Nicotine-induced neuroprotection against N-methyl-D-aspartic acid or β-amyloid peptide occur through independent mechanisms distinguished by pro-inflammatory cytokines

Journal of Neurochemistry

Volumn 87, Issue 5, 2003, Pages 1125-1136

  Gahring, Lorise C ^a,b   Meyer, Erin L ^b   Rogers, Scott W ^a,b  

^a Education and Clinical Center   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Amyloid peptide; Cytokine; N methyl D aspartic acid; Neuroprotection; Nicotine; Tumor necrosis factor alpha

Indexed keywords

AMYLOID BETA PROTEIN[25-35]; CASPASE 6; CASPASE 8; CERAMIDE; CYTOKINE; N METHYL DEXTRO ASPARTIC ACID; NICOTINE; NICOTINIC ACETYLCHOLINE RECEPTOR ALPHA 4 BETA 2; NICOTINIC ACETYLCHOLINE RECEPTOR ALPHA 7; NICOTINIC RECEPTOR; RECEPTOR SUBTYPE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG MECHANISM; EMBRYO; ENZYME ACTIVITY; INFLAMMATION; MOUSE; NERVE CELL CULTURE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

AMYLOID BETA-PROTEIN; ANIMALS; CELLS, CULTURED; CERAMIDES; CEREBRAL CORTEX; CYTOKINES; CYTOPROTECTION; INFLAMMATION MEDIATORS; MICE; MICE, TRANSGENIC; MUTATION; N-METHYLASPARTATE; NEURONS; NEUROPROTECTIVE AGENTS; NF-KAPPA B; NICOTINE; PEPTIDE FRAGMENTS; RECEPTORS, NICOTINIC; SIGNAL TRANSDUCTION; TRANSGENES;

ANIMALIA; MUS MUSCULUS; NICOTIANA TABACUM;

EID: 0345305845     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.02074.x     Document Type: Article

References (67)

