The effects of chronic ethanol consumption on neurotrophins and their receptors in the rat hippocampus and basal forebrain

Brain Research

Volumn 950, Issue 1-2, 2002, Pages 137-147

  Miller, R ^a   King, M A ^a,b   Heaton, M B ^a   Walker, D W ^a,b  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Acetylcholine; Alcoholism; Forebrain; Receptor; Trophic factor

Indexed keywords

ALCOHOL; BRAIN PROTEIN; MESSENGER RNA; NEUROTROPHIN; NEUROTROPHIN RECEPTOR;

ALCOHOL CONSUMPTION; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; BRAIN REGION; CONTROLLED STUDY; FOREBRAIN; HIPPOCAMPUS; LEARNING; MALE; MALNUTRITION; NONHUMAN; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; WESTERN BLOTTING;

ALCOHOL DRINKING; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; ETHANOL; HIPPOCAMPUS; MALE; PROSENCEPHALON; RATS; RATS, LONG-EVANS; RECEPTOR, NERVE GROWTH FACTOR; RECEPTOR, TRKA; RECEPTOR, TRKB; RECEPTORS, NERVE GROWTH FACTOR; RNA, MESSENGER;

EID: 0037145050     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(02)03014-7     Document Type: Article

References (100)

1. Alberch J., Pérez-Navarro E., Arenas E., Marsal J. Involvement of nerve growth factor and its receptor in the regulation of the cholinergic function in aged rats. J. Neurochem. 57:(5):1991;1483-1487.
2. Aloe L., Tirassa L.P. The effect of long-term alcohol intake on brain NGF-target cells of aged rats. Alcohol. 9:1992;299-304.
3. Alvarez P., Zola-Morgan S., Squire L.R. Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys. J Neurosci. 15:(5 Pt 2):1995;3796-3807.
4. Arendt T. Impairment in memory function and neurodegenerative changes in the cholinergic basal forebrain system induced by chronic intake of ethanol. J. Neural Transm. Suppl. 44:1994;173-187.
5. Arendt T., Brückner M.K., Paglius S., Krell T. Degeneration of rat cholinergic basal forebrain neurons and reactive changes of nerve growth factor expression after chronic neurotoxic injury I. Degeneration and plastic response of basal forebrain neurons. Neuroscience. 65:(3):1995;633-645.
6. Arendt T., Allen Y., Sinden J., Schugens M.M., Marchbanks R.M., Lantos P.L., Gray J.A. Cholinergic-rich brain transplants reverse alcohol-induced memory deficits. Nature. 332:(6163):1988;448-450.
7. Arendt T., Henning D., Marchbanks R. Loss of neurons in the rat basal forebrain cholinergic system after prolonged intake of ethanol. Brain Res. Bull. 21:1988;563-570.
8. Baek J.K., Heaton M.B., Walker D.W. Chronic alcohol ingestion: nerve growth factor gene expression and neurotrophic activity in rat hippocampus. Alcohol. Clin. Exp. Res. 18:(6):1994;1368-1376.
9. Baek J.K., Heaton M.B., Walker D.W. Upregulation of high-affinity neurotrophin receptor TrkB-like protein on Western blots of rat cortex after chronic ethanol treatment (CET). Mol. Brain Res. 40:1996;161-164.
10. Barettino D., Pombo P.M.G., Espliguero G., Rodriguez-Pena A. The mouse neurotrophin receptor trkB gene is transcribed from two different promoters. Biochim. Biophys. Acta. 1446:1999;24-34.
11. Barker P.A., Lomen-Hoerth C., Gensch E.M., Meakin S.O., Grass D.J., Shooter E.M. Tissue-specific alternative splicing generates two isoforms of the trkA receptor. J. Biol. Chem. 268:1993;15150-15157.
12. Baxter G.T., Radeke M.J., Kuo R.C., Makrides V., Hinkle B., Hoang R., Medina-Selby A., Coit D., Valenzuela P., Feinstein S.C. Signal transduction mediated by the truncated trkB receptor isoforms, trkB.T1 and trkB.T2. J. Neurosci. 17:(8):1997;2683-2690.
