Functional nerve growth factor and trkA autocrine/paracrine circuits in adult rat cortex are revealed by episodic ethanol exposure and withdrawal

Journal of Neurochemistry

Volumn 100, Issue 5, 2007, Pages 1155-1168

  Bruns, Marla B ^a   Miller, Michael W ^a,b,c  

^a State University of New York Upstate Medical University: College of Medicine   (United States)

^b SYRACUSE VA MEDICAL CENTER   (United States)

^c Developmental Exposure Alcohol Research Center   (United States)

Author keywords

Alcohol; Anterograde; Dementia; Neurotrophin; Pyramidal neurons; Receptor; Somatosensory cortex; Translation

Indexed keywords

ALCOHOL; MESSENGER RNA; NERVE GROWTH FACTOR; PHOSPHOPROTEIN; PROTEIN TYROSINE KINASE A;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOCRINE EFFECT; BRAIN CORTEX; BRAIN TISSUE; CHEMICAL LABELING; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME PHOSPHORYLATION; EXPOSURE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARACRINE SIGNALING; PERIKARYON; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT;

ANIMALS; AUTOCRINE COMMUNICATION; CEREBRAL CORTEX; ETHANOL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; NERVE GROWTH FACTOR; NEURONS; PARACRINE COMMUNICATION; PHOSPHORYLATION; RATS; RATS, LONG-EVANS; RECEPTOR, TRKA; RNA, MESSENGER; SUBSTANCE WITHDRAWAL SYNDROME;

RATTUS;

EID: 33847005102     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04301.x     Document Type: Article

References (92)

