Tyrosine kinase a, galanin and nitric oxide synthase within basal forebrain neurons in the rat

Neuroscience

Volumn 87, Issue 2, 1998, Pages 447-461

  Sobreviela, T ^a   Jaffar, S ^a   Mufson, E J ^a  

^a Research Center for Brain Repair   (United States)

Author keywords

Cholinergic; Co localization; Nerve growth factor; Neuropeptide; Receptor; Tyrosine kinase

Indexed keywords

GALANIN; NERVE GROWTH FACTOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROTEIN TYROSINE KINASE; TYROSINE KINASE RECEPTOR;

ANIMAL TISSUE; ARTICLE; CHOLINERGIC NERVE CELL; CHOLINERGIC SYSTEM; CONTROLLED STUDY; ENZYME LOCALIZATION; FOREBRAIN; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; GALANIN; IMMUNOHISTOCHEMISTRY; MALE; NADPH DEHYDROGENASE; NEURONS; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE I; PROSENCEPHALON; PROTO-ONCOGENE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, TRKA; RECEPTORS, NERVE GROWTH FACTOR;

EID: 0032551565     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(98)00153-5     Document Type: Article

References (89)

1. Bartus R. T., Dean R. L., Beer B., Lippa A. S. The cholinergic hypothesis of geriatric memory dysfunction. Science. 217:1982;408-417.
2. Benzing W. C., Kordower J. H., Mufson E. J. Galanin immunoreactivity within the primate basal forebrain: evolutionary change between monkeys and apes. J. comp. Neurol. 336:1993;31-39.
3. Benzing W. C., Mufson E. J. Increased number of NADPH-d-positive neurons within the substantia innominata in Alzheimer's disease. Brain Res. 670:1995;351-355.
4. Bohme G. A., Bon C., Stutzmann J.-M., Doble A., Blanchard J.-C. Possible involvement in nitric oxide in long-term potentiation. Eur. J. Pharmac. 199:1991;379-381.
5. Bothwell M. Keeping track of neurotrophin receptors. Cell. 65:1991;915-918.
6. Brauer K., Schober A., Wolff J. R., Winkelmann E., Luppa H., Luth H.-J., Bottcher H. Morphology of neurones in the rat basal forebrain nuclei: comparison between NADPH-diaphorase histochemistry and immunochemistry of glutamic acid decarboxylase, choline acetyltransferase, somatostatin, and parvalbumin. J. Hirnforsch. 32:1991;1-17.
7. Bredt D. S., Glatt C. E., Hwang P. M., Fotuhi M., Dawson T. M., Snyder S. H. Nitric oxide synthase and mRNA are discreetly localised in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron. 7:1991;615-624.
8. Bredt D. S., Snyder S. H. Nitric oxide: a physiologic messenger module. A. Rev. Biochem. 63:1994;175-195.
9. Carnahan J., Nawa H. Regulation of neuropeptide expression in the brain by neurotrophins (potential role in vivo). Molec. Neurobiol. 10:1995;135-149.
10. Chan-Palay V. Galanin hyperinnervates surviving neurons of the human basal nucleus of Meynert in dementias of Alzheimer's and Parkinson's disease: a hypothesis for the role of galanin in accentuating cholinergic dysfunction in dementia. J. comp. Neurol. 273:1988;543-557.
11. Charles V., Mufson E. J., Friden P. M., Bartus R. T., Kordower J. H. Atrophy of cholinergic basal forebrain neurons following excitotoxic cortical lesions is reversed by intravenous administration of an NGF conjugate. Brain Res. 728:1994;193-203.
12. Clary D. O., Weskamp G., Austin L. R., Reichardt L. F. TrkA cross-linking mimics neuronal responses to nerve growth factor. Molec. Biol. Cell. 5:1994;549-563.
13. Collier T. J., Coleman P. D. Divergence of biological and chronological aging: evidence from rodent studies. Neurobiol. Aging. 12:1991;685-693.
14. Crawley J. N., Wenk G. L. Co-existence of galanin and acetylcholine: is galanin involved in memory process and dementia? Trends Neurosci. 12:1989;278-282.
15. Crawley J. N. Functional interactions of galanin and acetylcholine: relevance to memory and Alzheimer's disease. Behav. Brain Res. 57:1993;133-141.
16. Dahlstrom A. Effect of colchicine on amine storage granules in sympathetic nerves of the rat. Eur. J. Pharmac. 5:1968;111-113.
