The multi-functional drug tropisetron binds APP and normalizes cognition in a murine Alzheimer's model

Brain Research

Volumn 1551, Issue , 2014, Pages 25-44

  Spilman, Patricia ^a   Descamps, Olivier ^a   Gorostiza, Olivia ^a   Peters Libeu, Clare ^a   Poksay, Karen S ^a   Matalis, Alexander ^a   Campagna, Jesus ^a   Patent, Alexander ^a   Rao, Rammohan ^a   John, Varghese ^a,b   Bredesen, Dale E ^a,c  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^b DOMINICAN UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alzheimer's disease; Candidate therapeutic; Improvement in sAPP A 42 biomarker ratio; Memory improvement; Multi functional drug; Orally effective

Indexed keywords

ALZHEIMER'S DISEASE; CANDIDATE THERAPEUTIC; IMPROVEMENT IN SAPPΑ/AΒ42 BIOMARKER RATIO; MEMORY IMPROVEMENT; MULTI-FUNCTIONAL DRUG; ORALLY EFFECTIVE;

ADMINISTRATION, ORAL; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CHO CELLS; COGNITION; CRICETULUS; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; INDOLES; MICE; MICE, INBRED C57BL;

EID: 84894102112     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.12.029     Document Type: Article

References (64)

1. T. Alkam, M. Hiramatsu, T. Mamiya, Y. Aoyama, A. Nitta, K. Yamada, H.C. Kim, and T. Nabeshima Evaluation of object-based attention in mice Behav. Brain Res. 220 2011 185 193
2. Y. Aracava, E.F. Pereira, A. Maelicke, and E.X. Albuquerque Memantine blocks alpha7* nicotinic acetylcholine receptors more potently than n-methyl-D-aspartate receptors in rat hippocampal neurons J. Pharmacol. Exp. Ther. 312 2005 1195 1205 (Pubitemid 40293781)
3. N.M. Barnes, and T. Sharp A review of central 5-HT receptors and their function Neuropharmacology 38 1999 1083 1152 (Pubitemid 29292403)
4. R.A. Bevins, and J. Besheer Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study 'recognition memory' Nat. Protocols 1 2006 1306 1311
5. C. Bianchi, A. Siniscalchi, and L. Beani 5-HT1A agonists increase and 5-HT3 agonists decrease acetylcholine efflux from the cerebral cortex of freely-moving guinea-pigs Br. J. Pharmacol. 101 1990 448 452 (Pubitemid 20292904)
6. D.E. Bredesen Neurodegeneration in Alzheimer's disease: caspases and synaptic element interdependence Mol. Neurodegener. 4 2009 27
7. G. Chen, K.S. Chen, J. Knox, J. Inglis, A. Bernard, S.J. Martin, A. Justice, L. McConlogue, D. Games, S.B. Freedman, and R.G. Morris A learning deficit related to age and beta-amyloid plaques in a mouse model of Alzheimer's disease Nature 408 2000 975 979 (Pubitemid 32101643)
8. I.H. Cheng, K. Scearce-Levie, J. Legleiter, J.J. Palop, H. Gerstein, N. Bien-Ly, J. Puolivali, S. Lesne, K.H. Ashe, P.J. Muchowski, and L. Mucke Accelerating amyloid-beta fibrillization reduces oligomer levels and functional deficits in Alzheimer disease mouse models J. Biol. Chem. 282 2007 23818 23828 (Pubitemid 47328006)
9. A.M. Claasen, D. Guevremont, S.E. Mason-Parker, K. Bourne, W.P. Tate, W.C. Abraham, and J.M. Williams Secreted amyloid precursor protein-alpha upregulates synaptic protein synthesis by a protein kinase G-dependent mechanism Neurosci. Lett. 460 2009 92 96