1. Acheson A. and Lindsay R. M. (1996) Non target-derived roles of the neurotrophins. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 351, 417-422.
2. Allen S. J. and Dawbarn D. (2006) Clinical relevance of the neurotrophins and their receptors. Clin. Sci. 110, 175-191.
3. Aloe L., Bracci-Laudiero L. and Tirassa P. (1993) The effect of chronic ethanol intake on brain NGF level and on NGF-target tissues of adult mice. Drug Alcohol Depend. 31, 159-167.
4. Arendt T. (1994) Impairment in memory function and neurodegenerative changes in the cholinergic basal forebrain system induced by chronic intake of ethanol. J. Neural. Trans. Suppl. 44, 173-187.
5. Arendt T., Allen Y., Sinden J., Schugens M. M., Marchbanks R. M., Lantos P. L. and Gray J. A. (1988) Cholinergic-rich brain transplants reverse alcohol-induced memory deficits. Nature 332, 448-450.
6. Arendt T., Allen Y., Marchbanks R. M., Schugens M. M., Sinden J., Lantos P. L. and Gray J. A. (1989) Cholinergic system and memory in the rat:effects of chronic ethanol, embryonic basal forebrain brain transplants and excitotoxic lesions of cholinergic basal forebrain projection system. Neuroscience 33, 435-462.
7. Arendt T., Bruckner M. K., Krell T., Pagliusi S., Kruska L. and Heumann R. (1995) Degeneration of rat cholinergic basal forebrain neurons and reactive changes in nerve growth factor expression after chronic neurotoxic injury - II. Reactive expression of the nerve growth factor gene in astrocytes. Neuroscience 65, 647-659.
8. Barde Y. A. (1994) Neurotrophins: a family of proteins supporting the survival of neurons. Prog. Clin. Biol. Res. 390, 45-56.
9. Blesch A., Conner J., Pfeifer A., Gasmi M., Ramirez A., Britton W., Alfa R., Verma I. and Tuszynski M. H. (2005) Regulated lentiviral NGF gene transfer controls rescue of medial septal cholinergic neurons. Mol. Ther. 11, 916-925.
10. Brooks A. I., Cory-Slechta D. A., Bowers W. J., Murg S. L. and Federoff H. J. (2000) Enhanced learning in mice parallels vector-mediated nerve growth factor expression in hippocampus. Hum. Gene Ther. 11, 2341-2352.
11. Cadete-Leite A., Pereira P. A., Madeira M. D. and Paula-Barbosa M. M. (2003) Nerve growth factor prevents cell death and induces hypertrophy of basal forebrain cholinergic neurons in rats withdrawn from prolonged ethanol intake. Neuroscience 119, 1055-1069.
12. Carmignoto G., Pizzorusso T., Tia S. and Vicini S. (1997) Brain-derived neurotrophic factor and nerve growth factor potentiate excitatory synaptic transmission in the rat visual cortex. J. Physiol. 498, 153-164.
13. Chao M. V. (2000) Trophic factors: an evolutionary cul-de-sac or door into higher neuronal function? J. Neurosci. Res. 59, 353-355.
14. Chao M. V., Rajagopal R. and Lee F. S. (2006) Neurotrophin signalling in health and disease. Clin. Sci. (Lond.) 110, 167-173.
15. Charness M. E. (1993) Brain lesions in alcoholics. Alcohol. Clin. Exp. Res. 17, 2-11.
16. Chen C. and Tonegawa S. (1997) Molecular genetic analysis of synaptic plasticity, activity-dependent neural development, learning, and memory in the mammalian brain. Annu. Rev. Neurosci. 20, 157-184.
17. Conner J. M., Lauterborn J. C., Yan Q., Gall C. M. and Varon S. (1997) Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J. Neurosci. 17, 2295-2313.
18. Cuello A. C., Maysinger D. and Garofalo L. (1992) Trophic factor effects on cholinergic innervation in the cerebral cortex of the adult rat brain. Mol. Neurobiol. 6, 451-461.
19. De Simone R. and Aloe L. (1993) Influence of ethanol consumption on brain nerve growth factor and its target cells in developing and adult rodents. Ann. Ist Super. Sanita 29, 179-183.
20. De Witte P., Pinto E., Ansseau M. and Verbanck P. (2003) Alcohol and withdrawal: from animal research to clinical issues. Neurosci. Biobehav. Rev. 27, 189-197.
21. Ernfors P. and Persson H. (1991) Developmentally regulated expression of HDNF/NT-3 mRNA in rat spinal cord motoneurons and expression of BDNF mRNA in embryonic dorsal root ganglion. Eur. J. Neurosci. 3, 953-961.
22. Ernfors P., Wetmore C., Olson L. and Persson H. (1990) Identification of cells in rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family. Neuron 5, 511-526.
23. Fischer W. (1994) Nerve growth factor reverses spatial memory impairments in aged rats. Neurochem. Int. 25, 47-52.
