Hippocampal neurotrophin and trk receptor mRNA levels are altered by local administration of nicotine, carbachol and pilocarpine

Molecular Brain Research

Volumn 67, Issue 1, 1999, Pages 124-136

  French, Sarah J ^a,b,c   Humby, Trevor ^b   Horner, Catherine H ^b   Sofroniew, Michael V ^b   Rattray, Marcus ^a  

^a NEUROSCIENCE RESEARCH CENTRE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Acetylcholine; Alzheimer's disease; Brain derived neurotrophic factor; Nerve growth factor; Neurotrophin 3; p75(NTR); Septum; TrkA

Indexed keywords

AMINO ACID; AMPA RECEPTOR ANTAGONIST; BRAIN DERIVED NEUROTROPHIC FACTOR; CARBACHOL; CHOLINERGIC RECEPTOR STIMULATING AGENT; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NERVE GROWTH FACTOR; NEUROTROPHIN; NEUROTROPHIN RECEPTOR; NICOTINE; PILOCARPINE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MALE; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT;

ACETYLCHOLINE; ANIMALS; BEHAVIOR, ANIMAL; BRAIN CHEMISTRY; BRAIN-DERIVED NEUROTROPHIC FACTOR; CARBACHOL; CELL DEATH; CHOLINERGIC AGONISTS; CHOLINERGIC FIBERS; EPILEPSY; GENE EXPRESSION; GLUTAMIC ACID; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MALE; MUSCARINIC AGONISTS; NERVE GROWTH FACTORS; NEUROPROTECTIVE AGENTS; NEUROTROPHIN 3; NICOTINE; NICOTINIC AGONISTS; PILOCARPINE; PROTO-ONCOGENE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, CILIARY NEUROTROPHIC FACTOR; RECEPTOR, NERVE GROWTH FACTOR; RECEPTOR, TRKA; RECEPTOR, TRKC; RECEPTORS, NERVE GROWTH FACTOR; RNA, MESSENGER; SEPTAL NUCLEI; SYNAPTIC TRANSMISSION;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS;

EID: 0033528692     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-328X(99)00048-0     Document Type: Article

References (77)