17. Dawson V. L., Dawson T. M., London E. D., Bredt D. S., Snyder S. H. Nitric oxide mediates glutamate neurotoxicity in primary cortical culture. Proc. natn. Acad. Sci. U.S.A. 88:1991;6368-6371.
18. Dawson T. M., Bredt D. S., Fotuhi M., Hwang P. M., Snyder S. H. Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc. natn. Acad. Sci. U.S.A. 88:1991;7797-7801.
19. Dawson V. L., Dawson T. M., Bartley D. A., Uhl G. R., Synder S. H. Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures. J. Neurosci. 13:1993;2651-2661.
20. De Lacalle S., Kulkarni S., Mufson E. J. Plasticity of galanergic fibers following neurotoxic damage within the rat basal forebrain: initial observations. Expl Neurol. 146:1997;361-366.
21. Ellison D. W., Kowall N. W., Martin J. B. Subset of neurons characterized by NADPH-diaphorase activity in the human substantia innominata. J. comp. Neurol. 260:1987;233-245.
22. Emerich D. F., Winn S. R., Harper J., Hammang J. P., Baetge E. E., Kordower J. H. Implants of polymer-encapsulated human NGF-secreting cells in the nonhuman primate: rescue and sprouting of degenerating cholinergic basal forebrain neurons. J. comp. Neurol. 349:1997;148-164.
23. Fisone G., Wu C. H., Consolo S., Nordström Ö., Brynne N., Bartfai T., Melander T., Hokfelt T. Galanin inhibits acetylcholine release in the ventral hippocampus of the rat: histochemical, autoradiographic, in vivo, and in vitro studies. Proc. natn. Acad. Sci. U.S.A. 84:1987;7339-7343.
24. Gally J. A., Montague P. R., Reeke G. N. Jr., Edelmen G. M. The NO hypothesis: possible effects of a short-lived, rapidly diffusible signal in the development and function of the nervous system. Proc. natn. Acad. Sci. U.S.A. 87:1990;3547-3551.
25. Geula C., Schatz C. R., Mesulam M.-M. Differential localization of NADPH-diaphorase and calbindin-D within the cholinergic neurons of the basal forebrain, striatum and brainstem in the rat, monkey, baboon and human. Neuroscience. 54:1993;461-476.
26. Gibbs R. B., Pfaff D. W. In situ hybridization detection of trkA mRNA in brain: distribution, colocalization with p75NGFR and up-regulation by nerve growth factor. J. comp. Neurol. 341:1994;324-339.
27. Girotti P., Bertorelli R., Fisone G., Land T., Langel O., Consolo A., Bartfai T. N-terminal galanin fragments inhibit the hippocampal release of acetylcholine in vivo. Brain Res. 612:1993;258-262.
28. Gnahn H., Hefti F., Heumann R., Schwab M. E., Thoenen H. NGF-mediated increase of choline acetyltransferase (ChAT) in the neonatal rat forebrain: evidence for a physiological role of NGF in the brain? Brain Res. 285:1983;45-52.
29. Hefti F., Mash D. C. Localization of nerve growth factor receptors in the normal human brain and in Alzheimer's disease. Neurobiol. Aging. 10:1989;75-87.
30. Hefti F., Hartikka J., Knusel B. Function of neurotrophic factors in the adult and aging brain and their possible use in the treatment of neurodegenerative diseases. Neurobiol. Aging. 10:1989;515-533.
31. Herdegen T., Fiallos-Estrada C. E., Bravo R., Zimmermann M. Colocalization and covariation of c-JUN transcription factor with galanin in primary afferent neurons and with CGRP in spinal motoneurons following transection of rat sciatic nerve. Molec. Brain Res. 17:1993;147-154.
32. Higgins G. A., Mufson E. J. NGF receptor gene expression is decreased in the nucleus basalis in Alzheimer's disease. Expl Neurol. 106:1989;222-236.
33. Hokfelt T., Dahlstrom A. Effect of two mitosis inhibitors (colchicine and vinblastine) on the distribution and axonal transport of noradrenaline storage particles, studied by fluorescence and electron microscopy. Z. Zellforsch. 119:1971;460-482.
34. Holtzman D. M., Kilbridge J., Bredt D. S., Black S. M., Li Y., Clary D. O., Reichardt L. F., Mobley W. C. NOS introduction by NGF in the basal forebrain cholinergic neurones: evidence for regulation of brain NOS by a neurotrophin. Neurobiol. Disease. 1:1994;51-60.
