Nicotine exposure during a critical period of development leads to persistent changes in nicotinic acetylcholine receptors of adult rat brain

Journal of Neurochemistry

Volumn 70, Issue 2, 1998, Pages 752-762

  Miao, H ^a   Liu, C ^a,b   Bishop, K ^a   Gong, Z H ^a,c   Nordberg, A ^a   Zhang, X ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^c Beijing Institute of Toxicology and Pharmacology   (China)

Author keywords

Development; Nicotine treatment; Nicotinic acetylcholine receptor; Receptor binding sites; Subunit mRNA

Indexed keywords

ALPHA BUNGAROTOXIN; EPIBATIDINE; MESSENGER RNA; NICOTINE; NICOTINIC AGENT; NICOTINIC RECEPTOR; TRITIUM;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; BRAIN DEVELOPMENT; BRAIN TISSUE; CIGARETTE SMOKING; CONTROLLED STUDY; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; RECEPTOR BINDING; SUBCUTANEOUS DRUG ADMINISTRATION;

ANIMALIA; TRITIUM;

EID: 0031890761     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1998.70020752.x     Document Type: Article

References (72)

1. Badio B. and Daly J. W. (1994) Epibatidine, a potent analgesic and nicotinic agonist. Mol. Pharmacol. 45, 563-569.
2. Bartus R. T., Dean R. L. III, Beer B., and Lippa A. S. (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217, 408-417.
3. Beani L., Bianchi C., Ferraro L., Nilsson L., Nordberg A., Romanelli L., Spalluto P., Sundwall A., and Tanganelli S. (1989) Effect of nicotine on the release of acetylcholine and amino acids in the brain. Prog. Brain Res. 79, 149-155.
4. Bencherif M., Fowler K., Lukas R. J., and Lippiello P. M. (1995) Mechanisms of up-regulation of neuronal nicotinic acetylcholine receptors in clonal cell lines and primary cultures of fetal rat brain. J. Pharmacol. Exp. Ther. 275, 987-994.
5. Bhat R. V., Turner S. L., Selvaag S. R., Marks M. J., and Collins A. C. (1991) Regulation of brain nicotinic receptors by chronic-agonist infusion. J. Neurochem. 56, 1932-1939.
6. Broide R. S., O'Connor L. T., Smith M. A., Smith J. A. M., and Leslie F. M. (1995) Developmental expression of α7 neuronal nicotinic receptor messenger RNA in rat sensory cortex and thalamus. Neuroscience 67, 83-94.
7. Broide R. S., Robertson R. T., and Leslie F. M. (1996) Regulation of α7 nicotinic acetylcholine receptors in the developing rat somatosensory cortex by thalamocortical afferents. J. Neurosci. 16, 2956-2971.
8. Chan J. and Quik M. (1993) A role for the nicotinic α-bungarotoxin receptor in neurite outgrowth in PC12 cells. Neuroscience 56, 441-451.
9. Chomczynski P. and Sacchi N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
10. Cimino M., Marini P., Colombo S., Andena M., Cattabeni F., Fornasari D., and Clementi F. (1995) Expression of neuronal acetylcholine nicotinic receptor α4 and β2 subunits during postnatal development of the rat brain. J. Neural Transm. [Gen. Sect.] 100, 77-92.
11. Clarke P. B. S. (1992) The fall and rise of neuronal α-bungarotoxin binding proteins. Trends Pharmacol. Sci. 13, 407-413.
12. Clos J., Ghandour S., Eberhart R., Vincendon G., and Gombos G. (1989) The cholinergic system in developing cerebellum: comparative study of normal, hypothyroid and underfed rats. Dev. Neurosci. 11, 188-204.
13. Couturier S., Bertrand D., Matter J. M., Hernandez M. C., Bertrand S., Millar N., Valera S., Barkes T., and Ballivet M. (1990) A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-BTX. Neuron 5, 847-856.
