α7 Nicotinic receptor activation reduces β-amyloid-induced apoptosis by inhibiting caspase-independent death through phosphatidylinositol 3-kinase signaling

Journal of Neurochemistry

Volumn 119, Issue 4, 2011, Pages 848-858

  Yu, Wenfeng ^a   Mechawar, Naguib ^a   Krantic, Slavica ^a   Quirion, Rémi ^a  

^a DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

Author keywords

amyloid ; apoptosis inducing factor; neuronal culture; neuroprotection; nicotine; phosphatidylinositol 3 kinase

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; AMYLOID BETA PROTEIN[1-42]; APOPTOSIS INDUCING FACTOR; BUNGAROTOXIN RECEPTOR; CASPASE; CASPASE 3; CYTOCHROME C; DIHYDRO BETA ERYTHROIDINE; METHYLLYCACONITINE; NICOTINE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CULTURE; CELL DEATH; CELL TRANSPORT; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; MITOCHONDRION; NERVE CELL; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

AMYLOID BETA-PEPTIDES; ANIMALS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; BENZYL COMPOUNDS; CASPASES; CELLS, CULTURED; CEREBRAL CORTEX; CHOLINERGIC AGENTS; CYTOCHROMES C; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; ENZYME INHIBITORS; HYDROCARBONS, FLUORINATED; MICROSCOPY, CONFOCAL; MITOCHONDRIA; NEURONS; NICOTINE; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; PHOSPHATIDYLINOSITOL 3-KINASE; RATS; RECEPTORS, NICOTINIC; SIGNAL TRANSDUCTION;

RATTUS;

EID: 80054811612     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07466.x     Document Type: Article

References (47)