1. M.T. Akbar, M. Rattray, R.J. Williams, N.W.S. Chong, B.S. Meldrum, Down-regulation of GABA and glutamate transporter mRNAs in the severe-seizure genetically epilepsy-prone rat (GEPR-9), Neuroscience 85 (1998) 1235-1251.
2. M. Alkodon, E.F.R. Pereira, C.T.F. Barbosa, E.X. Albuquerque, Neuronal nicotinic acetylcholine receptor activation modulates gamma-aminobutyric acid release from CA1 neurons of rat hippocampal slices, J. Pharmacol. Exp. Ther. 283 (1997) 1396-1411.
3. M.P. Armanini, S.B. McMahon, J. Sutherland, D.L. Shelton, H.S. Phillips, Truncated and catalytic isoforms of trkB are coexpressed in neurons of rat and mouse CNS, Eur. J. Neurosci. 7 (1995) 1403-1409.
4. G.T. Baxter, M.J. Radeke, R.C. Kuo, V. Makrides, B. Hinkle, R. Hoang, A. MedinaSelby, D. Coit, P. Valenzuela, S.C. Feinstein, Signal transduction mediated by the truncated trkB receptor isoforms, trkB.T1 and trkB.T2, J. Neurosci. 17 (1997) 2683-2690.
5. M.P. Berzaghi, J.D. Cooper, E. Castrén, F. Zafra, M.V. Sofroniew, H. Thoenen, D. Lindholm, Cholinergic regulation of brain-derived neurotrophic factor (BDNF) and nerve growth factor (NGF) but not neurotrophin-3 (NT-3) mRNA levels in the developing rat hippocampus, J. Neurosci. 13 (1993) 3818-3826.
6. P.C. Bickford, K.D. Wear, Restoration of sensory gating of auditory evoked response by nicotine in fimbria-fornix lesioned rats, Brain Res. 705 (1995) 235-240.
7. M.A. Burke, W.C. Mobley, J.Y. Cho, S.J. Wiegand, R.M. Lindsay, E.J. Mufson, J.H. Kordower, Loss of developing cholinergic basal forebrain neurons following excitotoxic lesions of the hippocampusrescue by neurotrophins, Exp. Neurol. 130 (1994) 178-195.
8. S.B. Caine, M.A. Geyer, N.R. Swerdlow, Hippocampal modulation of acoustic startle and prepulse inhibition in the rat, Pharmacol. Biochem. Behav. 43 (1992) 1201-1208.
9. E. Castren, M.P. Berzaghi, D. Lindholm, H. Thoenen, Differential effects of MK-801 on brain-derived neurotrophic factor mRNA levels in different regions of the rat brain, Exp. Neurol. 122 (1993) 244-252.
10. A. Cellerino, Expression of messenger RNA coding for the nerve growth factor receptor trkA in the hippocampus of the adult rat, Neuroscience 70 (1996) 613-616.
11. K.S. Chen, M.C. Nishimura, M.P. Armanini, C. Crowley, S.D. Spencer, H.D. Phillips, Disruption of a single allele of the nerve growth factor gene results in atrophy of basal forebrain cholinergic neurons and memory deficits, J. Neurosci. 17 (1997) 7288-7296.
12. M. Didier, G. Bix, S.A. Berman, S. Bursztajn, Expression of the alpha 4 neuronal nicotinic acetylcholine receptor subunit in the developing mouse hippocampus, Int. J. Dev. Neurosci. 13 (1995) 703-713.
13. P. Ernfors, C. Wetmore, H. Persson, Identification of cells in rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family, Neuron 5 (1990) 511-526.
14. B.J. Everitt, T.W. Robbins, Central cholinergic systems and cognition, Annu. Rev. Psychol. 48 (1997) 649-684.
15. C.P. Fenster, M.F. Rains, B. Noerager, M.W. Quick, R.A.J. Lester, Influence of subunit composition on desensitization of neuronal acetylcholine receptors at low concentrations of nicotine, J. Neurosci. 17 (1997) 5747-5759.
16. I. Ferencz, M. Kokaia, M. Keep, E. Elmer, M. Metsis, Z. Kokaia, O. Lindvall, Effects of cholinergic denervation on seizure development and neurotrophin messenger RNA regulation in rapid hippocampal kindling, Neuroscience 80 (1997) 389-399.
17. S.E. File, L.E. Gonzalez, N. Andrews, Endogenous acetylcholine in the dorsal hippocampus reduces anxiety through actions on nicotinic and muscarinic1 receptors, Behav. Neurosci. 112 (1998) 352-359.
18. E. Förster, T. Naumann, T. Deller, A. Straube, R. Nitsch, M. Frotscher, Cholinergic sprouting in the rat fascia dentata after entorhinal lesion is not linked to early changes in neurotrophin messenger RNA production, Neuroscience 80 (1997) 731-739.