10. E. Dere, J.P. Huston, and De Souza Silva M.A. The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents Neurosci. Biobehav. Rev. 31 2007 673 704 (Pubitemid 46670336)
11. H. Dong, C.A. Csernansky, M.V. Martin, A. Bertchume, D. Vallera, and J.G. Csernansky Acetylcholinesterase inhibitors ameliorate behavioral deficits in the Tg2576 mouse model of Alzheimer's disease Psychopharmacology (Berl) 181 2005 145 152 (Pubitemid 41440925)
12. R.S. Doody, J. Corey-Bloom, R. Zhang, H. Li, J. Ieni, and R. Schindler Safety and tolerability of donepezil at doses up to 20 mg/day: results from a pilot study in patients with Alzheimer's disease Drugs Aging 25 2008 163 174 (Pubitemid 351225820)
13. C.M. Flores, S.W. Rogers, L.A. Pabreza, B.B. Wolfe, and K.J. Kellar 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 1992 31 37
14. C. Garbe, S. Drechsler, H. Fiedler, W. Tilgen, M. Landthaler, K. Schroeder, K.H. Kuehne, and L. Faerber Dose comparison of tropisetron (Navoban) 5 mg and 10 mg orally in the prophylaxis of dacarbazine-induced nausea and emesis Semin. Oncol. 21 1994 12 16 (Pubitemid 24325189)
15. H. Hodges, P. Sowinski, J.J. Turner, and A. Fletcher Comparison of the effects of the 5-HT3 receptor antagonists WAY-100579 and ondansetron on spatial learning in the water maze in rats with excitotoxic lesions of the forebrain cholinergic projection system Psychopharmacology (Berl) 125 1996 146 161
16. C. Holmes, D. Boche, D. Wilkinson, G. Yadegarfar, V. Hopkins, A. Bayer, R.W. Jones, R. Bullock, S. Love, J.W. Neal, E. Zotova, and J.A. Nicoll Long-term effects of Abeta42 immunisation in Alzheimer's disease: follow-up of a randomised, placebo-controlled phase I trial Lancet 372 2008 216 223 (Pubitemid 351978111)
17. D.M. Holtzman, J.C. Morris, and A.M. Goate Alzheimer's disease: the challenge of the second century Sci. Transl. Med. 3 2011 77sr1
18. A.Y. Hsia, E. Masliah, L. McConlogue, G.Q. Yu, G. Tatsuno, K. Hu, D. Kholodenko, R.C. Malenka, R.A. Nicoll, and L. Mucke Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models Proc. Natl. Acad. Sci. USA 96 1999 3228 3233 (Pubitemid 29148873)
19. B. Ju Yeon, and S. Yeon Hee Blockade of 5-HT(3) receptor with MDL 72222 and Y 25130 reduces beta-amyloid protein (25-35)-induced neurotoxicity in cultured rat cortical neurons Eur. J. Pharmacol. 520 2005 12 21
20. K. Kawa Distribution and functional properties of 5-HT3 receptors in the rat hippocampal dentate gyrus: a patch-clamp study J. Neurophysiol. 71 1994 1935 1947 (Pubitemid 24153054)
21. W.E. Klunk, C.A. Mathis, J.C. Price, B.J. Lopresti, and S.T. DeKosky Two-year follow-up of amyloid deposition in patients with Alzheimer's disease Brain 129 2006 2805 2807 (Pubitemid 44684503)
22. D.H. Lee, and H.Y. Wang Differential physiologic responses of alpha7 nicotinic acetylcholine receptors to beta-amyloid1-40 and beta-amyloid1-42 J. Neurobiol. 55 2003 25 30 (Pubitemid 36396959)
23. C.P. Libeu, K.S. Poksay, V. John, and D.E. Bredesen Structural and functional alterations in amyloid-beta precursor protein induced by amyloid-beta peptides J. Alzheimers Dis. 25 2011 547 566
24. J.E. Macor, D. Gurley, T. Lanthorn, J. Loch, R.A. Mack, G. Mullen, O. Tran, N. Wright, and J.C. Gordon The 5-HT3 antagonist tropisetron (ICS 205-930) is a potent and selective alpha7 nicotinic receptor partial agonist Bioorg. Med. Chem. Lett. 11 2001 319 321 (Pubitemid 32115836)
