Cotinine reduces amyloid-β aggregation and improves memory in Alzheimer's disease mice

Journal of Alzheimer's Disease

Volumn 24, Issue 4, 2011, Pages 817-835

  Echeverria, Valentina ^a,b,h   Zeitlin, Ross ^a   Burgess, Sarah ^a   Patel, Sagar ^a   Barman, Arghya ^c   Thakur, Garima ^c   Mamcarz, Magorzota ^a,d   Wang, Li ^d   Sattelle, David B ^e   Kirschner, Daniel A ^f   Mori, Takashi ^g   Leblanc, Roger M ^c   Prabhakar, Rajeev ^c   ArendaS H , Gary W ^d  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c Department of Biology   (United States)

^d UNIVERSITY OF SOUTH FLORIDA   (United States)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

^f BOSTON COLLEGE   (United States)

^g SAITAMA MEDICAL UNIVERSITY   (Japan)

^h NONE   (United States)

Author keywords

Alzheimer's disease; amyloid ; cotinine; neurodegeneration; oligomerization

Indexed keywords

AMYLOID BETA PROTEIN; COTININE; GLYCOGEN SYNTHASE KINASE 3BETA; HISTIDINE; PROTEIN KINASE B;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DRUG EFFECT; HIPPOCAMPUS; IN VITRO STUDY; LEARNING; MOLECULAR DYNAMICS; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; REFERENCE MEMORY; SIGNAL TRANSDUCTION; SURVIVAL; WILD TYPE; WORKING MEMORY;

EID: 79959218579     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2011-102136     Document Type: Article

References (84)