19. C.J. Frazier, Y.D. Rollins, C.R. Breese, S. Leonard, R. Freedman, T.V. Dunwiddie, Acetylcholine activates an α-bungarotoxin-sensitive nicotinic current in rat hippocampal interneurons, but not pyramidal cells, J. Neurosci. 18 (1998) 1187-1195.
20. R. Freedman, C. Wetmore, I. Stromberg, S. Leonard, L. Olson, Alpha-bungarotoxin binding to hippocampal interneurons: immunocytochemical characterization and effects on growth factor expression, J. Neurosci. 13 (1993) 965-1975.
21. F.G. Gage, K.S. Chen, G. Buzsaki, D. Armstrong, Experimental approaches to age-related cognitive impairments, Neurobiol. Aging 9 (1988) 645-655.
22. G. Golarai, J.E. Cavazos, T.P. Sutula, Activation of the dentate gyrus by pentylenetetrazol evoked seizures induces mossy fibre synaptic re-organisation, Brain Res. 593 (1992) 257-264.
23. R. Gray, A.S. Rajan, K.A. Radcliffe, M. Yakehiro, J.A. Dani, Hippocampal synaptic transmission enhanced by low concentrations of nicotine, Nature 383 (1996) 713-716.
24. D.A. Gurley, T.H. Lanthorn, Nicotinic agonists competitively antagonize serotonin at mouse 5-HT3 receptors expressed in Xenopus oocytes, Neurosci. Lett. 247 (1998) 107-110.
25. B.J. Gwag, F. Sessler, K. Kimmerer, J.E. Springer, Neurotrophic factor mRNA expression in the dentate gyrus is increased following angular bundle transection, Brain Res. 647 (1994) 23-29.
26. C.P. Heisenberg, J.D. Cooper, J. Berke, M.V. Sofroniew, NMDA potentiates NGF-induced sprouting of septal cholinergic fibres, NeuroReport 12 (1994) 413-416.
27. R. Hellweg, C. Humpel, A. Lowe, H. Hortnagl, Moderate lesion of rat cholinergic septohippocampal pathway increases hippocampal nerve growth factor synthesis: evidence for long-term compensatory changes?, Mol. Brain Res. 45 (1997) 177-181.
28. G.A. Higgins, S. Koh, K.S. Chen, F.H. Gage, NGF induction of NGF receptor gene expression and cholinergic neuronal hypertrophy within the basal forebrain of the adult rat, Neuron 3 (1989) 247-256.
29. H.J. Kang, E.M. Schuman, Long-lasting neurotrophin induced enhancement of synaptic transmission in the adult hippocampus, Science 267 (1995) 1658-1662.
30. M. Knipper, M.D. Berzaghi, A. Blochl, H. Breer, H. Thoenen, D. Lindholm, Positive feedback between acetylcholine and the neurotrophins nerve growth factor and brain derived neurotrophic factor in the rat hippocampus, Eur. J. Neurosci. 6 (1994) 668-671.
31. M. Kokaia, I. Ferencz, G. Leanza, E. Elmer, M. Metsis, Z. Kokaia, R.G. Wiley, O. Lindvall, Immunolesioning of the basal forebrain cholinergic neurons facilitates hippocampal kindling and perturbs neurotrophin messenger RNA regulation, Neuroscience 70 (1996) 313-327.
32. V.E. Koliatsos, D.L. Price, G.K. Gouras, M.H. Cayouette, L.E. Burton, J.W. Winslow, Highly selective effects of nerve growth factor, brain-derived neurotrophic factor, and neurotrophin-3 on intact and injured basal forebrain magnocellular neurons, J. Comp. Neurol. 343 (1994) 247-262.
33. P.A. Lapchak, D.J. Jenden, F. Hefti, Pharmacological stimulation reveals recombinant human nerve growth factor-induced increases of in vivo hippocampal cholinergic function measured in rats with partial fimbria transections, Neuroscience 50 (1992) 847-856.
34. G. Leanza, J. Muir, O.G. Nilsson, R.G. Wiley, S.B. Dunnett, A. Bjorklund, Selective immunolesioning of the basal forebrain cholinergic system disrupts short-term memory in rats, Eur. J. Neurosci. 8 (1996) 1535-1544.
35. E.S. Levine, C.F. Dreyfus, I.B. Black, M.R. Plummer, Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors, Proc. Natl. Acad. Sci. USA 92 (1995) 8074-8077.
36. N. Lindefors, P. Ernfors, T. Falkenberg, H. Persson, Septal cholinergic afferents regulate expression of brain-derived neurotrophic factor and beta nerve growth factor messenger RNA in rat hippocampus, Exp. Brain Res. 88 (1992) 78-90.
37. R. Maggio, M. Riva, F. Vaglini, F. Fornai, G. Racagni, G.U. Corsini, Striatal increase of neurotrophic factors as a mechanism of nicotine protection in experimental parkinsonism, J. Neural Transm. 104(1997) 1113-1123.