13. Berse B., Lopez-Coviella I., Blusztajn J.K. Activation of trkA by nerve growth factor upregulates expression of the cholinergic gene locus but attenuates the response to cililary neurotrophic growth factor. Biochem. J. 342:1999;301-308.
14. Bibel M., Hoppe E., Barde Y.-A. Biochemical and functional interactions between the neurotrophin receptors trk and p75NTR. EMBO. 18:(3):1999;616.
15. Birling M.-C., Barde A., Price J. Influence of growth factors on neuronal differentiation. Curr. Opin. Cell Biol. 7:1995;878-884.
16. Bohbot V.D., Allen J.J., Nadel L. Memory deficits characterized by patterns of lesions to the hippocampus and parahippocampal cortex. Ann. N. Y. Acad. Sci. 91:2000;355-368.
17. Boissiere F., Faucheux B., Ruberg M., Agid Y., Hirsch E.C. Decreased trkA gene expression in cholinergic neurons of the striatum and basal forebrain of patients with Alzheimer's disease. Exp. Neurol. 145:1997;245-252.
18. Cadete-Leite A., Andrade J.P., Sousa N., Ma W., Ribeiro-Da-Silva A. Effects of chronic alcohol consumption on the cholinergic innervation of the rat hippocampal formation as revealed by choline acetyltransferase immunocytochemistry. Neuroscience. 64:(2):1995;357-374.
19. Canals J.M., Checa N., Marco S., Michels A., Perez-Navarro E., Alberch J. The neurotrophin receptor trkA, trkB and trkC are differentially regulated after excitotoxic lesion in rat striatum. Mol. Brain Res. 69:1999;242-248.
20. Casaccia-Bennefil P., Carter B.D., Dobrowsky R.T., Chao M.V. Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature. 383:1996;716-719.
21. Casamenti F., Scali C., Vannucchi M.G., Bartolini L., Pepeu G. Long-term ethanol consumption by rats: effect on acetylcholine release in vivo, choline acetyltransferase activity, and behavior. Neuroscience. 56:(2):1993;465-471.
22. Charness M.E. Clinical and pathologic overview of the brain disorders in alcoholics. in NIAAA. Res. Monogr. 22:1993;15-35.
23. Chrobak J., Septal J. Orchestration of hippocampal network dynamics. Numan R., The Behavorial Neuroscience of the Septal Region. 2000;71-91 Springer, New York.
24. Cullen K.M., Halliday G.M. Mechanisms of cell death in cholinergic basal forebrain neurons in chronic alcoholics. Metab. Brain Dis. 10:1995;81-91.
25. DiStefano P.S., Friedman B., Radziejewski C., Alexander C., Boland P., Schick C.M., Lindsay R.M., Wiegand S.J. The neurotrophins BDNF, NT-3, and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron. 8:1992;983-993.
26. Fadda F., Rossetti Z.L. Chronic ethanol consumption: from neuroadaptation to neurodegeneration. Prog. Neurobiol. 56:1998;385-431.
27. Fischer W., Bjorkland A., Chen K., Gage I.H. NGF improves spatial memory in aged rodents as a function of age. J. Neurosci. 1:(7):1991;1889-1906.
28. Floyd E.A., Young-Siegler A.C., Ford B.D., Reasor J.D., Moore E.L., Townsel J.G., Rucker H.K. Chronic ethanol ingestion produces cholinergic hypofunction in rat brain. Alcohol. 14:(1):1997;93-98.
29. Gayer G.G., Gordon A., Miles M.F. Ethanol increases tyrosine hydroxylase gene expression in N1E-115 neuroblastoma cells. JBC. 33:(25):1991;22279-22284.
30. Givens B., Williams J.M., Gill T.M. Septohippocampal pathway as a site for the memory-impairing effects of ethanol. Hippocampus. 10:(1):2000;111-121.