1. Lawrence AD, Sahakian BJ (1995) Alzheimer disease, attention, and the cholinergic system. Alzheimer Dis Assoc Disord 9(Suppl 2), 43-49.
2. Echeverria V, Cuello AC (2002) Intracellular A-beta amyloid, a sign for worse things to come? Mol Neurobiol 26, 299-316. (Pubitemid 35239806)
3. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimers disease: progress and problems on the road to therapeutics. Science 297, 353-356. (Pubitemid 34790756)
4. Nordberg A (2001) Nicotinic receptor abnormalities of Alzheimers disease: therapeutic implications. Biol Psychiatry 49, 200-210. (Pubitemid 32178429)
5. Mufson EJ, Counts SE, Perez SE, Ginsberg SD (2008) Cholinergic system during the progression of Alzheimers disease: therapeutic implications. Expert Rev Neurother 8, 1703-1718.
6. Tsuno N (2009) Donepezil in the treatment of patients with Alzheimers disease. Expert Rev Neurother 9, 591-598.
7. Nordberg A (2006) Mechanisms behind the neuroprotective actions of cholinesterase inhibitors in Alzheimer disease. Alzheimer Dis Assoc Disord 20, S12-S18. (Pubitemid 44305904)
8. Bullock R (2002) The clinical benefits of rivastigmine may reflect its dual inhibitory mode of action: an hypothesis. Int J Clin Pract 56, 206-214. (Pubitemid 34477205)
9. Munoz-Torrero D (2008) Acetylcholinesterase inhibitors as disease-modifying therapies for Alzheimers disease. Curr Med Chem 15, 2433-2455.
10. Umegaki H, Itoh A, SuzukiY, Nabeshima T (2008) Discontinuation of donepezil for the treatment of Alzheimers disease in geriatric practice. Int Psychogeriatr 20, 800-806. (Pubitemid 351704882)
11. Raina P, Santaguida P, Ismaila A, Patterson C, Cowan D, Levine M, Booker L, Oremus M (2008) Effectiveness of cholinesterase inhibitors and memantine for treating dementia: evidence review for a clinical practice guideline. Ann Intern Med 148, 379-397. (Pubitemid 351665469)
12. Gongadze N, Antelava N,Kezeli T, Okudjava M, PachkoriaK (2008) The mechanisms of neurodegenerative processes and current pharmacotherapy of Alzheimers disease. Georgian Med News, 44-48.
13. Graves AB, van Duijn CM, ChandraV, Fratiglioni L, Heyman A, Jorm AF, Kokmen E, Kondo K, Mortimer JA, Rocca WA, et al. (1991) Alcohol and tobacco consumption as risk factors for Alzheimers disease: a collaborative re-analysis of casecontrol studies. EURODEM Risk Factors Research Group. Int J Epidemiol 20(Suppl 2), S48-S57.
14. Hellstrom-Lindahl E, Mousavi M, Ravid R, Nordberg A (2004) Reduced levels of Abeta 40 and Abeta 42 in brains of smoking controls and Alzheimers patients. Neurobiol Dis 15, 351-360. (Pubitemid 38296766)
15. Nordberg A, Hellstrom-Lindahl E, Lee M, Johnson M, Mousavi M, Hall R, Perry E, Bednar I, Court J (2002) Chronic nicotine treatment reduces beta-amyloidosis in the brain of a mouse model of Alzheimers disease (APPsw). J Neurochem 81, 655-658. (Pubitemid 34809344)
16. Karaconji IB (2005) Facts about nicotine toxicity. Arh Hig Rada Toksikol 56, 363-371.
17. Carlson J, Noguchi K, Ellison G (2001) Nicotine produces selective degeneration in the medial habenula and fasciculus retroflexus. Brain Res 906, 127-134. (Pubitemid 32595546)
18. Vaglenova J, Parameshwaran K, Suppiramaniam V, Breese CR, Pandiella N, Birru S (2008) Long-lasting teratogenic effects of nicotine on cognition: gender specificity and role of AMPA receptor function. Neurobiol Learn Mem 90, 527-536.
19. Terry AV Jr, Hernandez CM, Hohnadel EJ, Bouchard KP, Buccafusco JJ (2005) Cotinine, a neuroactive metabolite of nicotine: potential for treating disorders of impaired cognition. CNS Drug Rev 11, 229-252. (Pubitemid 43100463)
20. Briggs CA, McKenna DG (1998) Activation and inhibition of the human alpha7 nicotinic acetylcholine receptor by agonists. Neuropharmacology 37, 1095-1102. (Pubitemid 29027823)
21. Briggs CA, McKenna DG, Monteggia LM, Touma E, Roch JM, Arneric SP, Gopalakrishnan M, Sullivan JP (1999) Gain of function mutation of the alpha7 nicotinic receptor: distinct pharmacology of the human alpha7 V274T variant. Eur J Pharmacol 366, 301-308. (Pubitemid 29080795)
22. Vainio PJ, Tuominen RK (2001) Cotinine binding to nicotinic acetylcholine receptors in bovine chromaffin cell and rat brain membranes. Nicotine Tob Res 3, 177-182. (Pubitemid 32621779)
