Cotinine halts the advance of Alzheimer's disease-like pathology and associated depressive-like behavior in Tg6799 mice

Frontiers in Aging Neuroscience

Volumn 6, Issue JUN, 2014, Pages 1-27

  Patel, Sagar ^a   Alex Grizzell, J ^a,c   Holmes, Rosalee ^a   Zeitlin, Ross ^a   Solomon, Rosalynn ^a   Sutton, Thomas ^a   Rohani, Adeeb ^a   Charry, Laura C ^a   Iarkov, Alexandre ^a   Mori, Takashi ^d   Moran, Valentina Echeverria ^a,b,c,e  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b DEPARTMENT OF VETERANS AFFAIRS   (United States)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

^d SAITAMA MEDICAL UNIVERSITY   (Japan)

^e UNIVERSIDAD AUTÓNOMA DE CHILE   (Chile)

Author keywords

Akt; Alzheimer's disease; Amyloid ; Cotinine; Depression; Memory loss; Postsynaptic density protein 95; Protein kinase B

Indexed keywords

AMYLOID BETA PROTEIN; COTININE; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN KINASE B;

ALZHEIMER DISEASE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPRESSION; DISEASE COURSE; ENTORHINAL CORTEX; FORCED SWIM TEST; FRONTAL CORTEX; GENOTYPE; HIPPOCAMPUS; MALE; MENTAL STRESS; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; SIGNAL TRANSDUCTION; WESTERN BLOTTING; WORKING MEMORY;

EID: 84904546955     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2014.00162     Document Type: Article

References (87)