25. E. Marcello, C. Saraceno, S. Musardo, H. Vara, A.G. de la Fuente, S. Pelucchi, D. Di Marino, B. Borroni, A. Tramontano, I. Perez-Otano, A. Padovani, M. Giustetto, F. Gardoni, and M. Di Luca Endocytosis of synaptic ADAM10 in neuronal plasticity and Alzheimer's disease J. Clin. Invest. 123 2013 2523 2538
26. M.B. Marrero, R.L. Papke, B.S. Bhatti, S. Shaw, and M. Bencherif The neuroprotective effect of 2-(3-pyridyl)-1-azabicyclo[3.2.2]nonane (TC-1698), a novel alpha7 ligand, is prevented through angiotensin II activation of a tyrosine phosphatase J. Pharmacol. Exp. Ther. 309 2004 16 27 (Pubitemid 38393109)
27. M.A. Mintun, G.N. Larossa, Y.I. Sheline, C.S. Dence, S.Y. Lee, R.H. Mach, W.E. Klunk, C.A. Mathis, S.T. DeKosky, and J.C. Morris [11C]PIB in a nondemented population: potential antecedent marker of Alzheimer disease Neurology 67 2006 446 452 (Pubitemid 44214969)
28. M. Morales, E. Battenberg, L. de Lecea, P.P. Sanna, and F.E. Bloom Cellular and subcellular immunolocalization of the type 3 serotonin receptor in the rat central nervous system Brain Res. Mol. Brain Res. 36 1996 251 260 (Pubitemid 26095584)
29. M. Morales, and F.E. Bloom The 5-HT3 receptor is present in different subpopulations of GABAergic neurons in the rat telencephalon J. Neurosci. 17 1997 3157 3167 (Pubitemid 27175828)
30. J.C. Morris, and J.L. Price Pathologic correlates of nondemented aging, mild cognitive impairment, and early-stage Alzheimer's disease J. Mol. Neurosci. 17 2001 101 118 (Pubitemid 33063515)
31. R. Morris Developments of a water-maze procedure for studying spatial learning in the rat J. Neurosci. Methods 11 1984 47 60 (Pubitemid 14088970)
32. G.R. Morrow, J.T. Hickok, and S.N. Rosenthal Progress in reducing nausea and emesis. Comparisons of ondansetron (Zofran), granisetron (Kytril), and tropisetron (Navoban) Cancer 76 1995 343 357
33. L. Mucke, E. Masliah, G.Q. Yu, M. Mallory, E.M. Rockenstein, G. Tatsuno, K. Hu, D. Kholodenko, K. Johnson-Wood, and L. McConlogue High-level neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation J. Neurosci. 20 2000 4050 4058 (Pubitemid 30365675)
34. R.G. Nagele, M.R. D'Andrea, W.J. Anderson, and H.Y. Wang Intracellular accumulation of beta-amyloid(1-42) in neurons is facilitated by the alpha 7 nicotinic acetylcholine receptor in Alzheimer's disease Neuroscience 110 2002 199 211 (Pubitemid 34214939)
35. J.M. Orgogozo, S. Gilman, J.F. Dartigues, B. Laurent, M. Puel, L.C. Kirby, P. Jouanny, B. Dubois, L. Eisner, S. Flitman, B.F. Michel, M. Boada, A. Frank, and C. Hock Subacute meningoencephalitis in a subset of patients with AD after Abeta42 immunization Neurology 61 2003 46 54 (Pubitemid 36818745)
36. J.J. Palop, B. Jones, L. Kekonius, J. Chin, G.Q. Yu, J. Raber, E. Masliah, and L. Mucke Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer's disease-related cognitive deficits Proc. Natl. Acad. Sci. USA 100 2003 9572 9577 (Pubitemid 37033969)
37. C.G. Parsons, W. Danysz, and G. Quack Memantine is a clinically well tolerated N-methyl-D-aspartate (NMDA) receptor antagonist - a review of preclinical data Neuropharmacology 38 1999 735 767 (Pubitemid 29187336)