35. Holtzman D. M., Kilbridge J., Li Y., Cunningham E. T. Jr., Lenn N. J., Clary D. O., Reichardt L. F., Mobley W. C. TrkA expression in the CNS: evidence for the existence of several novel NGF-responsive CNS neurons. J. Neurosci. 15:1995;1567-1576.
36. Hyman B., Marzloff K., Wenniger J., Dawson T., Bredt D., Snyder S. Relative sparing of nitric oxide synthase-containing neurons in the hippocampal formation in Alzheimer's disease. Ann. Neurol. 32:1992;818-820.
37. Kitchener P. D., Diamond J. Distribution and colocalization of choline acetyltransferase immunocreativity and NADPH diaphorase reactivity in neurons within the medial septum and diagonal band of Broca in the rat basal forebrain. J. comp. Neurol. 335:1993;1-15.
38. Kokaia Z., Bengzon J., Metsis M., Kokaia M., Persson H., Lindvall O. Coexpression of neurotrophins and their receptors in neurons of the central nervous system. Proc. natn. Acad. Sci. U.S.A. 90:1993;6711-6715.
39. Kordower J. H. and Mufson E. J. (1989) NGF and Alzheimer's disease: unfulfilled promise and untapped potential. Neurobiol. Aging 10, 543-544; discussion 552-553.
40. Kordower J. H., Gash D. M., Bothwell M., Hersh L., Mufson E. J. Nerve growth factor receptor and choline acetyltransferase remain colocalized in the nucleus basalis (Ch4) of Alzheimer's patients. Neurobiol. Aging. 10:1989;67-74.
41. Kordower J. H., Mufson E. J. Galanin-like immunoreactivity within the primate basal forebrain: differential staining patterns between humans and monkeys. J. comp. Neurol. 294:1990;281-292.
42. Kordower J. H., Le H. K., Mufson E. J. Galanin-immunoreactivity in the primate central nervous system. J. comp. Neurol. 319:1992;479-500.
43. Kordower J. H., Winn S. R., Liu Y. T., Mufson E. J., Sladek J. R. Jr., Hammang J. P., Baetge E. E., Emerich D. F. The aged monkey basal forebrain: rescue and sprouting of axotomized basal forebrain neurons after grafts of encapsulated cells secreting human nerve growth factor. Proc. natn. Acad. Sci. U.S.A. 91:1994;10898-10902.
44. Kreutzberg G. Neuronal dynamics and axonal flow - IV. Blockage of intra axonal enzyme transport. Proc. natn. Acad. Sci. U.S.A. 62:1969;722-728.
45. Lu B., Buck C. R., Dreyfus C. F., Black I. B. Expression of NGF and NGF receptor mRNAs in the developing brain: evidence for local delivery and action of NGF. Expl Neurol. 104:1989;191-199.
46. 2+/calmodulin-dependent nitric oxide synthase from porcine cerebellum. Cofactor-role of tetrahydrobiopterin. Fedn Eur. biochem. Socs Lett. 277:1990;215-219.
47. Melander T., Staines W. A., Hokfelt T., Rokaeus A., Eckenstein F., Salvaterra P. M., Wainer B. H. Galanin-like immunoreactivity in cholinergic neurons of the septum-basal forebrain complex projecting to the hippocampus of the rat. Brain Res. 360:1985;130-138.
48. Melander T., Hîkfelt T., Rîkaeus A. Distribution of galanin-like immunoreactivity in the rat central nervous sytem. J. comp. Neurol. 248:1986;175-517.
49. Melander T., Staines W. A. A galanin-like peptide exists in putative cholinergic somata of the septal-basal forebrain complex and in acetylcholinesterase-containing fibres and varicosities within the hippocampus in the owl monkey. Neurosci. Lett. 68:1986;17-22.
50. Mesulam M.-M., Mufson E. J., Wainer B. H., Levey A. I. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature. Neuroscience. 10:1983;1185-1201.
51. Mesulam M.-M., Geula C., Bothwell M. A., Hersh L. B. Human reticular formation: cholinergic neurons of the pedunculopontine and laterodorsal tegmental nuclei and some cytochemical comparisons to forebrain cholinergic neurons. J. comp. Neurol. 281:1989;611-633.