38. S.O. Meakin, U. Suter, C.C. Drinkwater, A.A. Welcher, E.M. Shooter, The rat trk protooncogene product exhibits properties characteristic of the slow nerve growth factor receptor, Proc. Natl. Acad. Sci. USA 89 (1992) 2374-2378.
39. J.P. Merlio, P. Ernfors, M. Jaber, H. Persson, Molecular cloning of rat trkC and distribution of cells expressing messenger RNAs for members of the trk family in the rat central nervous system, Neuroscience 51 (1992) 513-532.
40. D.S. Middlemas, R.A. Lindberg, T. Hunter, TrkB, a neural receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors, Mol. Cell. Biol. 11 (1991) 143-153.
41. N.S. Mingo, G. Cottrell, L. Zhang, M.C. Wallace, W.M. Burnham, J.H. Eubanks, Kainic acid-induced generalized seizures alter the regional hippocampal expression of the rat ml and m3 muscarinic acetylcholine receptor genes, Epilepsy Res. 29 (1997) 71-79.
42. J.K. Morse, S.J. Wiegand, K. Anderson, Y.M. You, N. Cai, J. Carnahan, J. Miller, P.S. DiStefano, C.A. Altar, R.M. Lindsay, R.F. Alderson, Brain-derived neurotrophic factor (BDNF) prevents the degeneration of medial septal cholinergic neurons following fimbria transection, J. Neurosci. 13 (1993) 4146-4156.
43. G. Mudó, X.H. Jiang, T. Timmusk, M. Bindoni, N. Belluardo, Change in neurotrophins and their receptor mRNAs in the rat forebrain after status epilepticus induced by pilocarpine, Epilepsia 37 (1996) 198-207.
44. M. Pascual, N. Rocamora, L. Acsady, T.F. Freund, E. Soriano, Expression of nerve growth factor and neurotrophin-3 mRNAs in hippocampal interneurons: morphological characterization, levels of expression and colocalization of nerve growth factor and neurotrophin-3, J. Comp. Neurol. 395 (1998) 73-90.
45. G. Paxinos, C. Watson, The Rat Brain in Stereotaxic Coordinates, 2nd edn., Academic Press, London, 1986.
46. M.A. Pelleymounter, M.J. Cullen, M.B. Baker, M. Gollub, C. Wellman, The effects of intrahippocampal BDNF and NGF on spatial learning in aged Long-Evans rats, Mol. Chem. Neuropathol. 29 (1996) 211-226.
47. H.S. Phillips, J.M. Hains, G.R. Laramee, A. Rosenthal, J.W. Winslow, Widespread expression of BDNF but not NT3 by target areas of basal forebrain cholinergic neurons, Science 250 (1990) 290-294.
48. M.J. Radeke, T.P. Misko, C. Hsu, L.A. Herzenberg, E.M. Shooter, Gene transfer and molecular cloning of the rat nerve growth factor receptor, Nature 325 (1987) 593-597.
49. M. Rattray, G.J. Michael, In situ hybridisation using oligonucleotide probes, in: D. Wilkinson (Ed.), In Situ Hybridisation: A Practical Approach, 2nd edn., Oxford Univ. Press, Oxford, 1998, pp. 23-67.
50. J.O. Rinne, T. Myllkyla, P. Lonnberg, P. Marjamaki, A postmortem study of brain nicotinic receptors in Parkinson's and Alzheimer's disease, Brain Res. 547 (1991) 167-170.
51. N. Rocamora, M. Pascual, L. Acsady, L. de Lecea, T.F. Freund, E. Soriano, Expression of NGF and NT3 mRNAs in hippocampal interneurons innervated by the GABAergic septohippocampal pathway, J. Neurosci. 16 (1996) 3991-4004.
52. S. Rossner, G. Wortwein, Z. Gu, J. Yu, R. Schlievs, V. Bigl, J.R. Perez-Polo, Cholinergic control of nerve growth factor in adult rats: evidence from cortical cholinergic deafferentation and chronic drug treatment, J. Neurochem. 69 (1997) 947-953.
53. S.T. Rouse, A.I. Levey, Expression of ml-m4 muscarinic acetylcholine receptor immunoreactivity in septohippocampal neurons and other identified hippocampal afferents, J. Comp. Neurol. 375 (1996) 406-416.
54. R. Schmidtkastner, L. Olson, Decrease of neurotrophin-3 messenger RNA in adult rat hippocampus after pilocarpine seizures, Exp. Neurol. 136 (1995) 199-204.
55. R. Schmidtkastner, C. Humpel, C. Wetmore, L. Olson, Cellular hybridisation for BDNF, trkB and NGF messenger RNAs and BDNF immunoreactivity in rat forebrain after pilocarpine-induced status epilepticus, Exp. Brain Res. 107 (1996) 3331-3347.
56. J. Scott, M. Selby, M. Urdea, M. Quiroga, G.I. Bell, W.J. Rutter, Isolation and nucleotide sequence of a cDNA encoding the precursor of mouse nerve growth factor, Nature 302 (1983) 538-540.