14. Dahlström A., Lundell B., Curvall M., and Thapeper L. (1990) Nicotine and cotinine concentrations in the nursing mother and her infant. Acta Paediatr. Scand. 79, 142-147.
15. Daly J. W., Brown G. B., Mensah-Dwumah M., and Myers C. W. (1978) Classification of skin alkaloids from neotropical poisondart frogs (Dendrobatidae). Toxicon 16, 163-188.
16. Davison A. N. and Dobbing J. (1986) Applied Neurochemistry, pp. 178-221, 253-316. Blackwell, Oxford.
17. Didier M., Bix G., Berman S. A., and Bursztajn S. (1995) Expression of the α4 neuronal nicotinic acetylcholine receptor subunit in the developing mouse hippocampus. Int. J. Dev. Neurosci. 13, 703-713.
18. Falkeborn Y., Larsson C., Nordberg A., and Slanina P. (1983) A comparison of the regional ontogenesis of nicotine-and muscarine-like binding sites in mouse brain. Int. J. Dev. Neurosci. 1, 289-296.
19. Fibiger H. C. (1991) Cholinergic mechanisms in learning, memory and dementia; a review of recent evidence. Trends Neurosci. 14, 220-223.
20. Fiedler E. P., Marks M. J., and Collins A. C. (1990) Postnatal development of two nicotinic cholinergic receptors in seven mouse brain regions. Int. J. Dev. Neurosci. 8, 533-540.
21. Flores C. M., Rogers S. W., Pabreza L. A., Wolfe B. B., and Kellar K. J. (1992) A subtype of nicotinic cholinergic receptor in rat brain is composed of α4 and β2 subunits and is up-regulated by chronic nicotine treatment. Mol. Pharmacol. 41, 31-37.
22. Flores C. M., DeCamp R. M., Kilo S., Rogers S. W., and Hargreaves K. M. (1996) Neuronal nicotinic receptor expression in sensory neurons of the rat trigeminal ganglion: demonstration of α3β4, a novel subtype in the mammalian nervous system. J. Neurosci. 16, 7892-7901.
23. Gould E., Woolf N. J., and Butcher L. L. (1991) Postnatal development of cholinergic neurons in the rat: I. Forebrain. Brain Res. Bull. 27, 767-789.
24. Halvorsen S. W. and Berg D. K. (1990) Subunit composition of nicotinic acetylcholine receptors from chick ciliary ganglia. J. Neurosci. 10, 1711-1718.
25. 3H] nicotine. Acta. Physiol. Scand. 132, 1-14.
26. 3H]epibatidine binding to nicotinic cholinergic receptors in rat and human brain. Mol. Pharmacol. 48, 280-287.
27. Huang L. M. (1989) Origin of thalamically projecting somatosensory relay neurons in the immature rat. Brain Res. 495, 108-114.
28. Jakubowski M., Blum M., and Roberts J. L. (1991) Postnatal development of gonadotropin-releasing hormone and cyclophilin gene expression in the female and male rat brain. Endocrinology 128, 2702-2708.
29. 3H]nicotine binding in the human brainstem. Neuroscience 55, 1127-1138.
30. Knopman D. S. and Nissen M. J. (1987) Implicit learning in patients with probable Alzheimer's disease. Neurology 37, 784-788.
31. Kobayashi J., Inman O., Buno W., and Himwich H. E. (1963) A multidisciplinary study of changes in mouse brain with age. Res. Adv. Psychiatry 5, 239-298.
32. Kostovic I. and Rakic P. (1990) Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J. Comp. Neurol. 297, 441-470.
33. Kristt D. A. and Molliver M. E. (1976) Synapses in newborn rat cerebral cortex: a quantitative ultrastructural study. Brain Res. 108, 180-186.
34. 3H]acetylcholine to nicotinic receptors. Neuropharmacology 24, 527-531.
35. Larsson C. and Nordberg A. (1985) Comparative analysis of nicotine-like receptor-ligand interactions in rodent brain homogenate. J. Neurochem. 45, 24-31.
36. 3H] nicotine binding in developing mouse brain. Int. J. Dev. Neurosci. 3, 667-671.
37. Lèna C., Changeux J.-P., and Mulle C. (1993) Evidence for preterminal nicotinic receptors on GABAergic axons in the rat interpeduncular nucleus. J. Neurosci. 13, 2680-2688.