1. Akaike A., Takada-Takatori Y., Kume T., and, Izumi Y., (2010) Mechanisms of neuroprotective effects of nicotine and acetylcholinesterase inhibitors: role of alpha4 and alpha7 receptors in neuroprotection. J. Mol. Neurosci. 40, 211-216.
2. 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.
3. Allen J. W., Eldadah B. A., Huang X., Knoblach S. M., and, Faden A. I., (2001) Multiple caspases are involved in beta-amyloid-induced neuronal apoptosis. J. Neurosci. Res. 65, 45-53.
4. Bastianetto S., Ramassamy C., Poirier J., and, Quirion R., (1999) Dehydroepiandrosterone (DHEA) protects hippocampal cells from oxidative stress-induced damage. Brain Res. Mol. Brain Res. 66, 35-41. (Pubitemid 29148331)
5. Bastianetto S., Ramassamy C., Dore S., Christen Y., Poirier J., and, Quirion R., (2000) The Ginkgo biloba extract (EGb 761) protects hippocampal neurons against cell death induced by beta-amyloid. Eur. J. Neurosci. 12, 1882-1890. (Pubitemid 30348827)
6. Bastianetto S., Yao Z. X., Papadopoulos V., and, Quirion R., (2006) Neuroprotective effects of green and black teas and their catechin gallate esters against beta-amyloid-induced toxicity. Eur. J. Neurosci. 23, 55-64.
7. Bitner R. S., Bunnelle W. H., Decker M. W., et al. (2010) In vivo pharmacological characterization of a novel selective alpha7 neuronal nicotinic acetylcholine receptor agonist ABT-107: preclinical considerations in Alzheimer's disease. J. Pharmacol. Exp. Ther. 334, 875-886.
8. Buckingham S. D., Jones A. K., Brown L. A., and, Sattelle D. B., (2009) Nicotinic acetylcholine receptor signalling: roles in Alzheimer's disease and amyloid neuroprotection. Pharmacol. Rev. 61, 39-61.
9. Cheung E. C., Melanson-Drapeau L., Cregan S. P., Vanderluit J. L., Ferguson K. L., McIntosh W. C., Park D. S., Bennett S. A., and, Slack R. S., (2005) Apoptosis-inducing factor is a key factor in neuronal cell death propagated by BAX-dependent and BAX-independent mechanisms. J. Neurosci. 25, 1324-1334. (Pubitemid 40250708)
10. Cregan S. P., Fortin A., MacLaurin J. G., et al. (2002) Apoptosis-inducing factor is involved in the regulation of caspase-independent neuronal cell death. J. Cell Biol. 158, 507-517. (Pubitemid 34851709)
11. Cregan S. P., Dawson V. L., and, Slack R. S., (2004) Role of AIF in caspase-dependent and caspase-independent cell death. Oncogene 23, 2785-2796. (Pubitemid 38638842)
12. Dajas-Bailador F. A., Soliakov L., and, Wonnacott S., (2002) Nicotine activates the extracellular signal-regulated kinase 1/2 via the alpha7 nicotinic acetylcholine receptor and protein kinase A, in SH-SY5Y cells and hippocampal neurones. J. Neurochem. 80, 520-530. (Pubitemid 36383035)
13. Daugas E., Susin S. A., Zamzami N., et al. (2000) Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB J. 14, 729-739. (Pubitemid 30198571)
14. Giovanni A., Keramaris E., Morris E. J., Hou S. T., O'Hare M., Dyson N., Robertson G. S., Slack R. S., and, Park D. S., (2000) E2F1 mediates death of B-amyloid-treated cortical neurons in a manner independent of p53 and dependent on Bax and caspase 3. J. Biol. Chem. 275, 11553-11560. (Pubitemid 30237711)
15. Jin Z., Gao F., Flagg T., and, Deng X., (2004) Nicotine induces multi-site phosphorylation of Bad in association with suppression of apoptosis. J. Biol. Chem. 279, 23837-23844. (Pubitemid 38685702)
16. Joza N., Susin S. A., Daugas E., et al. (2001) Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410, 549-554. (Pubitemid 32267191)
17. 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. (Pubitemid 27340459)
18. 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. (Pubitemid 28267549)
19. 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, 13541-13546.
20. Krantic S., Mechawar N., Reix S., and, Quirion R., (2007) Apoptosis-inducing factor: a matter of neuron life and death. Prog. Neurobiol. 81, 179-196. (Pubitemid 46282274)
21. LeBlanc A. C., (2005) The role of apoptotic pathways in Alzheimer's disease neurodegeneration and cell death. Curr. Alzheimer Res. 2, 389-402.
22. Levin E. D., McClernon F. J., and, Rezvani A. H., (2006) Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacology (Berl) 184, 523-539. (Pubitemid 43255869)
23. Liu Q., and, Zhao B., (2004) Nicotine attenuates beta-amyloid peptide-induced neurotoxicity, free radical and calcium accumulation in hippocampal neuronal cultures. Br. J. Pharmacol. 141, 746-754. (Pubitemid 38453267)
24. Liu Y., Peterson D. A., Kimura H., and, Schubert D., (1997) Mechanism of cellular 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) reduction. J. Neurochem. 69, 581-593. (Pubitemid 27327958)