24. Franke B., Bayatti N. and Engele J. (2000) Neurotrophins require distinct extracellular signals to promote the survival of CNS neurons in vitro. Exp. Neurol. 165, 125-135.
25. Fryer R. H., Kaplan D. R., Feinstein S. C., Radeke M. J., Grayson D. R. and Kromer L. F. (1996) Developmental and mature expression of full-length and truncated trkB receptors in the rat forebrain. J. Comp. Neurol. 374, 21-40.
26. Garofalo L. and Cuello A. C. (1994) Nerve growth factor and the monosialoganglioside GM1: analogous and different in vivo effects on biochemical, morphological, and behavioral parameters of adult cortically lesioned rats. Exp. Neurol. 125, 195-217.
27. Gericke C. A., Schulte-Herbrüggen O., Arendt T. and Hellweg R. (2006) Chronic alcohol intoxication in rats leads to a strong but transient increase in NGF levels in distinct brain regions. J. Neural. Trans. 113, 813-820.
28. Givens B., Williams J. M. and Gill T. M. (2000) Septohippocampal pathway as a site for the memory-impairing effects of ethanol. Hippocampus 10, 111-121.
29. Hallman L. E., Schofield B. R. and Lin C.-S. (1988) Dendritic morphology and axon collaterals of corticotectal, corticopontine, and callosal neurons in layer V of primary visual cortex of the hooded rat. J. Comp. Neurol. 272, 149-160.
30. Hamelink C., Hampson A., Wink D. A., Eiden L. E. and Eskay R. L. (2005) Comparison of cannabidiol, antioxidants, and diuretics in reversing binge ethanol-induced neurotoxicity. J. Pharmacol. Exp. Ther. 314, 780-788.
31. Hashimoto T., Volk D. W., Eggan S. M., Mirnics K., Pierri J. N., Sun Z., Sampson A. R. and Lewis D. A. (2003) Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J. Neurosci. 23, 6315-6326.
32. Hicks S. P. and D'Amato C. J. (1977) Locating corticospinal neurons by retrograde axonal transport of horseradish peroxidase. Exp. Neurol. 56, 410-420.
33. Howe C. L. and Mobley W. C. (2005) Long-distance retrograde neurotrophic signaling. Curr. Opin. Neurobiol. 15, 40-48.
34. Huang E. J. and Reichardt L. F. (2001) Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24, 677-736.
35. Huerta M. F. and Harting J. K. (1984) The mammalian superior colliculus: studies of its morphology and connections, in Comparative Neurology of the Optic Tectum (Venagas H., ed.), pp. 687-773. Plenum, New York.
36. Humpel C. and Weis C. (2002) Nerve growth factor and cholinergic CNS neurons studied in organotypic brain slices. Implication in Alzheimer's disease? J. Neural. Transm. Suppl. 62, 253-263.
37. Jacobs J. S. and Miller M. W. (1999) Expression of nerve growth factor, p75, and the high affinity neurotrophin receptors in the adult rat trigeminal system: evidence for multiple trophic support systems. J. Neurocytol. 28, 571-595.
38. Jakubowska-Dogru E. and Gumusbas U. (2005) Chronic intracerebroventricular NGF administration improves working memory in young adult memory deficient rats. Neurosci. Lett. 382, 45-50.
39. Jiang B., Akaneya Y., Hata Y. and Tsumoto T. (2003) Long-term depression is not induced by low-frequency stimulation in rat visual cortex in vivo: a possible preventing role of endogenous brain-derived neurotrophic factor. J. Neurosci. 23, 3761-3770.
40. Jiang X., Tian F., Mearow K., Okagaki P., Lipsky R. H. and Marini A. M. (2005) The excitoprotective effect of N-methyl-D-aspartate receptors is mediated by a brain-derived neurotrophic factor autocrine loop in cultured hippocampal neurons. J. Neurochem. 94, 713-722.
41. Klein R. L., Hirko A. C., Meyers C. A., Grimes J. R., Muzyczka N. and Meyer E. M. (2000) NGF gene transfer to intrinsic basal forebrain neurons increases cholinergic cell size and protects from age-related, spatial memory deficits in middle-aged rats. Brain Res. 875, 144-151.
42. Koh S., Oyler G. A. and Higgins G. A. (1989) Localization of nerve growth factor receptor messenger RNA and protein in the adult rat brain. Exp. Neurol. 106, 209-221.
43. Korsching S., Auburger G., Heumann R., Scott J. and Thoenen H. (1985) Levels of nerve growth factor and its mRNA in the central nervous system of the rat correlate with cholinergic innervation. EMBO J. 4, 1389-1393.
44. Larkfors L., Ebendal T., Whittemore S. R., Persson H., Hoffer B. and Olson L. (1987) Decreased level of nerve growth factor (NGF) and its messenger RNA in the aged rat brain. Brain Res. 427, 55-60.
