Impact of sustained exposure to β-amyloid on calcium homeostasis and neuronal integrity in model nerve cell system expressing α4β2 Nicotinic acetylcholine receptors

Journal of Biological Chemistry

Volumn 288, Issue 16, 2013, Pages 11175-11190

  Arora, Komal ^a   Alfulaij, Naghum ^a   Higa, Jason K ^a   Panee, Jun ^a   Nichols, Robert A ^a  

^a UNIVERSITY OF HAWAII   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER DISEASE; CALCIUM HOMEOSTASIS; CELL SYSTEM; CELLULAR TOXICITIES; NICOTINIC ACETYLCHOLINE RECEPTORS; NICOTINIC RECEPTOR; TOXIC ACTION;

NEURONS;

GLYCOPROTEINS;

AMYLOID BETA PROTEIN[1-42]; CALCIUM ION; NICOTINE; NICOTINIC RECEPTOR ALPHA4BETA2; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM HOMEOSTASIS; CELL NUCLEUS; CONTROLLED STUDY; ENDOCYTOSIS; MITOCHONDRION; NERVE CELL; NERVE CELL CULTURE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; CALCIUM; CELL LINE, TUMOR; HOMEOSTASIS; HUMANS; MICE; MODELS, BIOLOGICAL; NEURONS; PEPTIDE FRAGMENTS; REACTIVE OXYGEN SPECIES; RECEPTORS, NICOTINIC;

EID: 84876520365     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.453746     Document Type: Article

References (57)