57. M. Shoaib, M.E. Benwell, M.T. Akbar, I.P. Stolerman, D.J. Balfour, Behavioural and neurochemical adaptations to nicotine in rats: influence of NMDA antagonists, Br. J. Pharmacol. 111 (1994) 1073-1080.
58. M. Shoaib, I.P. Stolerman, Conditioned taste aversions in rats after intracerebral administration of nicotine, Behav. Pharmacol. 6 (1995) 375-385.
59. M.V. Sofroniew, J.D. Cooper, C.N. Svendsen, P. Crossman, N.Y. Ip, R.M. Lindsay, F. Zafra, D. Lindholm, Atrophy but not death of adult septal cholinergic neurons after ablation of target capacity to produce mRNAs for NGF, BDNF, and NT-3, J. Neurosci. 13 (1993) 5263-5276.
60. M.V. Sofroniew, N.P. Galletly, O. Isacson, C.N. Svendsen, Survival of adult basal forebrain cholinergic neurons after loss of target neurons, Science 247 (1990) 338-342.
61. J. Sambrook, E.F. Fritsch, T. Maniatis, Molecular Cloning: A Laboratory Manual, 2nd edn., Cold Spring Harbor Laboratory Press, 1989.
62. D.C. Sterio, The unbiased estimation of the number and sizes of arbitrary particles using the dissector, J. Microsc. 134 (1984) 127-136.
63. M.J. Stillman, B. Shukitt-Hale, R.L. Galli, A. Levy, H.R. Lieberman, Effects of M2 antagonists on in vivo acetylcholine levels, Brain Res. Bull. 41 (1996) 221-226.
64. K. Sugaya, C. Clamp, D. Bryan, M. McKinney, mRNA for the m4 muscarinic receptor subtype is expressed in adult rat brain cholinergic neurons, Mol. Brain Res. 50 (1997) 305-313.
65. K. Sugaya, E. Giacobini, V.A. Chiappinelli, Nicotinic acetylcholine receptor subtypes in human frontal cortex: changes in Alzheimer's disease, J. Neurosci. Res. 27 (1990) 349-359.
66. D.M. Valenzuela, P.C. Maisonpierre, D.J. Glass, E. Rojas, L. Nunez, Y. Kong, D.R. Gies, T.N. Stitt, N.Y. Ip, G.D. Yancopoulos, Alternative forms of rat TrkC with different functional capabilities, Neuron 10 (1993) 1-20.
67. C.E. Van der Zee, S. Lourenssen, J. Stanisz, J. Diamond, NGF deprivation of adult rat brain results in cholinergic hypofunction and selective impairments in spatial learning, Eur. J. Neurosci. 7 (1995) 160-168.
68. J.L. Venero, F. Hefti, Regionally specific induction of BDNF and truncated trkB.T1 receptors in the hippocampal formation after intraseptal injection of kainic acid, Brain Res. 790 (1998) 270-277.
69. J.L. Venero, B. Knusel, K.D. Beck, F. Hefti, Expression of neurotrophin and trk receptor genes in adult rats with fimbria transections: effect of intraventricular nerve growth factor and brain-derived neurotrophic factor administration, Neuroscience 59 (1994) 797-815.
70. M.T. Vilaró, G.M. Mengod, J.M. Palacios, Advances and limitations of the molecular neuroanatomy of cholinergic receptors: the example of multiple muscarinic receptors, Prog. Brain Res. 98 (1993) 95-101.
71. G.I. Wilkie, P. Hutson, J.P. Sullivan, S. Wonnacott, Pharmacological characterisation of a nicotinic autoreceptor in rat hippocampal synaptosomes, Neurochem. Res. 21 (1996) 1141-1148.
72. J.H. Williams, J.A. Kauer, Properties of carbachol-induced oscillatory activity in rat hippocampus, J. Neurophysiol. 78 (1997) 2631-2640.
73. N.J. Woolf, E. Gould, L.L. Butcher, Nerve growth factor receptor is associated with cholinergic neurons of the basal forebrain but not the pontomesencephalon, Neuroscience 30 (1989) 143-152.
74. J. Yu, D.P. Pizzo, L.A. Hutton, J.R. Perez-Polo, Role of the cholinergic system in the regulation of neurotrophin synthesis, Brain Res. 705 (1995) 247-252.
75. J. Yu, R.G. Wiley, R.J. Perez-Polo, Altered NGF protein levels in different brain areas after immunolesion, J. Neurosci. Res. 43 (1996) 213-223.
76. F. Zafra, B. Heingerer, J. Leibrock, H. Thoenen, D. Lindholm, 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.
77. Z. Zang, I. Creese, Differential regulation of expression of rat hippocampal muscarinic receptor subtypes following fimbria-fornix lesion, Biochem. Pharmacol. 53 (1997) 1379-1382.