1. Alva, G., & Cummings, J. L. (2008). Relative tolerability of Alzheimer's disease treatments. Psychiatry (Edgmont), 5(11), 27-36.
2. Arendash, G. W., et al.,(2009). Caffeine Reverses Cognitive Impairment and Decreases Brain Amyloid-beta Levels in Aged Alzheimer's Disease Mice. J Alzheimers Dis, 17(3), 661-680.
3. Assal, F., & van der Meulen, M. (2009). Pharmacological interventions in primary care: hopes and illusions. Front Neurol Neurosci, 24, 54-65.
4. Aubert, I., et al., (1992). Comparative alterations of nicotinic and muscarinic binding sites in Alzheimer's and Parkinson's diseases. J Neurochem, 58(2), 529-541.
5. Aznar, S., & Knudsen, G. M. (2011). Depression and Alzheimer's disease: is stress the initiating factor in a common neuropathological cascade? J Alzheimers Dis, 23(2), 177-193.
6. Baldinger, S. L., & Schroeder, D. J. (1995). Nicotine therapy in patients with Alzheimer's disease. Ann Pharmacother, 29(3), 314-315.
7. Barber, R. (2011). Inflammatory signaling in Alzheimer disease and depression.. Cleve Clin J Med, 78 Suppl 1, S47-49. doi: 10.3949/ccjm.78.s1.08
8. Brown, D., et al., (2013). Nicotine promotes survival of cells expressing amyloid precursor protein and presenilin: implication for Alzheimer's disease. Neurosci Lett, 535, 57-61. doi: 10.1016/j.neulet.2012.12.046
9. Caccamo, A., et al., (2013). mTOR regulates tau phosphorylation and degradation: implications for Alzheimer's disease and other tauopathies. Aging Cell, 12(3), 370-380. doi: 10.1111/acel.12057
10. Cajigas, I. J., et al., (2012). The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. Neuron, 74(3), 453-466. doi: 10.1016/j.neuron.2012.02.036
11. Cheng, Q., & Yakel, J. L. (2014). Presynaptic alpha7 nicotinic acetylcholine receptors enhance hippocampal mossy fiber glutamatergic transmission via PKA activation. J Neurosci, 34(1), 124-133. doi: 10.1523/jneurosci.2973-13.2014
12. Chung, J. A., & Cummings, J. L. (2000). Neurobehavioral and neuropsychiatric symptoms in Alzheimer's disease: characteristics and treatment. Neurol Clin, 18(4), 829-846.
13. Cohen-Mansfield, J. (1995). Assessment of disruptive behavior/agitation in the elderly: function, methods, and difficulties. J Geriatr Psychiatry Neurol, 8(1), 52-60.
14. De Aguiar, R. B., et al., (2013). Neuroactive effects of cotinine on the hippocampus: behavioral and biochemical parameters. Neuropharmacology, 71, 292-298. doi: 10.1016/j.neuropharm.2013.03.032
15. Decker, M. W., et al., (1992). Effects of nicotine on spatial memory deficits in rats with septal lesions. Brain Res, 572(1-2), 281-285.
16. Deimling, G. T., & Bass, D. M. (1986). Symptoms of mental impairment among elderly adults and their effects on family caregivers. J Gerontol, 41(6), 778-784.
17. Djuric, V. J., et al., (1999). Antidepressant effect of ingested nicotine in female rats of Flinders resistant and sensitive lines. Physiol Behav, 67(4), 533-537.
18. Dwoskin, L. P., et al., (1999). (S)-(-)-Cotinine, the major brain metabolite of nicotine, stimulates nicotinic receptors to evoke [3H]dopamine release from rat striatal slices in a calcium dependent manner. J Pharmacol Exp Ther, 288(3), 905-911.
19. Echeverria, V., et al., (2009). Sorafenib inhibits nuclear 653 factor kappa B, decreases inducible nitric oxide synthase and cyclooxygenase-2 expression, and restores working memory in APPswe mice. Neuroscience.
20. Echeverria, V., et al., (2011). Cotinine Reduces Amyloid-? Aggregation and Improves Memory in Alzheimer's Disease Mice. Journal of Alzheimer's Disease, 24, 817-835.
21. Eichenbaum, H. (2006). Remembering: functional organization of the declarative memory system. Curr Biol, 16(16), R643-645. doi: 10.1016/j.cub.2006.07.026
22. Elkobi, A., et al., (2008). ERK-dependent PSD-95 induction in the gustatory cortex is necessary for taste learning, but not retrieval. Nat Neurosci, 11(10), 1149-1151. doi: 10.1038/nn.2190