1. Albuquerque E. X., Pereira E. F., Mike A., Eisenberg H. M., Maelicke A. and Alkondon M. (2000) Neuronal nicotinic receptors in synaptic functions in humans and rats: physiological and clinical relevance. Behav. Brain Res. 113, 131-141.
2. Anisman H., Baines M. G., Berczi I. et al. (1996a) Neuroimmune mechanisms in health and disease: 2. Disease. CMAJ 155, 1075-1082.
3. Anisman H., Baines M. G., Berczi I. et al. (1996b) Neuroimmune mechanisms in health and disease: 1. Health. CMAJ 155, 867-874.
4. Arredondo J., Nguyen V. T., Chernyavsky A. I., Jolkovsky D. L., Pinkerton K. E. and Grando S. A. (2001) A receptor-mediated mechanism of nicotine toxicity in oral keratinocytes. Lab. Invest. 81, 1653-1668.
5. Arredondo J., Nguyen V. T., Chernyavsky A. I., Bercovich D., Orr-Urtreger A., Kummer W., Lips K., Vetter D. E. and Grando S. A. (2002) Central role of alpha7 nicotinic receptor in differentiation of the stratified squamous epithelium. J. Cell Biol. 159, 325-336.
6. Arredondo J., Hall L. L., Ndoye A., Nguyen V. T., Chernyavsky A. I., Bercovich D., Orr-Urtreger A., Beaudet A. L. and Grando S. A. (2003) Central role of fibroblast alpha3 nicotinic acetylcholine receptor in mediating cutaneous effects of nicotine. Lab. Invest. 83, 207-225.
7. Barger S. W., Horster D., Furukawa K., Goodman Y., Krieglstein J. and Mattson M. P. (1995) Tumor necrosis factors alpha and beta protect neurons against amyloid beta-peptide toxicity: evidence for involvement of kappa B-binding factor and attenuation of peroxide and Ca2+ accumulation. Proc. Natl Acad. Sci. USA 92, 9328-9332.
8. Bauer J., Rauschka H. and Lassmann H. (2001) Inflammation in the nervous system: the human perspective. Glia 36, 235-243.
9. Bernik T. R., Friedman S. G., Ochani M., DiRaimo R., Ulloa L., Yang H., Sudan S., Czura C. J., Ivanova S. M. and Tracey K. J. (2002) Pharmacological stimulation of the cholinergic antiinflammatory pathway. J. Exp. Med 195, 781-788.
10. Botchkina G. I., Meistrell M. E. 3rd, Botchkina I. L. and Tracey K. J. (1997) Expression of TNF and TNF receptors (p55 and p75) in the rat brain after focal cerebral ischemia. Mol. Med. 3, 765-781.
11. Britto L. R., Rogers S. W., Hamassaki-Britto D. E. and Duvoisin R. M. (1994) Nicotinic acetylcholine receptors in the ground squirrel retina: localization of the beta 4 subunit by immunohistochemistry and in situ hybridization. Vis. Neurosci. 11, 569-577.
12. Broide R. S. and Leslie F. M. (1999) The alpha7 nicotinic acetylcholine receptor in neuronal plasticity. Mol. Neurobiol. 20, 1-16.
13. Buisson B. and Bertrand D. (2001) Chronic exposure to nicotine upregulates the human (alpha)4(beta)2 nicotinic acetylcholine receptor function. J. Neurosci. 21, 1819-1829.
14. Buisson B. and Bertrand D. (2002) Nicotine addiction: the possible role of functional upregulation. Trends Pharmacol. Sci. 23, 130-136.
15. Carlson N. G., Gahring L. C., Twyman R. E. and Rogers S. W. (1997) Identification of amino acids in the glutamate receptor, GluR3, important for antibody-binding and receptor-specific activation. J. Biol. Chem. 272, 11 295-11 301.
16. Carlson N. G., Bacchi A., Rogers S. W. and Gahring L. C. (1998) Nicotine blocks TNF-alpha-mediated neuroprotection to NMDA by an alpha-bungarotoxin-sensitive pathway. J. Neurobiol. 35, 29-36.
17. Carlson N. G., Wieggel W. A., Chen J., Bacchi A., Rogers S. W. and Gahring L. C. (1999) Inflammatory cytokines IL-1alpha, IL-1beta, IL-6, and TNF-alpha impart neuroprotection to an excitotoxin through distinct pathways. J. Immunol. 163, 3963-3968.
18. Cauley K., Marks M., Gahring L. C. and Rogers S. W. (1996) Nicotinic receptor subunits alpha 3, alpha 4, and beta 2 and high affinity nicotine binding sites are expressed by P19 embryonal cells. J. Neurobiol. 30, 303-314.
19. Cheng B., Christakos S. and Mattson M. P. (1994) Tumor necrosis factors protect neurons against metabolic-excitotoxic insults and promote maintenance of calcium homeostasis. Neuron 12, 139-153.
20. Conroy W. G. and Berg D. K. (1998) Nicotinic receptor subtypes in the developing chick brain: appearance of a species containing the alpha4, beta2, and alpha5 gene products. Mol. Pharmacol. 53, 392-401.