52. Miranda R. C., Sohrabji F., Toran-Allerand C. D. Neuronal colocalization of mRNAs for neurotrophins and their receptors in the developing central nervous system suggests a potential for autocrine interactions. Proc. natn. Acad. Sci. U.S.A. 90:1993;6439-6443.
53. Mufson E. J., Mash D. C., Hersh L. B. Neurofibrillary tangles in cholinergic pedunculopontine neurons in Alzheimer's disease. Ann. Neurol. 24:1988;623-629.
54. Mufson E. J., Bothwell M., Hersh L. B., Kordower J. H. Nerve growth factor receptor immunoreactive profiles in the normal, aged human basal forebrain: colocalization with cholinergic neurons. J. comp. Neurol. 285:1989;196-217.
55. Mufson E. J., Bothwell M., Kordower J. H. Loss of nerve growth factor receptor-containing neurons in Alzheimer's disease: a quantitative analysis across subregions of the basal forebrain. Expl Neurol. 105:1989;221-232.
56. Mufson E. J., Brady D. R., Carey R. G. Reduced nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d) histochemistry in the hippocampal formation of the New World monkey (Saimiri sciureus). Brain Res. 516:1990;237-247.
57. Mufson E. J., Cochran E., Benzing W., Kordower J. H. Galaninergic innervation of the cholinergic vertical limb of the diagonal band (Ch2) and bed nucleus of the stria terminalis in aging. Alzheimer's disease and Down's syndrome. Dementia. 4:1993;237-250.
58. Mufson E. J., Brandabur M. M. Sparing of NADPH-diaphorase striatal neurons in Parkinson's and Alzheimer's diseases. NeuroReport. 5:1994;705-708.
59. Mufson E. J., Li J. M., Sobreviela T., Kordower J. H. Decreased trkA gene expression within basal forebrain neurons in Alzheimer's disease. NeuroReport. 20(8):1996;25-29.
60. Mufson E. J., Lavine N., Jaffar S., Kordower J. H., Quirion R., Saragovi H. U. Reduction in p140-TrkA receptor protein within the nucleus basalis and cortex in Alzheimer's disease. Expl Neurol. 146:1997;91-103.
61. Nieuwenhuys R. (1985) Chemoarchitecture of the Brain. Springer-Verlag, New York.
62. Ogren S. O., Hîkfelt T., Kask K., Langel Ö., Bartfai T. Evidence for a role of the neuropeptide galanin in spatial learning. Neuroscience. 51:1992;1-5.
63. Palazzi E., Fisone G., Hökfelt T., Bartfai T., Consolo S. Galanin inhibits the muscarinic stimulation of phosphoinositide turnover in rat ventral hippocampus. Eur. J. Pharmac. 148:1988;479-480.
64. Pasqualotto B. A., Vincent S. R. Galanin and NADPH-diaphorase coexist in cholinergic neurons of the rat basal forebrain. Brain Res. 551:1991;78-86.
65. Pitkanen A., Amaral D. G. Distribution of reduced nicotinamide adenine dinucleotide phosphate diaphorase (NADPH-d) cells and fibers in the monkey amygdaloid complex. J. comp. Neurol. 313:1991;326-348.
66. Planas B., Kolb P. E., Raskind M. A., Miller M. Nerve growth induces galanin gene expression in the rat basal forebrain: implications for the treatment of cholinergic dysfunction. J. comp. Neurol. 379:1997;563-570.
67. Prast H., Philippu A. Nitric oxide releases acetylcholine in the basal forebrain. Eur. J. Pharmac. 216:1992;139-140.
68. Rebeck G. W., Marzloff K., Hyman B. T. The pattern of NADPH-diaphorase staining, a marker of nitric oxide synthase activity, is altered in the perforant pathway terminal zone in Alzheimer's disease. Neurosci. Lett. 152:1993;165-168.
69. Robbin T. W., Everitt B. J., Marston H. M., Wilkinson J., Jones G. H., Page K. J. Comparative effects on idotenic acid- and quisqualic-acid induced lesions of the substantia nigra on attentional function in the rat; further implications for the role of the cholinergic neurons of the nucleus basalis in cognitive processes. Behav. Brain Res. 35:1989;221-241.
70. Robinson J. K., Crawley J. N. Intraventricular galanin impairs delayed nonmatching-to-sample performance in rats. Behav. Neurosci. 107:1993;458-467.
71. Rodrigo J., Springall D. R., Uttenthal O., Bentura M. L., Abadia-Molina F., Riveros-Moreno V., Martinez-Murillo R., Polak J. M., Moncada S. Localization of nitric oxide synthase in the adult rat brain. Phil. Trans. R. Soc. Lond. B. 345:1994;175-221.