31. Greferath U., Bennie A., Kourakis A., Bartlett P.F., Murphy M., Barrett G.L. Enlarged cholinergic forebrain neurons and improved spatial learning in p75 knockout mice. Eur. J. Neursoci. 12:2000;885-893.
32. Hagg T., Straube A., Frotscher M. Recovery of ChAT immunoreactivity in axotomizd rat cholinergic septal neurons despite reduced NGF receptor expression. Eur. J. Neurosci. 9:(7):1997;1340-1349.
33. Halford W.P. The essential prerequisites for quantitative RT-PCR. Nat. Biotechnol. 17:1999;835.
34. Haniu M., Montesruque S., Bures E.J., Talvenheimo J., Toso R., Lewis-Sandy S., Welcher A.A., Rohde M.F. Interactions between brain-derived neurotrophic factor and the trkB receptor. JBC. 272:(40):1997;25296-25315.
35. Harding A.J., Wong A., Svoboda M., Kril J.J., Halliday G.M. Chronic alcohol consumption does not cause hippocampal neuron loss in humans. Hippocampus. 7:(1):1997;78-87.
36. Hasenöhrl R.U., Söderström S., Mahammed A.H., Ebendal T., Huston J.P. Reciprocal changes in expression of mRNA for nerve growth factor and its receptors trkA and LNGFR in brain of aged rats in relation to maze learning deficits. Exp. Brain Res. 114:1997;205-213.
37. Hata T., Meyer J.S., Tanahashi N., Ishikawa Y., Imai A., Shinohara T., Velez M., Fann W.E., Kandula P., Sakai F. Three-dimensional mapping of local cerebral perfusion in alcoholic encephalopathy with and without Wernicke-Korsakoff syndrome. J. Cereb. Blood Flow Metab. 7:1987;35-44.
38. Hofer M., Pagliusi S., Hohn A., Leibrock J., Barde Y.-A. Regional distribution of brain-derived neurotrophic factor RNA in the adult mouse brain. EMBO. 9:1990;2459-2464.
39. Holtzman D.M., Li Y., Parada L.F., Kinsman S., Chen C.K., Valletta J.S., Zhou J., Long J.B., Mobley W.C. p140 trk mRNA marks NGF-responsive forebrain neurons: evidence that trk gene expression is induced by NGF. Neuron. 9:1992;465-478.
40. Hortnagl H., Hellweg R. Insights into the role of the cholinergic component of the septohippocampal pathway: what have we learned from experimental lesion studies? Brain Res. Bull. 43:(3):1997;245-255.
41. Huang E.J., Zang K., Schmidt A., Saulys A., Xiang M., Reichardt L.F. POU domain factor Brn-3a controls the differentiation and survival of trigeminal neuron by regulation Trk receptor expression. Development. 126:1999;2869-2882.
42. Ibanez C.F., Ebendal T., Barbany G., Murray-Rust J., Blundell T.L. Disruption of the low affinity receptor-binding site in NGF allows neuronal survival and differentiation by binding to the trk gene product. Cell. 69:1992;329-341.
43. Kaplan D.R., Hemstead B.L., Martin-Zanca D., Chao M.V., Parada L.F. Trk proto-oncogene product: a signal transduction receptor for nerve growth factor. Science. 252:1991;554-558.
44. Klein R., Jing S., Nanduri V., O'Rourke E., Barbacid M. The trk proto-oncogene encodes a receptor for nerve growth factor. Cell. 65:1991;189-197.
45. Kojima M., Ikeuchi T., Hatanaka H. Nerve growth factor induces trkA mRNA expression in cultured basal forebrain neurons from 17-day fetal rats. Neurosci. Lett. 169:1994;47-50.
46. Knusel B., Gao H., Okazaki T., Yoshida T., Mori N., Hefti F., Kaplan D.R. Ligand-induced down-regulation of trk messenger RNA, protein, and tyrosine phosphorylation in rat cortical neurons. Neuroscience. 78:1997;851-862.