23. Even, C., & Weintraub, D. (2010). Case for and against specificity of depression in Alzheimer's disease. Psychiatry Clin Neurosci, 64(4), 358-366. doi: 10.1111/j.1440- 1819.2010.02108.x
24. Ferri CP, P. M., (2005).et al.,Alzheimer's Disease International. Global prevalence of dementia: a Delphi consensus study. The Lancet, 366(9503), 2112-2117.
25. Filali, M., et al., (2009). Cognitive and non-cognitive behaviors in an APPswe/PS1 bigenic model of Alzheimer's disease. Genes Brain Behav, 8(2), 143-148. doi: 10.1111/j.1601-183X.2008.00453.x
26. Flynn, D. D., & Mash, D. C. (1986). Characterization of l-[3H]Nicotine Binding in Human Cerebral Cortex: Comparison Between Alzheimer's Disease and the Normal. J Neurochem, 47(6), 1948-1954. doi: 10.1111/j.1471-4159.1986.tb13113.x
27. Franklin, K. B. J., and Paxinos, G. (2001). The Mouse Brain in Stereotaxic Coordinates,. San Diego, CA: Academic Press
28. Freedman, R., et al., (1995). Evidence in postmortem brain tissue for decreased numbers of hippocampal nicotinic receptors in schizophrenia. Biological Psychiatry, 38(1).
29. Freir, D. B., & Herron, C. E. (2003). Nicotine enhances the depressive actions of A beta 1-40 on long-term potentiation in the rat hippocampal CA1 region in vivo. [Research Support, Non-U.S. Gov't]. J Neurophysiol, 89(6), 2917-2922. doi: 10.1152/jn.00996.2002
30. Fuxe, K., et al., (1979). On the action of nicotine and cotinine on central 5-hydroxytryptamine neurons. Pharmacol Biochem Behav, 10(5), 671-677.
31. Gardette, V., et al., (2012). Antipsychotic use and mortality risk in community-dwelling Alzheimer's disease patients: evidence for a role of dementia severity. [Research Support, Non-U.S. Gov't]. Curr Alzheimer Res, 9(9), 1106-1116.
32. Gouras, G. K. (2013). mTOR: at the crossroads of aging, chaperones, and Alzheimer's disease.. J Neurochem, 124(6), 747-748. doi: 10.1111/jnc.12098
33. Grizzell, J. A., et al., (2014). Cotinine reduces depressive-like behavior, working memory deficits, and synaptic loss associated with chronic stress in mice. Behav Brain Res, 268C, 55-65. doi: 10.1016/j.bbr.2014.03.047
34. Hansen, R. A., et al., (2007). Functional outcomes of drug treatment in Alzheimer's disease: A systematic review and meta-analysis. Drugs Aging, 24(2), 155-167.
35. Hayase, T. (2007). Chronologically overlapping occurrences of nicotine-induced anxiety- and depression-related behavioral symptoms: effects of anxiolytic and cannabinoid drugs.. BMC Neurosci, 8, 76. doi: 10.1186/1471-2202-8-76
36. Hayase, T. (2008). Nicotine (NC)-induced "depressive" behavioral symptoms and effects of antidepressants including cannabinoids (CBs). J Toxicol Sci, 33(5), 555-564.
37. Hayase, T. (2011). Depression-related anhedonic behaviors 698 caused by immobilization stress: a comparison with nicotine-induced depression-like behavioral alterations and effects of nicotine and/or "antidepressant" drugs. J Toxicol Sci, 36(1), 31-41.
38. Hayase, T. (2013). Working memory- and anxiety-related behavioral effects of repeated nicotine as a stressor: the role of cannabinoid receptors. BMC Neurosci, 14, 20. doi: 10.1186/1471-2202-14-20
39. Hollingworth, P., et al.,(2006). Four components describe behavioral symptoms in 1,120 individuals with late-onset Alzheimer's disease. J Am Geriatr Soc, 54(9), 1348-1354.
40. Hou, Y., et al., Anti-depressant natural flavonols modulate BDNF and beta amyloid in neurons and hippocampus of double TgAD mice. Neuropharmacology, 58(6), 911-920.
41. Hou, Y., et al., (2010). Anti-depressant natural flavonols modulate BDNF and beta amyloid in neurons and hippocampus of double TgAD mice. Neuropharmacology, 58(6), 911-920.
42. Inestrosa, N. C., et al., (2013). Nicotine prevents synaptic impairment induced by amyloid-beta oligomers through alpha7-nicotinic acetylcholine receptor activation. [Research Support, Non-U.S. Gov't]. Neuromolecular Med, 15(3), 549-569. doi: 10.1007/s12017-013-8242-1
43. James, J., & Nordberg, A. (1995). Genetic and environmental aspects of the role of nicotinic receptors in neurodegenerative disorders: Emphasis on Alzheimer's disease and Parkinson's disease. Behav Genet, 25(2), 149-159. doi: 10.1007/bf02196924