38. Le Novère N., Zoli M., and Changeux J.-P. (1996) Neuronal nicotinic receptor α6 subunit mRNA is selectively concentrated in catecholaminergic nuclei of the rat brain. Eur. J. Neurosci. 8, 2428-2439.
39. Levin E. D., Wilkerson A., Jones J. P., Christopher N. C., and Briggs S. J. (1996) Prenatal nicotine effects on memory in rats: pharmacological and behavioural challenges. Dev. Brain Res. 97, 207-215.
40. Lichtensteiger W., Ribary U., Schlumpf M., Odermatt B., and Widmer H. R. (1988) Prenatal adverse effects of nicotine on the developing brain. Prog. Brain Res. 73, 137-157.
41. Lipton S. A., Frosch M. P., Phillips M. D., Tauck D. L., and Aizenman E. (1988) Nicotinic antagonists enhance process outgrowth by rat retinal ganglion cells in culture. Science 239, 1293-1296.
42. Listerud M., Bressaard A. B., Devay P., Colman D. R., and Role L. W. (1991) Functional contribution of neuronal AChR subunits revealed by antisense oligonucleotides. Science 254, 1518-1521.
43. Liu C., Nordberg A., and Zhang X. (1996) Differential co-expression of nicotinic acetylcholine receptor α4 and β2 subunit genes in various regions of rat brain. Neuroreport 7, 1645-1649.
44. Lucidi-Phillipi C. A. and Gage F. H. (1993) The neurotrophic hypothesis and the cholinergic basal forebrain projection. Prog. Brain Res. 98, 241-249.
45. Marks M. J., Stitzel J. A., and Collins A. C. (1985) Time course study of the effects of chronic nicotine infusion on drug response and brain receptors. J. Pharmacol. Exp. Ther. 235, 619-628.
46. Marks M. J., Pauly J. R., Gross S. D., Deneris E. S., Hermans-Borgmeyer I., Heinemann S. F., and Collins A. C. (1992) Nicotine binding and nicotinic receptor subunit RNA after chronic nicotine treatment. J. Neurosci. 12, 2765-2784.
47. 3H]nicotine binding sites in rat brain regions: an autoradiographic study. Dev. Brain Res. 68, 163-174.
48. Nordberg A., Zhang X., Fredriksson A., and Eriksson P. (1991) Neonatal nicotine exposure induces permanent changes in brain nicotinic receptors and behaviour in adult mice. Dev. Brain Res. 63, 201-207.
49. Ostermann C. H., Grunwald J., Wevers A., Lorke D. E., Reinhardt S., Maelicke A., and Schröder H. (1995) Cellular expression of α4 subunit mRNA of the nicotinic acetylcholine receptor in the developing rat telencephalon. Neurosci. Lett. 192, 21-24.
50. Peng X., Gerzanich V., Anand R., Whiting P. J., and Lindstrom J. (1994) Nicotine-induced increase in neuronal nicotinic receptors results from a decrease in the rate of receptor turnover. Mol. Pharmacol 46, 523-530.
51. 3H] Epibatidine labels nicotinic receptors in rat brain: an autoradiographic study. J. Pharmacol. Exp. Ther. 275, 1030-1034.
52. Picciotto M. R., Zoli M., Lèna C., Bessis A., Lallemand Y., Le Novère N., Vincent P., Merlo Pich E., Brûlet P., and Changeux J.-P. (1995) Abnormal avoidance learning in mice lacking functional high-affinity nicotine receptors in the brain. Nature 380, 347-351.
53. Pugh P. C. and Berg D. K. (1994) Neuronal acetylcholine receptors that bind α-bungarotoxin mediate neunte retraction in a calcium-dependent manner. J. Neurosci. 14, 889-896.
54. Romanelli L., Öhman B., Adem A., and Nordberg A. (1988) Subchronic treatment of rats with nicotine: interconversion of nicotine receptor subtypes in brain. Eur. J. Pharmacol. 148, 289-291.
55. Rylander R., Pershagen G., Curvall M., and Kazemi-Vala E. (1990) Exposure of environmental tobacco smoke and urinary excretion of cotinine and nicotine in children. Acta Paediatr. Scand. 78, 449-450.