38. P. Piguet, and M. Galvan Transient and long-lasting actions of 5-HT on rat dentate gyrus neurones in vitro J. Physiol. 481 1994 629 639 (Pt 3)
39. N. Pitsikas, A. Brambilla, and F. Borsini DAU 6215, a novel 5-HT3 receptor antagonist, improves performance in the aged rat in the Morris water maze task Neurobiol. Aging 14 1993 561 564
40. J. Prickaerts, N.P. van Goethem, R. Chesworth, G. Shapiro, F.G. Boess, C. Methfessel, O.A. Reneerkens, D.G. Flood, D. Hilt, M. Gawryl, S. Bertrand, D. Bertrand, and G. Konig EVP-6124, a novel and selective alpha7 nicotinic acetylcholine receptor partial agonist, improves memory performance by potentiating the acetylcholine response of alpha7 nicotinic acetylcholine receptors Neuropharmacology 62 2012 1099 1110
41. Z. Rakonczay Potencies and selectivities of inhibitors of acetylcholinesterase and its molecular forms in normal and Alzheimer's disease brain Acta Biol. Hung. 54 2003 183 189 (Pubitemid 37105630)
42. G. Rammes, R. Rupprecht, U. Ferrari, W. Zieglgansberger, and C.G. Parsons The N-methyl-D-aspartate receptor channel blockers memantine, MRZ 2/579 and other amino-alkyl-cyclohexanes antagonise 5-HT(3) receptor currents in cultured HEK-293 and N1E-115 cell systems in a non-competitive manner Neurosci. Lett. 306 2001 81 84 (Pubitemid 32524303)
43. S. Reagan-Shaw, M. Nihal, and N. Ahmad Dose translation from animal to human studies revisited FASEB J. 22 2008 659 661 (Pubitemid 351348146)
44. F. Revah, D. Bertrand, J.L. Galzi, A. Devillers-Thiery, C. Mulle, N. Hussy, S. Bertrand, M. Ballivet, and J.P. Changeux Mutations in the channel domain alter desensitization of a neuronal nicotinic receptor Nature 353 1991 846 849 (Pubitemid 21912638)
45. N. Ropert, and N. Guy Serotonin facilitates GABAergic transmission in the CA1 region of rat hippocampus in vitro J. Physiol. 441 1991 121 136
46. M.N. Sabbagh Drug development for Alzheimer's disease: where are we now and where are we headed? Am. J. Geriatr. Pharmacother. 7 2009 167 185
47. P. Seguela, J. Wadiche, K. Dineley-Miller, J.A. Dani, and J.W. Patrick Molecular cloning, functional properties, and distribution of rat brain alpha 7: a nicotinic cation channel highly permeable to calcium J. Neurosci. 13 1993 596 604 (Pubitemid 23045143)
48. A. Serrano-Pozo, C.M. William, I. Ferrer, E. Uro-Coste, M.B. Delisle, C.A. Maurage, C. Hock, R.M. Nitsch, E. Masliah, J.H. Growdon, M.P. Frosch, and B.T. Hyman Beneficial effect of human anti-amyloid-beta active immunization on neurite morphology and tau pathology Brain 133 2010 1312 1327
49. S. Shimohama, and T. Kihara Nicotinic receptor-mediated protection against beta-amyloid neurotoxicity Biol. Psychiatry 49 2001 233 239 (Pubitemid 32178432)
50. K. Simpson, C.M. Spencer, and K.J. McClellan Tropisetron: an update of its use in the prevention of chemotherapy-induced nausea and vomiting Drugs 59 2000 1297 1315 (Pubitemid 30410146)
51. S.M. Sine, and A.G. Engel Recent advances in Cys-loop receptor structure and function Nature 440 2006 448 455