44. Jones, G. M., et al., (1992). Effects of acute subcutaneous nicotine on attention, information processing and short-term memory in Alzheimer's disease. Psychopharmacology (Berl), 108(4), 485-494.
45. Karl, T., et al., (2003). Behavioral phenotyping of mice in pharmacological and toxicological research. Exp Toxicol Pathol, 55(1), 69-83.
46. Kelleher, R. J., et al., (2004). Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron, 44(1), 59-73. doi: 10.1016/j.neuron.2004.09.013
47. King, M. V., et al., (2008). A role for the 5-HT(1A), 5-HT(4) and 5-HT(6) receptors in learning and memory. Trends Pharmacol Sci.
48. Kristin M. et al., (2014). Cotinine impacts sensory processing in DBA/2 mice through changes in the conditioning amplitude. Pharmacology Biochemistry and Behavior, 117, 144-150.
49. Lafay-Chebassier, C., et al., (2005). mTOR/p70S6k signalling alteration by Aß exposure as well as in APP-PS1 transgenic models and in patients with Alzheimer's disease. J Neurochem, 94(1), 215-225. doi: 10.1111/j.1471-4159.2005.03187.x
50. Leal, G., et al., (2014). BDNF-induced local protein synthesis and synaptic plasticity. Neuropharmacology, 76 Pt C, 639-656. doi: 10.1016/j.neuropharm.2013.04.005
51. Li, X., et al., (2005). Levels of mTOR and its downstream targets 4E-BP1, eEF2, and eEF2 kinase in relationships with tau in Alzheimer's disease brain. FEBS Journal, 272(16), 4211-4220. doi: 10.1111/j.1742-4658.2005.04833.x
52. Ma, T., et al., (2010). Dysregulation of the mTOR pathway mediates impairment of synaptic plasticity in a mouse model of Alzheimer's disease. PLoS One, 5(9). doi: 10.1371/journal.pone.0012845
53. Mattson, M. P. (2007). Calcium and neurodegeneration. Aging Cell, 6(3), 337-350. doi: 10.1111/j.1474-9726.2007.00275.x
54. Meynen, G., et al., (2007). Relation between corticotropin-releasing hormone neuron number in the hypothalamic paraventricular nucleus and depressive state in Alzheimer's disease. Neuroendocrinology, 85(1), 37-44.
55. Modrego, P. J. (2010). Depression in Alzheimer's 743 disease. Pathophysiology, diagnosis, and treatment. J Alzheimers Dis, 21(4), 1077-1087.
56. Moran, V. E. (2012). Cotinine: Beyond that Expected, More than a Biomarker of Tobacco Consumption. Front Pharmacol, 3, 173. doi: 10.3389/fphar.2012.00173
57. Mori, T., et al., (2006). Arundic Acid ameliorates cerebral amyloidosis and gliosis in Alzheimer transgenic mice. J Pharmacol Exp Ther, 318(2), 571-578.
58. Naitoh, H., et al., (1992). [Behavioral assessment of antidepressants (1)--The forced swimming test: a review of its theory and practical application]. Yakubutsu Seishin Kodo, 12(3), 105-111.
59. Oakley, H., et al., (2006). Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J Neurosci, 26(40), 10129-10140.
60. Oddo, S. (2012). The role of mTOR signaling in Alzheimer disease. Front Biosci (Schol Ed), 4, 941-952.
61. Ohno, M., et al., (2006). Temporal memory deficits in Alzheimer's mouse models: rescue by genetic deletion of BACE1. Eur J Neurosci, 23(1), 251-260.
62. Pei, J. J., & Hugon, J. (2008). mTOR-dependent signalling in Alzheimer's disease. J Cell Mol Med, 12(6B), 2525-2532. doi: 10.1111/j.1582-4934.2008.00509.x
63. Pozueta, J., et al., (2013). Synaptic changes in Alzheimer's disease and its models. [Review]. Neuroscience, 251, 51-65. doi: 10.1016/j.neuroscience.2012.05.050
64. Pugh, P. L., et al., (2007). Non-cognitive behaviours in an APP/PS1 transgenic model of Alzheimer's disease. Behav Brain Res, 178(1), 18-28. doi: 10.1016/j.bbr.2006.11.044
65. Raina, P., et al., (2008). Effectiveness of cholinesterase inhibitors and memantine for treating dementia: evidence review for a clinical practice guideline. Ann Intern Med, 148(5), 379- 397.
66. Raudino, F. (2013). Non-cognitive symptoms and related conditions in the Alzheimer's disease: a literature review. Neurol Sci, 34(8), 1275-1282. doi: 10.1007/s10072-013-1424-7