45. Leong S. K. (1983) Localizing the corticospinal neurons by retrograde axonal transport of horseradish peroxidase. Exp. Neurol. 56, 410-420.
46. Lessmann V. (1998) Neurotrophin-dependent modulation of glutamatergic synaptic transmission in the mammalian CNS. Gen. Pharmacol. 31, 667-674.
47. Levi-Montalcini R. (1987) The nerve growth factor 35 years later. Science 237, 1154-1162.
48. Luo J. and Miller M. W. (1999) Platelet-derived growth factor-mediated signal transduction underlying astrocyte proliferation: site of ethanol action. J. Neurosci. 19, 10 014-10 025.
49. Luo J., West J. R. and Pantazis N. J. (1996) Ethanol exposure reduces the density of the low-affinity nerve growth factor receptor (p75) on pheochromocytoma (PC12) cells. Brain Res. 737, 34-44.
50. MacLennan A. J., Lee N. and Walker D. W. (1995) Chronic ethanol administration decreases brain-derived neurotrophic factor gene expression in the rat hippocampus. Neurosci. Lett. 197, 105-108.
51. Mallei A., Rabin S. J. and Mocchetti I. (2004) Autocrine regulation of nerve growth factor expression by trk receptors. J. Neurochem. 90, 1085-1093.
52. Melis F., Stancampiano R., Imperato A., Carta G. and Fadda F. (1996) Chronic ethanol consumption in rats: correlation between memory performance and hippocampal acetylcholine release in vivo. Neuroscience 74, 155-159.
53. Miller M. W. (1987) The origin of corticospinal projection neurons in rat. Exp. Brain Res. 67, 339-351.
54. Miller M. W. (1992) Circadian rhythm of cell proliferation in the telencephalic ventricular zone: effect of in utero exposure to ethanol. Brain Res. 595, 17-24.
55. Miller M. W. (2000) Expression of nerve growth factor and its receptors in the somatosensory-motor cortex of Macaca nemestrina. J. Neurocytol. 29, 453-469.
56. Miller M. W. (2004) Repeated episodic exposure to ethanol affects neurotrophin content in the forebrain of the mature rat. Exp. Neurol. 189, 173-181.
57. Miller M. W. and Mooney S. M. (2004) Chronic exposure to ethanol alters neurotrophin content in the basal forebrain-cortex system in the mature rat: effects on autocrine-paracrine mechanisms. J. Neurobiol. 60, 490-498.
58. Miller M. W. and Pitts A. F. (2000) Neurotrophin receptors in the somatosensory cortex of the mature rat: co-localization of p75, trk isoforms, and c-neu. Brain Res. 852, 355-366.
59. Miller M. W. and Rieck R. W. (1993) Effects of chronic ethanol administration on acetylcholinesterase activity in the somatosensory cortex and basal forebrain of the rat. Brain Res. 627, 104-112.
60. Miller R., King M. A., Heaton M. B. and Walker D. W. (2002) The effects of chronic ethanol consumption on neurotrophins and their receptors in the rat hippocampus and basal forebrain. Brain Res. 950, 137-147.
61. Miller M. W., Mooney S. M. and Middleton F. A. (2006) Transforming growth factor b1 and ethanol affect transcription of genes for cell adhesion proteins in B104 neuroblastoma cells. J. Neurochem. 97, 1182-1190.
62. Mooney S. M. and Miller M. W. (2001) Effects of prenatal exposure to ethanol on the expression of bcl-2, bax and caspase 3 in the developing rat cerebral cortex and thalamus. Brain Res. 911, 71-81.
63. Mufson E. J., Kroin J. S., Sendera T. J. and Sobreviela T. (1999) Distribution and retrograde transport of trophic factors in the central nervous system: functional implications for the treatment of neurodegenerative diseases. Prog. Neurobiol. 57, 451-484.
64. Nagy J., Muller F. and Laszlo L. (2001) Cytotoxic effect of alcohol-withdrawal on primary cultures of cortical neurones. Drug Alcohol Depend. 61, 155-162.
65. Niewiadomska G., Komorowski S. and Baksalerska-Pazera M. (2002) Amelioration of cholinergic neurons dysfunction in aged rats depends on the continuous supply of NGF. Neurobiol. Aging 23, 601-613.
66. Olton D., Markowska A., Voytko M. L., Givens B., Gorman L. and Wenk G. (1991) Basal forebrain cholinergic system: a functional analysis. Adv. Exp. Med. Biol. 295, 353-372.
67. Peters A. and Proskauer C. C. (1980) Synaptic relationships between a multipolar stellate cell and a pyramidal neuron in the rat visual cortex. A combined Golgi-electron microscope study. J. Neurocytol. 9, 163-183.
68. Pitts A. F. and Miller M. W. (1995) Expression of nerve growth factor, p75, and trk in the somatosensory and motor cortices of mature rats: evidence for local trophic support circuits. Somatosens. Mot. Res. 12, 329-342.