21. Corringer P. J., Bertrand S., Bohler S., Edelstein S. J., Changeux J. P. and Bertrand D. (1998) Critical elements determining diversity in agonist binding and desensitization of neuronal nicotinic acetylcholine receptors. J. Neurosci. 18, 648-657.
22. Corringer P. J., Bertrand S., Galzi J. L., Devillers-Thiery A., Changeux J. P. and Bertrand D. (1999) Mutational analysis of the charge selectivity filter of the alpha7 nicotinic acetylcholine receptor. Neuron 22, 831-843.
23. Darnay B. G. and Aggarwal B. B. (1997) Early events in TNF signaling: a story of associations and dissociations. J. Leukoc. Biol. 61, 559-566.
24. Diaz-Villoslada P. and Oksenberg J. R. (1998) Chronic inflammatory diseases of the nervous system. Curr. Opin. Neurol. 11, 235-240.
25. Digicaylioglu M. and Lipton S. A. (2001) Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature 412, 641-647.
26. Drisdel R. C. and Green W. N. (2000) Neuronal alpha-bungarotoxin receptors are alpha7 subunit homomers. J. Neurosci. 20, 133-139.
27. 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 alpha 4 and beta 2 subunits and is up-regulated by chronic nicotine treatment. Mol. Pharmacol. 41, 31-37.
28. 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 alpha3-beta4, a novel subtype in the mammalian nervous system. J. Neurosci. 16, 7892-7901.
29. Francis M. M., Vazquez R. W., Papke R. L. and Oswald R. E. (2000) Subtype-selective inhibition of neuronal nicotinic acetylcholine receptors by cocaine is determined by the alpha4 and beta4 subunits. Mol. Pharmacol. 58, 109-119.
30. Gahring L. C., Carlson N. G., Kulmar R. A. and Rogers S. W. (1996) Neuronal expression of tumor necrosis factor alpha in the murine brain. Neuroimmunomodulation 3, 289-303.
31. Gahring L. C., Carlson N. G., Wieggel W. A., Howard J. and Rogers S. W. (1999) Alcohol blocks TNFalpha but not other cytokine-mediated neuroprotection to NMDA. Alcohol Clin. Exp. Res. 23, 1571-1579.
32. Giacobini E. (1992) Nicotine acetylcholine receptors in human cortex: Aging and Alzheimer's disease, in Biology of Nicotine (Lippiello P. M., Collins A. C., Gray A. C. and Robinson J. H., eds), pp. 183-215. Raven Press, New York.
33. Girod R., Crabtree G., Ernstrom G., Ramirez-Latorre J., McGehee D., Turner J. and Role L. (1999) Heteromeric complexes of alpha 5 and/or alpha 7 subunits. Effects of calcium and potential role in nicotine-induced presynaptic facilitation. Ann. NY Acad. Sci. 868, 578-590.
34. Goodman Y. and Mattson M. P. (1996) Ceramide protects hippocampal neurons against excitotoxic and oxidative insults, and amyloid beta-peptide toxicity. J. Neurochem. 66, 869-872.
35. Kellar K. J., Whitehouse P. J., Martino-Barrows A. M., Marcus K. and Price D. L. (1987) Muscarinic and nicotinic cholinergic binding sites in Alzheimer's disease cerebral cortex. Brain Res. 436, 62-68.
36. Kihara T., Shimohama S., Sawada H., Kimura J., Kume T., Kochiyama H., Maeda T. and Akaike A. (1997) Nicotinic receptor stimulation protects neurons against beta-amyloid toxicity. Ann. Neurol. 42, 159-163.
37. Kihara T., Shimohama S., Urushitani M., Sawada H., Kimura J., Kume T., Maeda T. and Akaike A. (1998) Stimulation of alpha4beta2 nicotinic acetylcholine receptors inhibits beta-amyloid toxicity. Brain Res. 792, 331-334.
38. Kihara T., Shimohama S., Sawada H., Honda K., Nakamizo T., Shibasaki H., Kume T. and Akaike A. (2001) Alpha 7 nicotinic receptor transduces signals to phosphatidylinositol 3-kinase to block A beta-amyloid-induced neurotoxicity. J. Biol. Chem. 276, 13 541-13 546.
39. Le Novere N., Grutter T. and Changeux J. P. (2002) Models of the extracellular domain of the nicotinic receptors and of agonist- and Ca2+-binding sites. Proc. Natl Acad. Sci. USA 99, 3210-3215.
40. Lentz T. L. (2000) Nicotine binding to native and substituted peptides comprising residues 188-207 of nicotinic acetylcholine receptor alpha1, alpha2, alpha3, alpha4, alpha5, and alpha7 subunits. Biochem. Biophys. Res. Commun. 268, 480-484.
41. Levin E. D. (2002) Nicotinic receptor subtypes and cognitive function. J. Neurobiol. 53, 633-640.
42. Lindstrom J. (1996) Neuronal nicotinic acetylcholine receptors. Ion Channels 4, 377-450.
43. Lindstrom J. (1997) Nicotinic acetylcholine receptors in health and disease. Mol. Neurobiol. 15, 193-222.
44. Mansvelder H. D. and McGehee D. S. (2002) Cellular and synaptic mechanisms of nicotine addiction. J. Neurobiol. 53, 606-617.