47. Kramer B.M.R., Va Der Zee C.E.E.M., Hagg T. P75 nerve growth factor receptor is important for retrograde transport of neurotrophins in adult cholinergic basal forebrain neurons. Neuroscience. 94:(4):1999;1163-1172.
48. Lapchak P.A., Araujo D.M., Carswell S., Hefti F. Distribution of [125I]nerve growth factor in the rat brain following a single intraventricular injection: correlation with the topographical distribution of trkA messenger RNA-expressing cells. Neuroscience. 54:(20):1993;445-460.
49. Leanza G., Muir J., Nilsson O.G., Wiley R.G., Dunnett S.B., Bjorklund A. Selective immunolesioning of the basal forebrain cholinergic system disrupts short-term memory in rats. Eur. J. Neurosci. 8:(7):1996;1535-1544.
50. Lee T.-H., Kato H., Pan L.-H., Ryu J.H., Kogure K., Itoyama Y. Localization of nerve growth factor, trkA, and p75 immunoreactivity in the hippocampal formation and basal forebrain of adult rats. Neuroscience. 83:(2):1998;335-349.
51. Lei L., Ma L., Nef S., Thai T., Parada L.F. MKlf7, a potential transcriptional regulator of TrkA nerve growth factor receptor expression in sensory and sympathetic neurons. Development. 128:(7):2001;1147-1158.
52. Levi-Montalcini R., Skaper S.D., Dal Toso R., Peetrelli L., Leon A. Nerve growth factor: from neurotrophin to neurokine. Trends Neurosci. 19:1996;514-520.
53. Lucidi-Phillipi C.A., Clary D.O., Reichardt L.F., Gage F.H. TrkA activation is sufficient to rescue axotomized cholinergic neurons. Neuron. 16:1996;653-663.
54. Lukoyanov N.V., Brandao F., Cadete-Leite A., Madeira M.D., Paulla-Barbosa M.M. Synaptic reorganization in the hippocampal formation of alcohol-fed rats may compensate for functional deficits related to neuronal loss. Alcohol. 20:2000;139-148.
55. Luo J., West J.R., Pantazis N.J. Ethanol exposure reduces the density of the low-affinity nerve growth factor receptor (p75) on pheochromocytoma (PC12) cells. Brain Res. 737:1996;34-44.
56. Ma L., Merenmies J., Parada L.F. Molecular characterization of the TrkA/NGF receptor minimal enhancer reveals regulation by multiple cis elements to drive embryonic neuron expression. Development. 127:2000;3777-3788.
57. MacLennan A.J., Lee N., Walker D.W. Chronic ethanol administration decreased brain-derived neurotrophic factor gene expression in the rat hippocampus. Neurosci. Lett. 197:1995;105-108.
58. Matthews D.B., Morrow A.L. Effects of acute and chronic ethanol exposure on spatial cognitive processing and hippocampal function in the rat. Hippocampus. 10:(1):2000;122-130.
59. Melis F., Stancampiano R., Imperato A., Carta G., Fadda F. Chronic ethanol consumption in rats: correlation between memory performance and hippocampal acetylcholine release in vivo. Neuroscience. 74:(1):1996;155-159.
60. Middemas D.S., Lindberg R.A., Hunter T. TrkB, a neural receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors. Mol. Cell. Biol. 11:(1):1991;143-153.
61. Miles M.F., Diaz J.E., DeGuzman V. Ethanol-responsive gene expression in neural cell cultures. Biochim. Biophys. Acta. 1138:1992;268-274.
62. Miles M.F., Diaz J.E., DeGuzman V.S. Mechanisms of neuronal adaptation to ethanol. JBC. 266:(4):1991;2409-2414.
63. Miles M.F., Wilke N., Elliot M., Tanner W., Shah S. Ethanol-responsive genes in neural cells include the 78-kilodalton glucose-regulated protein (GRP78) and 94-kilodalton glucose-regulated protein (GRP94) molecular chaperones. Exp. Phamacol. 46:1994;873-879.