25. Loo D. T., Copani A., Pike C. J., Whittemore E. R., Walencewicz A. J., and, Cotman C. W., (1993) Apoptosis is induced by beta-amyloid in cultured central nervous system neurons. Proc. Natl. Acad. Sci. USA 90, 7951-7955. (Pubitemid 23260832)
26. Mattson M. P., (2000) Apoptosis in neurodegenerative disorders. Nat. Rev. Mol. Cell Biol. 1, 120-129.
27. Mattson M. P., (2004) Pathways towards and away from Alzheimer's disease. Nature 430, 631-639. (Pubitemid 39061671)
28. Movsesyan V. A., Stoica B. A., and, Faden A. I., (2004) MGLuR5 activation reduces beta-amyloid-induced cell death in primary neuronal cultures and attenuates translocation of cytochrome c and apoptosis-inducing factor. J. Neurochem. 89, 1528-1536. (Pubitemid 38802674)
29. Nordberg A., Hellstrom-Lindahl E., Lee M., Johnson M., Mousavi M., Hall R., Perry E., Bednar I., and, Court J., (2002) Chronic nicotine treatment reduces beta-amyloidosis in the brain of a mouse model of Alzheimer's disease (APPsw). J. Neurochem. 81, 655-658. (Pubitemid 34809344)
30. Nuutinen U., Postila V., Matto M., Eeva J., Ropponen A., Eray M., Riikonen P., and, Pelkonen J., (2006) Inhibition of PI3-kinase-Akt pathway enhances dexamethasone-induced apoptosis in a human follicular lymphoma cell line. Exp. Cell Res. 312, 322-330. (Pubitemid 41814841)
31. Otera H., Ohsakaya S., Nagaura Z., Ishihara N., and, Mihara K., (2005) Export of mitochondrial AIF in response to proapoptotic stimuli depends on processing at the intermembrane space. EMBO J. 24, 1375-1386. (Pubitemid 40593058)
32. Picciotto M. R., and, Zoli M., (2008) Neuroprotection via nAChRs: the role of nAChRs in neurodegenerative disorders such as Alzheimer's and Parkinson's disease. Front Biosci. 13, 492-504. (Pubitemid 351599760)
33. Reix S., Mechawar N., Susin S. A., Quirion R., and, Krantic S., (2007) Expression of cortical and hippocampal apoptosis-inducing factor (AIF) in aging and Alzheimer's disease. Neurobiol. Aging 28, 351-356. (Pubitemid 46177383)
34. Selkoe D. J., (2002) Alzheimer's disease is a synaptic failure. Science 298, 789-791. (Pubitemid 35231524)
35. Steiner R. C., Heath C. J., and, Picciotto M. R., (2007) Nicotine-induced phosphorylation of ERK in mouse primary cortical neurons: evidence for involvement of glutamatergic signaling and CaMKII. J. Neurochem. 103, 666-678. (Pubitemid 47498033)
36. Susin S. A., Lorenzo H. K., Zamzami N., et al. (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397, 441-446.
37. Susin S. A., Daugas E., Ravagnan L., et al. (2000) Two distinct pathways leading to nuclear apoptosis. J. Exp. Med. 192, 571-580.
38. Vivanco I., and, Sawyers C. L., (2002) The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat. Rev. Cancer 2, 489-501. (Pubitemid 37328931)
39. Wang H. Y., Bakshi K., Shen C., Frankfurt M., Trocme-Thibierge C., and, Morain P., (2010) S 24795 limits beta-amyloid-alpha7 nicotinic receptor interaction and reduces Alzheimer's disease-like pathologies. Biol. Psychiatry 67, 522-530.
40. Wei W., Norton D. D., Wang X., and, Kusiak J. W., (2002) Abeta 17-42 in Alzheimer's disease activates JNK and caspase-8 leading to neuronal apoptosis. Brain 125, 2036-2043.
41. Wellington C. L., and, Hayden M. R., (2000) Caspases and neurodegeneration: on the cutting edge of new therapeutic approaches. Clin. Genet. 57, 1-10. (Pubitemid 30105555)
42. Yaar M., Zhai S., Pilch P. F., Doyle S. M., Eisenhauer P. B., Fine R. E., and, Gilchrest B. A., (1997) Binding of beta-amyloid to the p75 neurotrophin receptor induces apoptosis. A possible mechanism for Alzheimer's disease. J. Clin. Invest. 100, 2333-2340. (Pubitemid 27500157)
43. Yu W., Mechawar N., Krantic S., and, Quirion R., (2010) Evidence for the involvement of apoptosis-inducing factor-mediated caspase-independent neuronal death in Alzheimer disease. Am. J. Pathol. 176, 2209-2218.
44. Yuan J., and, Yankner B. A., (2000) Apoptosis in the nervous system. Nature 407, 802-809.
45. Zanardi A., Leo G., Biagini G., and, Zoli M., (2002) Nicotine and neurodegeneration in ageing. Toxicol. Lett. 127, 207-215. (Pubitemid 34615512)
46. Zeng H., Zhang Y., Peng L., Shao H., Menon N. K., Yang J., Salomon A. R., Freidland R. P., and, Zagorski M. G., (2001) Nicotine and amyloid formation. Biol. Psychiatry 49, 248-257. (Pubitemid 32178434)
47. Zoli M., Lena C., Picciotto M. R., and, Changeux J. P., (1998) Identification of four classes of brain nicotinic receptors using beta2 mutant mice. J. Neurosci. 18, 4461-4472. (Pubitemid 28280157)