45. Marks M. J., Campbell S. M., Romm E. and Collins A. C. (1991) Genotype influences the development of tolerance to nicotine in the mouse. J. Pharmacol. Exp. Ther. 259, 392-402.
46. Mattson M. P., Goodman Y., Luo H., Fu W. and Furukawa K. (1997) Activation of NF-kappaB protects hippocampal neurons against oxidative stress-induced apoptosis: evidence for induction of manganese superoxide dismutase and suppression of peroxynitrite production and protein tyrosine nitration. J. Neurosci. Res. 49, 681-697.
47. McGeer P. L. and McGeer E. G. (2001) Inflammation, autotoxicity and Alzheimer disease. Neurobiol. Aging 22, 799-809.
48. Meda L., Baron P. and Scarlato G. (2001) Glial activation in Alzheimer's disease: the role of Abeta and its associated proteins. Neurobiol. Aging 22, 885-893.
49. Meyer E. L., Gahring L. C. and Rogers S. W. (2002) Nicotine preconditioning antagonizes activity-dependent caspase proteolysis of a glutamate receptor. J. Biol. Chem. 277, 10 869-10 875.
50. Mirzoian A. and Luetje C. W. (2002) Modulation of neuronal nicotinic acetylcholine receptors by mercury. J. Pharmacol. Exp. Ther. 302, 560-567.
51. Newhouse P. A., Potter A. and Levin E. D. (1997) Nicotinic system involvement in Alzheimer's and Parkinson's diseases. Implications for therapeutics. Drugs Aging 11, 206-228.
52. Pereira E. F., Hilmas C., Santos M. D., Alkondon M., Maelicke A. and Albuquerque E. X. (2002) Unconventional ligands and modulators of nicotinic receptors. J. Neurobiol. 53, 479-500.
53. Quik M. and Kulak J. M. (2002) Nicotine and nicotinic receptors; relevance to Parkinson's disease. Neurotoxicology 23, 581-594.
54. Richardson C. E., Morgan J. M., Jasani B., Green J. T., Rhodes J., Williams G. T., Lindstrom J., Wonnacott S., Peel S. and Thomas G. A. (2003) Effect of smoking and transdermal nicotine on colonic nicotinic acetylcholine receptors in ulcerative colitis. Qjm 96, 57-65.
55. Rogers S. W., Mandelzys A., Deneris E. S., Cooper E. and Heinemann S. (1992) The expression of nicotinic acetylcholine receptors by PC12 cells treated with NGF. J. Neurosci. 12, 4611-4623.
56. Rogers S. W., Gahring L. C., Collins A. C. and Marks M. (1998) Age-related changes in neuronal nicotinic acetylcholine receptor subunit alpha4 expression are modified by long-term nicotine administration. J. Neurosci. 18, 4825-4832.
57. Rogers S. W., Gregori N. Z., Carlson N., Gahring L. C. and Noble M. (2001) Neuronal nicotinic acetylcholine receptor expression by O2A/oligodendrocyte progenitor cells. Glia 33, 306-313.
58. Ruvolo P. P. (2001) Ceramide regulates cellular homeostasis via diverse stress signaling pathways. Leukemia 15, 1153-1160.
59. Sabbagh M. N., Lukas R. J., Sparks D. L. and Reid R. T. (2002) The nicotinic acetylcholine receptor, smoking, and Alzheimer's disease. J. Alzheimers Dis. 4, 317-325.
60. Sugano N., Shimada K., Ito K. and Murai S. (1998) Nicotine inhibits the production of inflammatory mediators in U937 cells through modulation of nuclear factor-kappaB activation. Biochem. Biophys. Res. Commun. 252, 25-28.
61. Wajant H., Pfizenmaier K. and Scheurich P. (2003) Tumor necrosis factor signaling. Cell Death Differ. 10, 45-65.
62. Wang H. Yu M. Ochani M. et al. (2003) Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421, 384-388.
63. Wang N., Orr-Urtreger A., Chapman J., Rabinowitz R., Nachman R. and Korczyn A. D. (2002) Autonomic function in mice lacking alpha5 neuronal nicotinic acetylcholine receptor subunit. J. Physiol. 542, 347-354.
64. Wang Y., Pereira E. F., Maus A. D., Ostlie N. S., Navaneetham D., Lei S., Albuquerque E. X. and Conti-Fine B. M. (2001) Humar bronchial epithelial and endothelial cells express alpha7 nicotinic acetylcholine receptors. Mol. Pharmacol. 60, 1201-1209.
65. Whitehouse P. J. (1997) Genesis of Alzheimer's disease. Neurology 48 S2-S7.
66. Zia S., Ndoye A., Nguyen V. T. and Grando S. A. (1997) Nicotine enhances expression of the alpha 3, alpha 4, alpha 5, and alpha 7 nicotinic receptors modulating calcium metabolism and regulating adhesion and motility of respiratory epithelial cells. Res. Commun. Mol. Pathol. Pharmacol. 97, 243-262.
67. Zwart R., Van Kleef R. G. and Vijverberg H. P. (1999) Physostigmine and atropine potentiate and inhibit neuronal alpha 4 beta 4 nicotinic receptors. Ann. NY Acad. Sci. 868, 636-639.