Membrane depolorization and calcium induce c-fos transcription via phosphorylation of transcription factor CREB, Neuron, 4 (1990) 571-582.
67. Simonato, M., Hosford, D.A., Labiner, D.M., Shin, C., Mansback, H.H. and McNamara, J.O., Differential expression of immediate early genes in the hippocampus in the kindling model of epilepsy, Mol. Brain Res., 11 (1991) 115-124.
68. 28k) and glutamate decarboxylase gene expression after kindling induced seizures, Mol. Brain Res., 9 (1991) 179-190.
69. Sonnenberg, J., Pansini, A.R. and Christakos, S., Vitamin D-dependent rat renal calcium-binding protein: development of a radioimmunoassay, tissue distribution and immunologic identification, Endocrinology, 115 (1984) 640-648.
70. Sonnenberg, J.L., Rauscher, F.J., Morgan, J.I. and Curran, T., Regulation of proenkephalin by fos and jun, Science, 246 (1989) 1622-1625.
71. Sukhatme, V.P., Cao, X., Chang, L.C., Tsai-Morris, C.-H., Stamenkovich, D., Ferreira, P.C., Cohen, D.R., Edwards, S.A., Shows, T.B., Curran, T., LeBeau, M.M. and Adamson, E.D., A zinc finger-encoding gene coregulated with c-fos during growth and differentiation, and after cellular depolorizatin, Cell, 53 (1988) 37-43.
72. Takeda, A., Onodera, H., Sugimoto, A., Kogure, K., Obinata, M. and Shibahara S., Coordinated expression of messenger RNAs for nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 in rat hippocampus following transient forebrain ischemia, Neuroscience, 55 (1993) 23-31.
73. 28k gene expression, J. Biol. Chem., 263 (1988) 9776-9784.
74. 28k, Mol. Endo., 9 (1995) 1510-1521.
75. Watson, M.A. and Mibrandt, J., The NGFI-B gene, a transcriptionally inducible member of the steroid receptor gene super family: genomic structure and expression in rat brain after seizure induction, Mol. Cell Biol., 9 (1989) 4213-4219.
76. 28k RNAs in rodent brain and kidney, DNA, 7 (1988) 585-593.
77. Zafra, F., Castren, E., Thoenen, H. and Lindholm, D. Interplay between glutamate and γ-aminobutyric acid transmitter systems in the physiological regulation of brain-derived neurotrophic factor and nerve growth factor synthesis in hippocampal neurons, Proc. Natl. Acad. Sci. USA, 83 (1991) 10037-10041.
78. Zafra, F., Hengerer, B., Leibrock, J., Thoenen, H. and Lindholm, D., Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors, EMBO J., 9 (1990) 3545-3550.