23. Hatsukami D, Pentel PR, Jensen J, Nelson D, Allen SS, Goldman A, Rafael D (1998) Cotinine: effects with and without nicotine. Psychopharmacology (Berl) 135, 141-150. (Pubitemid 28055497)
24. Benowitz NL, Kuyt F, Jacob P 3rd, Jones RT, Osman AL (1983) Cotinine disposition and effects. Clin Pharmacol Ther 34, 604-611. (Pubitemid 14247719)
25. Oakley H, Cole SL, Logan S, Maus E, Shao P, Craft J, Guillozet-Bongaarts A, Ohno M, Disterhoft J, Van Eldik L, Berry R, Vassar R (2006) Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimers disease mutations: potential factors in amyloid plaque formation. J Neurosci 26, 10129-10140. (Pubitemid 44527407)
26. Ohno M, Chang L, Tseng W, Oakley H, Citron M, Klein WL,Vassar R, Disterhoft JF (2006)Temporal memory deficits in Alzheimers mouse models: rescue by genetic deletion of BACE1. Eur J Neurosci 23, 251-260.
27. Kaczorowski CC, Sametsky E, Shah S, Vassar R, Disterhoft JF (2009) Mechanisms underlying basal and learning-related intrinsic excitability in a mouse model of Alzheimers disease. Neurobiol Aging. doi:10.1016/j. neurobiolaging.2009.09.003
28. Mizuno M, Yamada K, Takei N, Tran MH, He J, Nakajima A, Nawa H, Nabeshima T (2003) Phosphatidylinositol 3-kinase: a molecule mediating BDNF-dependent spatial memory formation. Mol Psychiatry 8, 217-224. (Pubitemid 36315230)
29. Chong ZZ, Li F, Maiese K (2005) Activating Akt and the brains resources to drive cellular survival and prevent inflammatory injury. Histol Histopathol 20, 299-315. (Pubitemid 40029007)
30. de Sarno P, Bijur GN, Zmijewska AA, Li X, Jope RS (2006) In vivo regulation of GSK3 phosphorylation by cholinergic and NMDA receptors. Neurobiol Aging 27, 413-422. (Pubitemid 43185326)
31. Frame S, Cohen P, Biondi RM (2001) A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation. Mol Cell 7, 1321-1327. (Pubitemid 32607364)
32. Arendash GW, Mori T, Cao C, Mamcarz M, Runfeldt M, Dickson A, Rezai-Zadeh K, Tan J, CitronBA, Lin X, Echeverria V, Potter H (2009) Caffeine reverses cognitive impairment and decreases brain Amyloid-beta levels in aged Alzheimers disease mice. J Alzheimers Dis 17, 661-680.
33. Echeverria V, Burgess S, Gamble-George J, Zeitlin R, Lin X, Cao C, Arendash GW (2009) Sorafenib inhibits nuclear factor kappa B, decreases inducible nitric oxide synthase and cyclooxygenase-2 expression, and restores working memory in APPswe mice. Neuroscience 162, 1220-1231.
34. Pompl PN, Mullan MJ, Bjugstad K, Arendash GW (1999) Adaptation of the circular platform spatial memory task for mice: use in detecting cognitive impairment in the APP(SW) transgenic mouse model for Alzheimers disease. J Neurosci Methods 87, 87-95. (Pubitemid 29087089)
35. Loewenstein DA, Acevedo A, Luis C, Crum T, Barker WW, Duara R (2004) Semantic interference deficits and the detection of mild Alzheimers disease and mild cognitive impairment without dementia. J Int Neuropsychol Soc 10, 91-100. (Pubitemid 38128466)
36. Tan J,TownT, Crawford F, MoriT, DelleDonne A, Crescentini R, Obregon D, Flavell RA, Mullan MJ (2002) Role of CD40 ligand in amyloidosis in transgenic Alzheimers mice. Nat Neurosci 5, 1288-1293. (Pubitemid 35417763)
37. Mori T, Town T, Tan J, Yada N, Horikoshi Y, Yamamoto J, Shimoda T, Kamanaka Y, Tateishi N, Asano T (2006) Arundic acid ameliorates cerebral amyloidosis and gliosis in Alzheimer transgenic mice. J Pharmacol Exp Ther 318, 571-578. (Pubitemid 44061231)
38. Necula M, Kayed R, Milton S, Glabe CG (2007) Small molecule inhibitors of aggregation indicate that amyloid beta oligomerization and fibrillization pathways are independent and distinct. J Biol Chem 282, 10311-10324. (Pubitemid 47093410)
39. Chromy BA, Nowak RJ, Lambert MP, Viola KL, Chang L, Velasco PT, Jones BW, Fernandez SJ, Lacor PN, Horowitz P, Finch CE, Krafft GA, Klein WL (2003) Self-assembly of Abeta(1-42) into globular neurotoxins. Biochemistry 42, 12749-12760.
40. Morris GM, Goodsell DS, Halliday RS, Huey R, Hart WE, Belew RK, Olson AJ (1998) Automated docking using a lamarckian genetic algorithm and empirical binding free energy function. J Comp Chem 19, 1639-1662. (Pubitemid 128590223)
41. Triguero L, Singh R, Prabhakar R (2008) Comparative molecular dynamics studies of wild-type and oxidized forms of full-length Alzheimer amyloid beta-peptides Abeta(1-40) and Abeta(1-42). J Phys Chem B 112, 7123-7131.