52. W.J. Strittmatter, and A.D. Roses Apolipoprotein E and Alzheimer's disease Annu. Rev. Neurosci. 19 1996 53 77 (Pubitemid 26080822)
53. K. Sugaya, E. Giacobini, and V.A. Chiappinelli Nicotinic acetylcholine receptor subtypes in human frontal cortex: changes in Alzheimer's disease J. Neurosci. Res. 27 1990 349 359
54. L.H. Tecott, A.V. Maricq, and D. Julius Nervous system distribution of the serotonin 5-HT3 receptor mRNA Proc. Natl. Acad. Sci. USA 90 1993 1430 1434 (Pubitemid 23058186)
55. Theendakara, V.; Patent, A.; Peters-Libeu, C.; Philpot, B.; Flores, S.; Descamps, O.; Poksay, K.; Zhang, Q.; Cailing, G.; Hart, M.; John, V.; Rao, R.; Bredesen, D.; 2013. Neuroprotective Sirtuin Ratio Reversed by ApoE4. Proc. Natl. Acad. Sci. USA 110, 18303-18308.
56. A.J. Thompson, and S.C. Lummis The 5-HT3 receptor as a therapeutic target Expert Opin. Ther. Targets 11 2007 527 540
57. K.R. Tietje, D.J. Anderson, R.S. Bitner, E.A. Blomme, P.J. Brackemeyer, C.A. Briggs, K.E. Browman, D. Bury, P. Curzon, K.U. Drescher, J.M. Frost, R.M. Fryer, G.B. Fox, J.H. Gronlien, M. Hakerud, E.J. Gubbins, S. Halm, R. Harris, R.J. Helfrich, K.L. Kohlhaas, D. Law, J. Malysz, K.C. Marsh, R.L. Martin, M.D. Meyer, A.L. Molesky, A.L. Nikkel, S. Otte, L. Pan, P.S. Puttfarcken, R.J. Radek, H.M. Robb, E. Spies, K. Thorin-Hagene, J.F. Waring, H. Ween, H. Xu, M. Gopalakrishnan, and W.H. Bunnelle Preclinical characterization of A-582941: a novel alpha7 neuronal nicotinic receptor agonist with broad spectrum cognition-enhancing properties CNS Neurosci. Ther. 14 2008 65 82
58. P.J. Tiseo, K. Foley, and L.T. Friedhoff The effect of multiple doses of donepezil HCl on the pharmacokinetic and pharmacodynamic profile of warfarin Br. J. Clin. Pharmacol. 46 1 1998 45 50 (Pubitemid 29197015)
59. J. Toyohara, and K. Hashimoto alpha7 Nicotinic receptor agonists: potential therapeutic drugs for treatment of cognitive impairments in schizophrenia and Alzheimer's disease Open Med. Chem. J. 4 2010 37 56
60. D. Van Dam, K. Coen, and P.P. De Deyn Cognitive evaluation of disease-modifying efficacy of donepezil in the APP23 mouse model for Alzheimer's disease Psychopharmacology (Berl) 197 2008 37 43
61. T.L. Wallace, P.M. Callahan, A. Tehim, D. Bertrand, G. Tombaugh, S. Wang, W. Xie, W.B. Rowe, V. Ong, E. Graham, A.V. Terry Jr.; J.S. Rodefer, B. Herbert, M. Murray, R. Porter, L. Santarelli, and D.A. Lowe RG3487, a novel nicotinic alpha7 receptor partial agonist, improves cognition and sensorimotor gating in rodents J. Pharmacol. Exp. Ther. 336 2011 242 253
62. H.Y. Wang, D.H. Lee, M.R. D'Andrea, P.A. Peterson, R.P. Shank, and A.B. Reitz beta-Amyloid(1-42) binds to alpha7 nicotinic acetylcholine receptor with high affinity. Implications for Alzheimer's disease pathology J. Biol. Chem. 275 2000 5626 5632 (Pubitemid 30115201)
63. H.Y. Wang, W. Li, N.J. Benedetti, and D.H. Lee Alpha 7 nicotinic acetylcholine receptors mediate beta-amyloid peptide-induced tau protein phosphorylation J. Biol. Chem. 278 2003 31547 31553 (Pubitemid 37048332)
64. R. Zhang, G. Xue, S. Wang, L. Zhang, C. Shi, and X. Xie Novel object recognition as a facile behavior test for evaluating drug effects in AbetaPP/PS1 Alzheimer's disease mouse model J. Alzheimers Dis. 31 2012 801 812