56. Sargent P. B. (1993) The diversity of neuronal nicotinic acetylcholine receptors. Annu. Rev. Neurosci. 16, 403-443.
57. Séguéla P., Wadiche J., Dineley-Miller K., Dani J. A., and Patrick J. W. (1993) Molecular cloning, functional properties, and distribution of rat brain α7: a nicotinic cation channel highly permeable to calcium. J. Neurosci. 13, 596-604.
58. 3H]nicotine binding sites in brain regions of rats exposed to nicotine prenatally via maternal injections or infusion. J. Pharmacol. Exp. Ther. 242, 232-237.
59. Sorenson C. A., Raskin L. A., and Suh Y. (1991) The effects of prenatal nicotine on radial-arm maze performance in rats. Pharmacol. Biochem. Behav. 40, 991-993.
60. Stanfield B. B. and Cowan W. M. (1988) The development of the hippocampal region, in Cerebral Cortex: Development and Maturation of Cerebral Cortex, Vol. 7 (Peters A. and Jones E. G., eds), pp. 91-122. Plenum Press, New York.
61. Thai L. J., Gilbertson E., Armstrong D. M., and Gage F. H. (1992) Development of the basal forebrain cholinergic system: phenotype expression prior to target innervation. Neurobiol. Aging 13, 67-72.
62. Wada E., Wada K., Boulter J., Deneris E., Heinemann S., Patrick J., and Swanson L. W. (1989) Distribution of alpha2, alpha3, alpha4, and beta2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: a hybridization histochemical study in the rat. J. Comp. Neurol. 284, 314-335.
63. Westfall T. C., Mereu G., Vickery L., Perry H., Haes L., and Yoon K. P. (1989) Regulation by nicotine of midbrain dopamine neurons. Prog. Brain Res. 79, 173-185.
64. Whiting P. and Lindstrom J. (1988) Characterization of bovine and human neuronal nicotinic acetylcholine receptors using monoclonal antibodies. J. Neurosci. 8, 3395-3404.
65. Wonnacott S. (1990) Characterization of nicotine receptor sites in the brain, in Nicotine Psychopharmacology (Wonnacott S., Russell M. A. H., and Stolarman I. P., eds). pp. 226-277. Oxford University Press, Oxford.
66. Yanai J., Pick C. G., Rogel-Fuchs Y., and Zahalka E. A. (1991) Alteration in septohippocampal cholinergic receptors and related behavior after prenatal exposure to nicotine, in Effects of Nicotine on Biological Systems (Adlkofer F. and Thurau K., eds). pp. 401-406. Birkhäuser. Boston.
67. Yanai J., Pick C. G., Rogel-Fuchs Y., and Zahalka E. A. (1992) Alterations in hippocampal cholinergic receptors and hippocampal behaviors after early exposure to nicotine. Brain Res. Bull. 29, 363-368.
68. Zhang X., Wahlström G., and Nordberg A. (1990) Influence of development and aging on nicotinic receptor subtypes in rodent brain. Int. J. Dev. Neurosci. 8, 715-721.
69. Zhang X., Gong Z.-H., and Nordberg A. (1994) Effects of chronic treatments with (+)-and (-)-nicotine on nicotinic acetylcholine receptors and N-methyl-D-aspartate receptors in rat brain. Brain Res. 644, 32-39.
70. Zhang X., Gong Z.-H., Hellström-Lindahl E., and Nordberg A. (1995) Regulation of α4β2 nicotinic acetylcholine receptors in M10 cells following treatment with nicotinic agents. Neuroreport 6, 313-317.
71. Zheng J. Q., Felder M., Connor J. A., and Poo M. (1994) Turning of nerve growth cones induced by neurotransmitters. Nature 368, 140-143.
72. Zoli M., Le Novère N., Hill J. A. Jr., and Changeux J.-P. (1995) Developmental regulation of nicotinic ACh receptor subunit mRNAs in the rat central and peripheral nervous systems. J. Neurosci. 15, 1912-1939.