67. Savonenko, A., et al., (2005). Episodic-like memory deficits in the APPswe/PS1dE9 mouse model of Alzheimer's disease: relationships to beta-amyloid deposition and neurotransmitter abnormalities. Neurobiol Dis, 18(3), 602-617. doi: 10.1016/j.nbd.2004.10.022
68. Semba, J., & Wakuta, M. (2008). Chronic effect of nicotine on serotonin transporter mRNA in the raphe nucleus of rats: reversal by co-administration of bupropion. Psychiatry Clin Neurosci, 62(4), 435-441.
69. Spencer, R. C., et al., (2012). Psychostimulants act within the prefrontal cortex to improve cognitive function. Biol Psychiatry, 72(3), 221-227. doi: 10.1016/j.biopsych.2011.12.002
70. Starkstein, S. E., & Mizrahi, R. (2006). Depression in Alzheimer's disease. Expert Rev Neurother, 6(6), 887-895.
71. Steele, C., et al., (1990). Psychiatric symptoms and nursing home placement of patients with Alzheimer's disease. Am J Psychiatry, 147(8), 1049-1051.
72. Stone, J. G., et al., (2011). Frontiers in Alzheimer's disease therapeutics. Ther Adv Chronic Dis, 2(1), 9-23. doi: 10.1177/2040622310382817
73. Sultana, R., et al., (2010). Decreased levels of PSD95 and two associated proteins and increased levels of BCl2 and caspase 3 in hippocampus from subjects with amnestic mild cognitive impairment: Insights into their potential roles for loss of synapses and memory, accumulation of Aβ, and neurodegeneration in a prodromal 788 stage of Alzheimer's disease. J Neurosci Res, 88(3), 469-477. doi: 10.1002/jnr.22227
74. Sun, Y. X., et al., (2014). Differential activation of mTOR complex 1 signaling in human brain with mild to severe Alzheimer's disease. J Alzheimers Dis, 38(2), 437-444. doi: 10.3233/JAD-131124
75. Tan, J., et al., (2002). Role of CD40 ligand in amyloidosis in transgenic Alzheimer's mice. Nat Neurosci, 5(12), 1288-1293.
76. Tang, Z., et al., (2013). Mammalian target of rapamycin (mTor) mediates tau protein dyshomeostasis: implication for Alzheimer disease. J Biol Chem, 288(22), 15556-15570. doi: 10.1074/jbc.M112.435123
77. Theleritis, C., et al., (2013). A review of neuroimaging findings of apathy in Alzheimer's disease. Int Psychogeriatr, 1-13. doi: 10.1017/S1041610213001725
78. Vainio, P. J., et al., (2000). Cotinine and nicotine inhibit each other's calcium responses in bovine chromaffin cells. Toxicol Appl Pharmacol, 163(2), 183-187.
79. Verri, M., et al., (2012). Mitochondrial alterations, oxidative stress and neuroinflammation in Alzheimer's disease. Int J Immunopathol Pharmacol, 25(2), 345-353.
80. Vilalta-Franch, J., et al., (2013). Depression subtypes and 5-year risk of dementia and Alzheimer disease in patients aged 70 years. Int J Geriatr Psychiatry, 28(4), 341-350. doi: 10.1002/gps.3826
81. Vloeberghs, E., et al., (2007). Mood and male sexual behaviour in the APP23 model of Alzheimer's disease. Behav Brain Res, 180(2), 146-151. doi: 10.1016/j.bbr.2007.03.002
82. Wang, Y. B., et al., (2012). Adaptor protein APPL1 couples synaptic NMDA receptor with neuronal prosurvival phosphatidylinositol 3-kinase/Akt pathway. J Neurosci, 32(35), 11919-11929. doi: 10.1523/JNEUROSCI.3852-11.2012
83. Weintraub, D., et al., (2010). Sertraline for the treatment of depression in Alzheimer disease: week-24 outcomes. Am J Geriatr Psychiatry, 18(4), 332-340.
84. Whitehouse, P. J., et al., (1986). Nicotinic acetylcholine binding sites in Alzheimer's disease. Brain Res, 371(1), 146-151.
85. Wuwongse, S., et al., (2010). The putative neurodegenerative links between depression and Alzheimer's disease. Prog Neurobiol, 91(4), 362-375. doi: 10.1016/j.pneurobio.2010.04.005
86. Yu, W., & Lu, B. (2012). Synapses and dendritic spines as pathogenic targets in Alzheimer's disease. Neural Plast, 2012, 247150. doi: 10.1155/2012/247150
87. Zeitlin, R., et al., (2012). Cotinine enhances the extinction of contextual fear memory and reduces anxiety after fear conditioning. Behav Brain Res, 228(2), 284-293. doi: 10.1016/j.bbr.2011.11.023