72. Scherer-Singler U., Vincent S. R., Kimura H., McGeer E. G. Demonstration of a unique poualation of neurons with NADPH-diaphorase histochemistry. J. Neurosci. Meth. 9:1983;229-234.
73. Schmidt H. H., Gagne G. D., Nakane M., Pollock J. S., Miller M. F., Murad F. Mapping of neural nitric oxide synthase in the rat suggests frequent co-localization with NADPH diaphorase but not with soluble guanylyl cyclase, and novel paraneural functions for nitrinergic signal transduction. J. Histochem. Cytochem. 40:1992;1439-1456.
74. Schober A., Brauer K., Luppa H. Alternate coexistence of NADPH-diaphorase with choline acetyltransferase or somatostatin in the rat neostriatum and basal forebrain. Acta histochem. cytochem. 22:1989;669-674.
75. Schuman E. M., Madison D. V. A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science. 254:1991;150-156.
76. Shandra A. A., Mazarati A. M., Servetskii K. L. Influence of the neuropeptide galanin on active avoidance in rats. Neurosci. behav. Physiol. 24:1994;429-432.
77. Skofitsch G., Jacobowitz D. M. Immunohistochemical mapping of galanin-like neurons in the rat central nervous system. Peptides. 6:1985;509-546.
78. Sobreviela T., Clary D. O., Reichardt L. F., Brandabur M. M., Kordower J. H., Mufson E. J. TrkA-Immunoreactive profiles in the central nervous system: colocalization with neurons containing p75 nerve growth factor receptor, choline acetyltransferase, and serotonin. J. comp. Neurol. 350:1994;587-611.
79. Sobreviela T., Mufson E. J. Reduced nicotinamide adenine dinucleotide phosphate-diaphorase/nitric oxide synthase profiles in the human hippocampal formation and perirhinal cortex. J. comp. Neurol. 358:1995;440-464.
80. Solodkin A., Traub R. J., Gebhart G. F. Unilateral hindpaw inflammation produces a bilateral increase in NADPH-diaphorase histochemical staining in the rat lumbar spinal cord. Neuroscience. 51:1992;495-499.
81. Springer J. E., Koh S., Tayrien M. W., Loy R. Basal forebrain magnocellular neurons strain for nerve growth factor receptor: correlation with cholinergic cell bodies and effects of axotomy. J. Neurosci. Res. 17:1987;111-118.
82. Steininger T. L., Wainer B. H., Klein R., Barbacid M., Palfrey H. C. High-affinity nerve growth factor receptor (Trk) immunoreactivity is localized in cholinergic neurons of the basal forebrain and striatum in the adult rat brain. Brain Res. 612:1993;330-335.
83. Ukai M., Miura M., Kameyama T. Effects of galanin on passive avoidance response, elevated plus-maze learning, and spontaneous alternation performance in mice. Peptides. 16:1995;1283-1286.
84. Walker L. C., Lokiatsos V. E., Kitt C. A., Richardson R. T., Rokaeus A., Price D. L. Peptide neurons in the basal forebrain magnocellular complex if the rhesus monkey. J. comp. Neurol. 280:1989;272-282.
85. Walker L. C., Rance N. E., Price D. L., Young W. S. Galanin in mRNA in the nucleus basalis of Meynert complex of baboons and humans. J. comp. Neurol. 303:1991;113-120.
86. Wenk G. L., Stoehr J. D., Quintana G., Mobley S., Wiley R. G. Behavioral, biochemical, histological, and electrophysiological effects of 192 IgG-saporin injections into the basal forebrain of rats. J. Neurosci. 10:1994;5986-5995.
87. Whitehouse P. J., Price D. I., Struble R. G., Clark A. W., Coyle J. T., DeLong M. R. Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science. 215:1982;1237-1239.
88. Williams L. R., Varon S., Peterson G. M., Wictorin K., Fischer W., Bjorklund A., Gage F. H. Continuous infusion of nerve growth factor prevents basal forebrain neuronal death after fimbria fornix transection. Proc. natn. Acad. Sci. U.S.A. 83:1986;9231-9235.
89. Wu W. Expression in nitric-oxide synthase (NOS) in injured CNS neurons as shown by NADPH diaphorase histochemistry. Expl Neurol. 120:1993;153-159.