1. 1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U.S.A. 95, 6448-6453.
2. Walsh, D. M., and Selkoe, D. J. (2007) Aβ oligomers. A decade of discovery. J. Neurochem. 101, 1172-1184.
3. Puzzo, D., Privitera, L., Leznik, E., Fà, M., Staniszewski, A., Palmeri, A., and Arancio, O. (2008) Picomolar amyloid-β positively modulates synaptic plasticity and memory in hippocampus. J. Neurosci. 28, 14537-14545.
4. Puzzo, D., Privitera, L., Fa', M., Staniszewski, A., Hashimoto, G., Aziz, F., Sakurai, M., Ribe, E. M., Troy, C. M., Mercken, M., Jung, S. S., Palmeri, A., and Arancio, O. (2011) Endogenous amyloid-β is necessary for hippocampal synaptic plasticity and memory. Ann. Neurol. 69, 819-830.
5. Cirrito, J. R., Yamada, K. A., Finn, M. B., Sloviter, R. S., Balesand K. R., May, P. C, Schoepp, D. D., Paul, S. M., Mennerick, S., and Holtzman, D. M. (2005) Synaptic activity regulates interstitial fluid amyloid-β levels in vivo. Neuron 48, 913-922.
6. Cirrito, J. R., Kang, J. E., Lee, J., Stewart, F. R., Verges, D. K., Silverio, L. M., Bu, G., Mennerick, S., and Holtzman, D. M. (2008) Endocytosis is required for synaptic activity-dependent release of amyloid-β in vivo. Neuron 58, 42-51.
7. Religa, D., Laudon, H., Styczynska, M., Winblad, B., Näslund, J., and Haroutunian, V. (2003) Amyloid β pathology in Alzheimer's disease and schizophrenia. Am. J. Psychiatry 160, 867-872.
8. Lazarov, O., Lee, M., Peterson, D. A., and Sisodia, S. S. (2002) Evidence that synaptically released β-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. J. Neurosci. 22, 9785-9793.
9. Patel, A. N., and Jhamandas, J. H. (2012) Neuronal receptors as targets for the action of amyloid-β protein (Aβ) in the brain. Expert Rev. Mol. Med. 14, e2.
10. Dani, J. A., and Bertrand, D. (2007) Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu. Rev. Pharmacol. Toxicol. 47, 699-729.
11. McGehee, D. S., and Role, L. W. (1995) Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons. Annu. Rev. Physiol. 57, 521-546.
12. Dougherty, J. J., Wu, J., and Nichols, R. A. (2003) β-Amyloid regulation of presynaptic nicotinic receptors in rat hippocampus and neocortex. J. Neurosci. 23, 6740-6747.
13. Wu, J., Khan, G. M., and Nichols, R. A. (2007) Dopamine release in prefrontal cortex in response to β-amyloid activation of α7* nicotinic receptors. Brain Res. 1182, 82-89.
14. Mehta, T. K., Dougherty, J. J., Wu, J., Choi, C. H., Khan, G. M., and Nichols, R. A. (2009) Defining pre-synaptic nicotinic receptors regulated by β amyloid in mouse cortex and hippocampus with receptor null mutants. J. Neurochem. 109, 1452-1458.
15. Tong, M., Arora, K., White, M. M., and Nichols, R. A. (2011) Role of key aromatic residues in the ligand-binding domain of α7 nicotinic receptors in the agonist action of β-amyloid. J. Biol. Chem. 286, 34373-34381.
16. Flores, C. M., Rogers, S. W., Pabreza, L. A., Wolfe, B. B., and Kellar, K. J. (1992) A subtype of the 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.
17. Zhang, X., Gong, Z.-H., and Nordberg, A. (1994) Effects of chronic treatment with (+)- and (-)-nicotine on nicotinic acetylcholine receptors and N-methyl-D-aspartate receptors in rat brain. Brain Res. 644, 32-39.
18. 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.
19. 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.
20. Hsu, Y. N., Amin, J., Weiss, D. S., and Wecker, L. (1996) Sustained nicotine exposure differentially affects α3β2 and α4β2 neuronal nicotinic receptors expressed in Xenopus oocytes. J. Neurochem. 66, 667-675.
21. Breese, C. R., Marks, M. J., Logel, J., Adams, C. E., Sullivan, B., Collins, A. C., and Leonard, S. (1997) Effect of smoking history on [3H]nicotine binding in human postmortem brain. J. Pharmacol. Exp. Ther. 282, 7-13.
22. Court, J. A., Lloyd, S., Thomas, N., Piggott, M. A., Marshall, E. F., Morris, C. M., Lamb, H., Perry, R. H., Johnson, M., and Perry, E. K. (1998) Dopamine and nicotinic receptor binding and the levels of dopamine and homovanillic acid in human brain related to tobacco use. Neuroscience 87, 63-78.
23. Staley, J. K., Krishnan-Sarin, S., Cosgrove, K. P., Krantzler, E., Frohlich, E., Perry, E., Dubin, J. A., Estok, K., Brenner, E., Baldwin, R. M., Tamagnan, G. D., Seibyl, J. P., Jatlow, P., Picciotto, M. R., London, E. D., O'Malley, S., and van Dyck, C. H. (2006) Human tobacco smokers in early abstinence have higher levels of β2* nicotinic acetylcholine receptors than nonsmokers. J. Neurosci. 26, 8707-8714.
24. Mukhin, A. G., Kimes, A. S., Chefer, S. I., Matochik, J. A., Contoreggi, C. S., Horti, A. G., Vaupel, D. B., Pavlova, O., and Stein, E. A. (2008) Greater nicotinic acetylcholine receptor density in smokers than in nonsmokers.A PET study with 2-18F-FA-85380. J. Nucl. Med. 49, 1628-1635.
25. Albuquerque, E. X., Pereira, E. F., Alkondon, M., and Rogers, S. W. (2009) Mammalian nicotinic acetylcholine receptors. From structure to function. Physiol. Rev. 89, 73-120.
26. Xiao, C., Nashmi, R., McKinney, S., Cai, H., McIntosh, J. M., and Lester, H. A. (2009) Chronic nicotine selectively enhances α4β2* nicotinic acetylcholine receptors in the nigrostriatal dopamine pathway. J. Neurosci. 29, 12428-12439.
27. Stenmark, H., Vitale, G., Ullrich, O., and Zerial, M. (1995) Rabaptin-5 is a direct effector of the small GTPase Rab5 in endocytic membrane fusion. Cell 83, 423-432.
28. Vitale, G., Rybin, V., Christoforidis, S., Thornqvist, P., McCaffrey, M., Stenmark, H., and Zerial, M. (1998) Distinct Rab-binding domains mediate the interaction of Rabaptin-5 with GTP-bound Rab4 and Rab5. EMBO J. 17, 1941-1951.