42. Salomon AR, Marcinowski KJ, Friedland RP, Zagorski MG (1996) Nicotine inhibits amyloid formation by the betapeptide. Biochemistry 35, 13568-13578. (Pubitemid 26359169)
43. Moore SA, Huckerby TN, Gibson GL, Fullwood NJ, Turnbull S, Tabner BJ, El-Agnaf OM, Allsop D (2004) Both the D-(+) and L-(-) enantiomers of nicotine inhibit Abeta aggregation and cytotoxicity. Biochemistry 43, 819-826. (Pubitemid 38114070)
44. Ono K, Hasegawa K, Yamada M, Naiki H (2002) Nicotine breaks down preformed Alzheimers beta-amyloid fibrils in vitro. Biol Psychiatry 52, 880-886. (Pubitemid 35223431)
45. Berendsen HJC, van der Spoel D, van Drunen, D (1995) GROMACS: A message-passing parallel molecular dynamics implementation. Computer Physics Communications 91, 43-56.
46. Schuettelkopf AW, van Aalten DMF (2004) PRODRG -a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallographica 60, 1355-1363.
47. Miyamoto S,Kollman PA(1992) SETTLE: An analytical version of the SHAKE and RATTLE algorithms for rigid water models. J Comp Chem 13, 952-962.
48. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM (1997) LINCS: A linear constraint solver for molecular simulations. J Comp Chem 18, 1463-1472. (Pubitemid 127637344)
49. Darden TA, York D, Pedersen L (1993) Particle mesh Ewald: An Nlog(N) method forEwald sums in large systems. J Chem Physics 98, 10089-10092.
50. York DM, Wlodawer A, Pedersen LG, Darden TA (1994) Atomic-level accuracy in simulations of large protein crystals. Proc Natl Acad Sci U S A 91, 8715-8718. (Pubitemid 24273735)
51. Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637.
52. Daura X, van Gunsteren WF, Mark AE (1999) Foldingunfolding thermodynamics of a beta-heptapeptide from equilibrium simulations. Proteins 34, 269-280. (Pubitemid 29071670)
53. Gomez de Barreda E, Perez M, Gomez Ramos P, de Cristobal J, Martin-Maestro P, Moran A, Dawson HN, Vitek MP, Lucas JJ, Hernandez F,Avila J (2010) Tau-knockout mice show reduced GSK3-induced hippocampal degeneration and learning deficits. Neurobiol Dis 37, 622-629.
54. Lockman PR, McAfee G, Geldenhuys WJ, van der Schyf CJ, Abbruscato TJ, Allen DD (2005) Brain uptake kinetics of nicotine and cotinine after chronic nicotine exposure. J Pharmacol Exp Ther 314, 636-642. (Pubitemid 41043844)
55. Riah O, Courriere P, Dousset JC, Todeschi N, Labat C (1998) Nicotine is more efficient than cotinine at passing the bloodbrain barrier in rats. Cell Mol Neurobiol 18, 311-318. (Pubitemid 28196723)
56. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci U S A 95, 6448-6453.
57. Ferreira ST, Vieira MN, de Felice FG (2007) Soluble protein oligomers as emerging toxins in Alzheimers and other amyloid diseases. IUBMB Life 59, 332-345. (Pubitemid 46763764)
58. Hatsukami D, Lexau B, Nelson D, Pentel PR, Sofuoglu M, Goldman A (1998) Effects of cotinine on cigarette selfadministration. Psychopharmacology (Berl) 138, 184-189.
59. Hatsukami DK, Grillo M, Pentel PR, Oncken C, Bliss R (1997) Safety of cotinine in humans: physiologic, subjective, and cognitive effects. Pharmacol Biochem Behav 57, 643-650. (Pubitemid 27334410)
60. Olcese JM, Cao C, Mori T, Mamcarz MB, Maxwell A, Runfeldt MJ, Wang L, Zhang C, Lin X, Zhang G, Arendash GW (2009) Protection against cognitive deficits and markers of neurodegeneration by long-term oral administration of melatonin in a transgenic model of Alzheimer disease. J Pineal Res 47, 82-96.
61. Takashima A (2006) GSK-3 is essential in the pathogenesis of Alzheimers disease. J Alzheimers Dis 9, 309-317. (Pubitemid 44253325)
62. Hooper C, Killick R, Lovestone S (2008) The GSK3 hypothesis of Alzheimers disease. J Neurochem 104, 1433-1439.
63. Plattner F, Angelo M, Giese KP (2006) The roles of cyclindependent kinase 5 and glycogen synthase kinase 3 in tau hyperphosphorylation. J Biol Chem 281, 25457-25465. (Pubitemid 44401934)
64. Baum L, Hansen L, Masliah E, Saitoh T (1996) Glycogen synthase kinase 3 alteration in Alzheimer disease is related to neurofibrillary tangle formation. Mol Chem Neuropathol 29, 253-261. (Pubitemid 27016933)
65. Jan A, Gokce O, Luthi-Carter R, LashuelHA(2008) The ratio of monomeric to aggregated forms of Abeta40 and Abeta42 is an important determinant of amyloid-beta aggregation, fibrillogenesis, and toxicity. J Biol Chem 283, 28176-28189.