69. Pitts A. F. and Miller M. W. (2000) Expression of nerve growth factor, brain-derived neurotrophic factor, and neurotrophin-3 in the somatosensory cortex of the mature rat: co-expression with high-affinity neurotrophin receptors. J. Comp. Neurol. 418, 241-254.
70. Reichardt L. F. and Mobley W. C. (2004) Going the distance, or not, with neurotrophin signals. Cell 118, 141-143.
71. Resnicoff M., Rubini M., Baserga R. and Rubin R. (1994) Ethanol inhibits insulin-like growth factor-1-mediated signalling and proliferation of C6 rat glioblastoma cells. Lab. Invest. 71, 657-662.
72. Rubin R., Harrison R., Chen X. F., Corzitotto J., Hoek J. B. and Hallak H. (2004) Inhibition of insulin-like growth factor I receptor tyrosine kinase by ethanol. Biochem. Pharmacol. 68, 2009-2017.
73. Santin L. J., Rubio S., Begega A. and Arias J. L. (2000) Effects of chronic alcohol consumption on spatial reference and working memory tasks. Alcohol 20, 149-159.
74. Schecterson L. C. and Bothwell M. (1992) Novel roles for neurotrophins are suggested by BDNF and NT-3 mRNA expression in developing neurons. Neuron 9, 449-463.
75. Schofield B. R., Hallman L. E. and Lin C. S. (1987) Morphology of corticotectal cells in the primary visual cortex of hooded rats. J. Comp. Neurol. 261, 85-97.
76. Seabold G., Luo J. and Miller M. W. (1998) Effect of ethanol on neurotrophin-mediated cell survival and receptor expression in cortical neuronal cultures. Dev. Brain. Res. 128, 139-145.
77. Steigerwald E. S. and Miller M. W. (1997) 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, 1553-1559.
78. Suzuki T., Higgins P. J. and Crawford D. R. (2000) Control selection for RNA quantitation. BioTechniques 29, 332-337.
79. Tang N., He M., O'Riordan M. A., Farkas C., Buck K., Lemmon V. and Bearer C. F. (2006) Ethanol inhibits L1 cell adhesion molecule activation of mitogen-activated protein kinases. J. Neurochem. 96, 1480-1490.
80. Tapia-Arancibia L., Rage F., Givalois L., Dingeon P., Arancibia S. and Beauge F. (2001) Effects of alcohol on brain-derived neurotrophic factor mRNA expression in discrete regions of the rat hippocampus and hypothalamus. J. Neurosci. Res. 63, 200-208.
81. Thoenen H. (1995) Neurotrophins and neuronal plasticity. Science 270, 593-598.
82. Thomas M. P., Davis M. I., Monaghan D. T. and Morrisett R. A. (1998) Organotypic brain slice cultures for functional analysis of alcohol-related disorders: novel versus conventional preparations. Alcohol. Clin. Exp. Res. 22, 51-59.
83. Thomson A. M., West D. C., Hahn J. and Deuchars J. (1996) Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. J. Physiol. 496, 81-102.
84. Tonra J. R. (1999) Classical and novel directions in neurotrophin transport and research: anterograde transport of brain-derived neurotrophic factor by sensory neurons. Microsc. Res. Tech. 45, 225-232.
85. Victor M. (1994) Alcoholic dementia. Can. J. Neurol. Sci. 21, 88-99.
86. Victor M., Adams R. D. and Collins G. H. (1971) The Wernicke-Korsakoff syndrome. A clinical and pathological study of 245 patients, 82 with post-mortem examinations. Contemp. Neurol. Ser. 7, 1-206.
87. Walker D.W. and Freund G. (1971) Impairment of shuttle box avoidance learning following prolonged alcohol consumption in rats. Physiol. Behav. 7, 773-778.
88. Walker D. W. and Hunter B. E. (1978) Short-term memory impairment following chronic alcohol consumption in rats. Neuropsychologia 16, 545-553.
89. White A. M., Matthews D. B. and Best P. J. (2000) Ethanol, memory, and hippocampal function: a review of recent findings. Hippocampus 10, 88-93.
90. Williams L. R., Varon S., Peterson G. M., Wictorin K., Fischer W., Bjorklund A. and Gage F. H. (1986) Continuous infusion of nerve growth factor prevents basal forebrain neuronal death after fimbria fornix transection. Proc. Natl Acad. Sci. USA 83, 9231-9235.
91. Wise S. P. and Jones E. G. (1977) Cells of origin and terminal distribution of descending projections of the rat somatic sensory cortex. J. Comp. Neurol. 175, 129-158.
92. Zou L., Yuan X., Long Y., Shine H. D. and Yang K. (2002) Improvement of spatial learning and memory after adenovirus-mediated transfer of the nerve growth factor gene to aged rat brain. Hum. Gene Ther. 13, 2173-2184.