64. Montero C.N., Hefti F. Rescue of lesioned septal cholinergic neurons by nerve growth factor: specificity and requirement for chronic treatment. J. Neurosci. 8:(8):1988;2986-2999.
65. Morel Y., Barouki R. Repression of gene expression by oxidative stress. Biochem. J. 342:1999;481-496.
66. Mufson E.J., Li J.-M., Subreviela T., Kordower J.H. Decreased trkA gene expression within basal forebrain neurons in Alzheimer's disease. Neuroreport. 8:1996;25-29.
67. Naumann T., Straube A., Frotscher M. Recovery of ChAT immunoreactivity in axotomized rat cholinergic septal neurons despite reduced NGF receptor expression. Eur. J. Neurosci. 9:(7):1997;1340-1349.
68. Nikam D.S., Tennekoon G.I., Christy B.A., Yoshino J.E., Rutkowski J.L. The Zinc finger transcription factor Zif268/Egr-1 is essential for Schwann cell expression of the p75 NGF receptor. Mol. Cell. Neurosci. 6:(4):1995;337-348.
69. Olton D.S. Dementia: animal models of the cognitive impairments following damage to the basal forebrain cholinergic system. Brain Res. Bull. 25:(3):1990;499-502.
70. Orona E., Hunter B.E., Walker D.W. Ethanol exposure following unilateral entorhinal deafferentation alters synaptic reorganization in the dentate gyrus: a quantitative analysis of acetylcholinesterase histochemistry. Exp. Neurol. 101:1988;114-131.
71. Pang K.C., Nocera R., Secor A.J., Yoder R.M. GABAergic septohippocampal neurons are not necessary for spatial memory. Hippocampus. 11:(6):2001;814-827.
72. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates. 2nd Edition, Academic Press. 1986, Fig. 30.
73. Ploner C.J., Gaymard B.M., Rivaud-Pechoux S., Baulac M., Clemenceau S., Samson S., Pierrot-Deseilligny C. Lesions affecting the parahippocampal cortex yield spatial memory deficits in humans. Cereb. Cortex. 10:(12):2000;1211-1216.
74. Pioro E.P., Cuello A.C. Distribution of nerve growth factor receptor-like immunoreactivity in the adult rat central nervous system. Effect of colchicine and correlation with the cholinergic system - I. Forebrain. Neuroscience. 34:(1):1990;57-87.
75. Pires R.G., Pereira S.R., Pittella J.E., Franco G.C., Ferreira C.L., Fernandes P.A., Ribeiro A.M. The contribution of mild thiamine deficiency and ethanol consumption to central cholinergic parameter dysfunction and rats' open-field performance impairment. Pharmacol. Biochem. Behav. 70:(2-3):2001;227-235.
76. Rachamin G., Luttge W.G., Hunter B.E., Walker D.W. Neither chronic exposure to ethanol nor aging affects Type I or Type II corticosteroid receptors in rat hippocampus. Exp. Neurol. 106:1989;164-171.
77. Rosenbaum R.S., Winocur G., Moscovitch M. New views on old memories: re-evaluating the role of the hippocampal complex. Behav. Brain Res. 127:(1-2):2001;183-197.
78. Sacristan M.P., de Diego J.G., Bopnilla M., Martin-Zanca D. Molecular cloning and characterization of the 5′ region of the mouse trkA proto-oncogene. Oncogene. 18:1999;5836-5842.
79. Santin L.J., Rubio S., Begega A., Arias J.L. Effects of chronic alcohol consumption on spatial reference and working memory tasks. Alcohol. 20:2000;149-159.
80. Seabold G.K., Luo J., Miller M.W. Effect of ethanol on neurotrophin-mediated cell survival and receptor expression in cultures of cortical neurons. Dev. Brain Res. 108:1998;139-145.
81. 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.
82. Sofroniew M.V., Cooper J.D., Svendsen C.N., Crossman P., Ip N.Y., Lindsay R.M., Zafra F., Lindholm D. Atrophy but not death of adult septal cholinergic neurons after ablation of target capacity to produce mRNA for NGF, BDNF, and NT3. J. Neurosci. 13:(12):1993;5263-5276.