29. Sönnichsen, B., De Renzis, S., Nielsen, E., Rietdorf, J., and Zerial, M. (2000) Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol. 149, 901-914.
30. Zerial, M., and McBride, H. (2001) Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107-117.
31. Tillement, L., Lecanu, L., and Papadopoulos, V. (2011) Alzheimer's disease. Effects of β-amyloid on mitochondria. Mitochondrion 11, 13-21.
32. Thies, E., and Mandelkow, E. M. (2007) Missorting of tau in neurons causes degeneration of synapses that can be rescued by the kinase MARK2/Par-1. J. Neurosci. 27, 2896-2907.
33. Hirai, K., Aliev, G., Nunomura, A., Fujioka, H., Russell, R. L., Atwood, C. S., Johnson, A. B., Kress, Y., Vinters, H. V., Tabaton, M., Shimohama, S., Cash, A. D., Siedlak, S. L., Harris, P. L., Jones, P. K., Petersen, R. B., Perry, G., and Smith, M. A. (2001) Mitochondrial abnormalities in Alzheimer's disease. J. Neurosci. 21, 3017-3023.
34. Iijima-Ando, K., Hearn, S. A., Shenton, C., Gatt, A., and Zhao, L. (2009) Mitochondrial mislocalization underlies Aβ42-induced neuronal dysfunction in a Drosophila model of Alzheimer's disease. PLoS One 4, e8310.
35. Zhao, X. L., Wang, W. A., Tan, J. X., Huang, J. K., Zhang, X., Zhang, B. Z., Wang, Y. H., YangCheng, H. Y., Zhu, H. L., Sun, X. J., and Huang, F. D. (2010) Expression of β-amyloid induced age-dependent presynaptic and axonal changes in Drosophila. J. Neurosci. 30, 1512-1522.
36. + elevation, missorting of endogenous tau into dendrites, tau phosphorylation, and destruction of microtubules and spines. J. Neurosci. 30, 11938-11950.
37. Khan, G. M., Tong, M., Jhun, M., Arora, K., and Nichols, R. A. (2010) β-Amyloid activates presynaptic α7 nicotinic acetylcholine receptors reconstituted into a model nerve cell system. Involvement of lipid rafts. Eur. J. Neurosci. 31, 788-796.
38. Lukyanetz, E. A. (1998) Diversity and properties of calcium channel types in NG108015 hybrid cells. Neuroscience 87, 265-274.
39. Fried, G., and Han, H. Q. (1995) Increase in synaptic vesicle proteins in synapsin-transfected NG108-15 cells. A subcellular fractionation study. Synapse 20, 44-53.
40. Nelson, P., Christian, C., Nirenberg, M. (1976) Synapse formation between clonal neuroblastoma X glioma hybrid cells and striated muscle cells. Proc. Natl. Acad. Sci. U.S.A. 73, 123-127.
41. + exchange. J. Biol. Chem. 282, 36102-36111.
42. + responses in isolated nerve terminals. Neurochem. Res. 33, 1106-1112.
43. Reddy, P. H. (2009) Amyloid β, mitochondrial structural and functional dynamics in Alzheimer's disease. Exp. Neurol. 218, 286-292.
44. Wang, X., Su, B., Zheng, L., Perry, G., Smith, M. A., and Zhu, X. (2009) The role of abnormal mitochondrial dynamics in the pathogenesis of Alzheimer's disease. J. Neurochem. 109, 153-159.
45. Fu, W., and Jhamandas, J. H. (2003) β-Amyloid peptide activates non-α7 nicotinic acetylcholine receptors in rat basal forebrain neurons. J. Neurophysiol. 90, 3130-3136.
46. Chin, J. H., Ma, L., MacTavish, D., and Jhamandas, J. H. (2007) Amyloid β protein modulates glutamate-mediated neurotransmission in the rat basal forebrain. Involvement of presynaptic neuronal nicotinic acetylcholine and metabotropic glutamate receptors. J. Neurosci. 27, 9262-9269.
47. Buisson, B., and Bertrand, D. (2002) Nicotine addiction. The possible role of functional up-regulation. Trends Pharmacol. Sci. 23, 130-136.
48. Nashmi, R., Dickinson, M. E., McKinney, S., Jareb, M., Labarca, C., Fraser, S. E., Lester, H. A. (2003) Assembly of α4β2 nicotinic acetylcholine receptors assessed with functional fluorescently labeled subunits. Effects of localization, trafficking, and nicotine-induced up-regulation in clonal mammalian cells and in cultured midbrain neurons. J. Neurosci. 23, 11554-11567.
49. Perry, D. C., Dávila-García, M. I., Stockmeier, C. A., and Kellar, K. J. (1999) Increased nicotinic receptors in brains from smokers. Membrane binding and autoradiography studies. J. Pharmacol. Exp. Ther. 289, 1545-1552.
50. Vallejo, Y. F., Buisson, B., Bertrand, D., and Green, W. N. (2005) Chronic nicotine exposure up-regulates nicotinic receptors by a novel mechanism. J. Neurosci. 25, 5563-5572.
51. 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.
52. Martinez-Pena y Valenzuela, I., Mouslim, C., and Akaaboune, M. (2010) Calcium/calmodulin kinase II-dependent acetylcholine receptor cycling at the mammalian neuromuscular junction in vivo. J. Neurosci. 30, 12455-12465.
53. Mohamed, A., and Posse de Chaves, E. (2011) Aβ internalization by neurons and glia. Int. J. Alzheimers Dis. 2011, 127984.
54. Nunomura, A., Perry, G., Aliev, G., Hirai, K., Takeda, A., Balraj, E. K., Jones, P. K., Ghanbari, H., Wataya, T., Shimohama, S., Chiba, S., Atwood, C. S., Petersen, R. B., and Smith, M. A. (2001) Oxidative damage is the earliest event in Alzheimer's disease. J. Neuropathol. Exp. Neurol. 60, 759-767.
55. Taguchi, N., Ishihara, N., Jofuku, A., Oka, T., and Mihara, K. (2007) Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J. Biol. Chem. 282, 11521-11529.
56. Cho, D. H., Nakamura, T., Fang, J., Cieplak, P., Godzik, A., Gu, Z., and Lipton, S. A. (2009) S-Nitrosylaton of Drp1 mediates β-amyloid-related mitochondrial fission and neuronal injury. Science 324, 102-105.
57. Vossel, K. A., Zhang, K., Brodbeck, J., Daub, A. C., Sharma, P., Finkbeiner, S., Cui, B., and Mucke, L. (2010) Tau reduction prevents Aβ-induced defects in axonal transport. Science 330, 198.