66. Kim J, Onstead L, Randle S, Price R, Smithson L, Zwizinski C, Dickson DW, Golde T, McGowan E (2007) Abeta40 inhibits amyloid deposition in vivo. J Neurosci 27, 627-633. (Pubitemid 46143766)
67. Kumar-Singh S, Theuns J, van Broeck B, Pirici D, Vennekens K, Corsmit E, Cruts M, Dermaut B,Wang R, van Broeckhoven C (2006) Mean age-of-onset of familial Alzheimer disease caused by presenilin mutations correlates with both increased Abeta42 and decreased Abeta40. Hum Mutat 27, 686-695.
68. Arendash GW, Sanchez-Ramos J, Mori T, Mamcarz M, Lin X, Runfeldt M, Wang L, Zhang G, Sava V, Tan J, Cao C (2010) Electromagnetic field treatment protects against and reverses cognitive impairment in Alzheimers disease mice. J Alzheimers Dis 19, 191-210.
69. Szymanska I, Radecka H, Radecki J, Kaliszan R (2007) Electrochemical impedance spectroscopy for study of amyloid beta-peptide interactions with (-) nicotine ditartrate and (-) cotinine. Biosens Bioelectron 22, 1955-1960. (Pubitemid 46349631)
70. de Felice FG,Wasilewska-Sampaio AP, Barbosa AC, Gomes FC, Klein WL, Ferreira ST (2007) Cyclic AMP enhancers and Abeta oligomerization blockers as potential therapeutic agents in Alzheimers disease. Curr Alzheimer Res 4, 263-271. (Pubitemid 47025424)
71. Walsh DM, Selkoe DJ (2007) A beta oligomers -a decade of discovery. J Neurochem 101, 1172-1184.
72. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimers amyloid beta-peptide. Nat Rev Mol Cell Biol 8, 101-112. (Pubitemid 46432529)
73. Tabaton M, Gambetti P (2006) Soluble amyloid-beta in the brain: the scarlet pimpernel. J Alzheimers Dis 9, 127-132. (Pubitemid 44253306)
74. Echeverria V, Ducatenzeiler A, Dowd E, Janne J, Grant SM, Szyf M, Wandosell F, Avila J, Grimm H, Dunnett SB, Hartmann T, Alhonen L, Cuello AC (2004) Altered mitogenactivated protein kinase signaling, tau hyperphosphorylation and mild spatial learning dysfunction in transgenic rats expressing the beta-amyloid peptide intracellularly in hippocampal and cortical neurons. Neuroscience 129, 583-592. (Pubitemid 39487112)
75. Rangachari V, Moore BD, Reed DK, Sonoda LK, Bridges AW, Conboy E, Hartigan D, Rosenberry TL (2007) Amyloidbeta( 1-42) rapidly forms protofibrils and oligomers by distinct pathways in low concentrations of sodium dodecylsulfate. Biochemistry 46, 12451-12462. (Pubitemid 350027406)
76. Mastrangelo IA, Ahmed M, Sato T, Liu W, Wang C, Hough P, Smith SO (2006) High-resolution atomic force microscopy of soluble Abeta42 oligomers. J Mol Biol 358, 106-119.
77. Kirschner DA, Gross AA, Hidalgo MM, Inouye H, Gleason KA, Abdelsayed GA, Castillo GM, Snow AD, Pozo-Ramajo A, Petty SA, Decatur SM (2008) Fiber diffraction as a screen for amyloid inhibitors. Curr Alzheimer Res 5, 288-307. (Pubitemid 351840278)
78. Antzutkin ON, Balbach JJ, Tycko R (2003) Site-specific identification of non-beta-strand conformations in Alzheimers beta-amyloid fibrils by solid-state NMR. Biophys J 84, 3326-3335. (Pubitemid 36531780)
79. Yu J, Bakhos L, Chang L, Holterman MJ, Klein WL, Venton DL (2002) Per-6-substituted beta-cyclodextrin libraries inhibit formation of beta-amyloid-peptide (A beta)-derived, soluble oligomers. J Mol Neurosci 19, 51-55. (Pubitemid 35013334)
80. Yang F, Lim GP, Begum AN, Ubeda OJ, Simmons MR, Ambegaokar SS, Chen PP, Kayed R, Glabe CG, Frautschy SA, Cole GM (2005) Curcumin inhibits formation of amyloid beta oligomers and fibrils, binds plaques, and reduces amyloid in vivo. J Biol Chem 280, 5892-5901. (Pubitemid 40280072)
81. Yao Z, Drieu K, Papadopoulos V (2001) The Ginkgo biloba extract EGb 761 rescues the PC12 neuronal cells from betaamyloid-induced cell death by inhibiting the formation of beta-amyloid-derived diffusible neurotoxic ligands. Brain Res 889, 181-190. (Pubitemid 32146280)
82. de Felice FG, Vieira MN, Saraiva LM, Figueroa-Villar JD, Garcia-Abreu J, Liu R, Chang L, Klein WL, Ferreira ST (2004) Targeting the neurotoxic species in Alzheimers disease: inhibitors of Abeta oligomerization. FASEB J 18, 1366-1372. (Pubitemid 39150351)
83. Zhao W, Wang J, Ho L, Ono K, Teplow DB, Pasinetti GM (2009) Identification of antihypertensive drugs which inhibit amyloid-beta protein oligomerization. J Alzheimers Dis 16, 49-57.
84. Hou Y, Aboukhatwa MA, Lei DL, Manaye K, Khan I, Luo Y (2010) Anti-depressant natural flavonols modulateBDNFand beta amyloid in neurons and hippocampus of double TgAD mice. Neuropharmacology 58, 911-920.