83. Steigerwald E.S., Miller M.W. Performance by adult rats in sensory-mediated radial arm maze tasks is not impaired and may be transiently enhanced by chronic exposure to ethanol. Alcohol. Clin. Exp. Res. 21:(9):1997;1553-1559.
84. Tapia-Arancibia L., Rage F., Givalois L., Dingeon P., Arancibia S., Beauge F. Effects of alcohol on brain-derived neurotrophic factor mRNA expression in discrete regions of the rat hippocampus and hypothalamus. J. Neurosci. Res. 63:2001;200-208.
85. Thoenen H. Neurotrophins and neuronal plasticity. Science. 170:1995;593-598.
86. Thoenen H. The changing scene of neurotrophic factors. Trends Neurosci. 14:1991;165-170.
87. Tian X., Sun S., Suszkiw J.B. Developmental age-dependent upregulation of choline acetyltransferase and vesicular acetylcholine transporter mRNA expression in neonatal rat septum by nerve growth factor. Neurosci. Lett. 209:1996;134-136.
88. Walker D.W., Heaton M.B., Hunter B.E. A role for neurotrophins in ethanol-induced brain damage. Alcohol Induced Brain Damage. NIAAA Research Monograph. Vol. 22:1993;401-414.
89. Walker D.W., Hunter B.E., Abraham W.C. Neuroanatomical and functional deficits subsequent to chronic ethanol administration in animals. Alcohol. Clin. Exp. Res. 5:1981;267-282.
90. Walker D.W., Barnes D.E., Zornettzer S.F., Hunter B.E., Kubanis P. Neuronal loss in hippocampus induced by prolonged ethanol consumption in rats. Science. 209:1980;711-713.
91. Walker D.W., Hunter B.E. Short-term memory impairment following chronic alcohol consumption in rats. Neuropsychologia. 16:1978;545-553.
92. Walker D.W., Freund G. Impairment of shuttle box avoidance learning following prolonged alcohol consumption in rats. Physiol. Behav. 7:1970;773-778.
93. Weis J.H., Tan S.S., Martin B.K., Wittwer C.T. Detection of rare mRNAs via quantitative RT-PCR. Trends Genet. 8:(8):1992;263-264.
94. White A.M., Matthews D.B., Best P.J. Ethanol, memory, and hippocampal function: a review of recent findings. Hippocampus. 10:(1):2000;88-93.
95. Whittemore P.L., Friedman P.L., Larhammar D., Persson H., Gonzalez-Carvaajal M., Holets V.R. Rat-nerve growth factor sequence and site of synthesis in the adult hippocampus. J. Neurosci. Res. 20:1988;403-410.
96. Woolf N.J., Milov A.M., Schweitzer E.S., Roghani A. Elevation of nerve growth factor and antisense knockdown of TrkA receptor during contextual memory consolidation. J. Neurosci. 21:(3):2001;1047-1055.
97. Wrenn C.C., Wiley R.G. The behavioral functions of the cholinergic basal forebrain: lessons from 192 IgG-saporin. Int. J. Dev. Neurosci. 16:(7-8):1998;595-602.
98. Yeo T.T., Couzens J.C., Butcher L.L., Bredesen D.E., Cooper J.D., Valletta J.S., Mobley W.C., Longo F.M. Absence of p75LNTR causes increased basal forebrain cholinergic neuron size, choline acetyltransferase activity, and target innervation. J. Neurosci. 17:(20):1997;7594-7605.
99. Yoon S.O., Casaccia-Bonnefil P., Carter B., Chao M.S. Competitive signaling between TrkA and p75 nerve growth factor receptors determines cell survival. J. Neurosci. 18:(9):1998;3273-3281.
100. Zoeller R.T., Fletcher D.L. A single administration of ethanol simultaneously increases c-fos mRNA and reduces c-jun mRNA in the hypothalamus and hippocampus. Mol. Brain Res. 24:1994;185-191.