Neurotrophic and Neuroprotective Actions of (-)- and (+)-Phenserine, Candidate Drugs for Alzheimer's Disease

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Lilja, Anna M ^a,b   Luo, Yu ^c   Yu, Qian Sheng ^b   Röjdner, Jennie ^a   Li, Yazhou ^b   Marini, Ann M ^d   Marutle, Amelia ^a   Nordberg, Agneta ^a   Greig, Nigel H ^b  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b NATIONAL INSTITUTE ON AGING   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; DOUBLECORTIN; DRUG METABOLITE; GLUTAMIC ACID; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; N1 NORPHENSERINE; N1,N8 BISNORPHENSERINE; N8 NORPHENSERINE; PHENSERINE; PROTEIN KINASE C; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL SIZE; CELL SURVIVAL; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; DRUG ACTIVITY; DRUG EFFICACY; DRUG MECHANISM; DRUG STRUCTURE; EMBRYO; ENANTIOMER; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MOUSE; NERVE CELL CULTURE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROPROTECTION; NEUROTROPHIC ACTIVITY; NONHUMAN; OXIDATIVE STRESS; SUBVENTRICULAR ZONE; TRANSGENIC MOUSE; WILD TYPE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG DISCOVERY; GENE EXPRESSION REGULATION; HUMANS; MICE; MICE, TRANSGENIC; MUTATION; NEURAL STEM CELLS; NEURONS; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; PHYSOSTIGMINE; STEREOISOMERISM;

EID: 84873824885     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054887     Document Type: Article

References (59)

1. Brookmeyer R, Johnson E, Ziegler-Graham K, Arrighi HM, (2007) Forecasting the global burden of Alzheimer's disease. Alzheimers Dement 3: 186-191.
2. Jonsson L, Wimo A, (2009) The cost of dementia in Europe: a review of the evidence, and methodological considerations. Pharmacoeconomics 27: 391-403.
3. Pouryamout L, Dams J, Wasem J, Dodel R, Neumann A, (2012) Economic evaluation of treatment options in patients with Alzheimer's disease: a systematic review of cost-effectiveness analyses. Drugs 72: 789-802.
4. Becker RE, Greig NH, (2010) Lost in translation: neuropsychiatric drug development. Sci Transl Med 2: 61rv66.
5. Alzheimer's Association *Corr. authors Thies W, Bleiler L, (2012) 2012 Alzheimer's disease facts and figures. Alzheimers Dement 8: 131-168.
6. Corbett A, Ballard C, (2012) New and emerging treatments for Alzheimer's disease. Expert Opin Emerg Drugs 17: 147-156.
7. Ashe KH, Zahs KR, (2010) Probing the biology of Alzheimer's disease in mice. Neuron 66: 631-645.
8. Claeysen S, Cochet M, Donneger R, Dumuis A, Bockaert J, et al. (2012) Alzheimer culprits: Cellular crossroads and interplay. Cell Signal.
9. Sambamurti K, Suram A, Venugopal C, Prakasam A, Zhou Y, et al. (2006) A partial failure of membrane protein turnover may cause Alzheimer's disease: a new hypothesis. Curr Alzheimer Res 3: 81-90.
10. Lahiri DK, Ge YW, Rogers JT, Sambamurti K, Greig NH, et al. (2006) Taking down the unindicted co-conspirators of amyloid beta-peptide-mediated neuronal death: shared gene regulation of BACE1 and APP genes interacting with CREB, Fe65 and YY1 transcription factors. Curr Alzheimer Res 3: 475-483.
11. Sambamurti K, Greig NH, Lahiri DK, (2002) Advances in the cellular and molecular biology of the beta-amyloid protein in Alzheimer's disease. Neuromolecular Med 1: 1-31.
12. Connor B, Young D, Yan Q, Faull RL, Synek B, et al. (1997) Brain-derived neurotrophic factor is reduced in Alzheimer's disease. Brain Res Mol Brain Res 49: 71-81.
13. Huang EJ, Reichardt LF, (2001) Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24: 677-736.
14. Niewiadomska G, Mietelska-Porowska A, Mazurkiewicz M, (2011) The cholinergic system, nerve growth factor and the cytoskeleton. Behav Brain Res 221: 515-526.
15. Cuello AC, Bruno MA, Allard S, Leon W, Iulita MF, (2010) Cholinergic involvement in Alzheimer's disease. A link with NGF maturation and degradation. J Mol Neurosci 40: 230-235.
16. Rao MS, Hattiangady B, Shetty AK, (2006) The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell 5: 545-558.
17. Rothman SM, Mattson MP, (2010) Adverse stress, hippocampal networks, and Alzheimer's disease. Neuromolecular Med 12: 56-70.
18. Winblad B, Giacobini E, Frolich L, Friedhoff LT, Bruinsma G, et al. (2010) Phenserine efficacy in Alzheimer's disease. J Alzheimers Dis 22: 1201-1208.
19. Becker RE, Greig NH (2012) Fire in the ashes: Can failed Alzheimer's disease drugs succeed with second chances? Alzheimers Dement.
20. Maccecchini ML, Chang MY, Pan C, John V, Zetterberg H, et al. (2012) Posiphen as a candidate drug to lower CSF amyloid precursor protein, amyloid-beta peptide and tau levels: target engagement, tolerability and pharmacokinetics in humans. J Neurol Neurosurg Psychiatry.
21. Greig NH, Sambamurti K, Yu QS, Brossi A, Bruinsma GB, et al. (2005) An overview of phenserine tartrate, a novel acetylcholinesterase inhibitor for the treatment of Alzheimer's disease. Curr Alzheimer Res 2: 281-290.
22. Lahiri DK, Chen D, Maloney B, Holloway HW, Yu QS, et al. (2007) The experimental Alzheimer's disease drug posiphen [(+)-phenserine] lowers amyloid-beta peptide levels in cell culture and mice. J Pharmacol Exp Ther 320: 386-396.
23. Mikkilineni S, Cantuti-Castelvetri I, Cahill CM, Balliedier A, Greig NH, et al. (2012) The anticholinesterase phenserine and its enantiomer posiphen as 5′untranslated-region-directed translation blockers of the Parkinson's alpha synuclein expression. Parkinsons Dis 2012: 142372.
24. Shaw KT, Utsuki T, Rogers J, Yu QS, Sambamurti K, et al. (2001) Phenserine regulates translation of beta-amyloid precursor protein mRNA by a putative interleukin-1 responsive element, a target for drug development. Proc Natl Acad Sci U S A 98: 7605-7610.
25. Kadir A, Andreasen N, Almkvist O, Wall A, Forsberg A, et al. (2008) Effect of phenserine treatment on brain functional activity and amyloid in Alzheimer's disease. Ann Neurol 63: 621-631.
26. Marutle A, Ohmitsu M, Nilbratt M, Greig NH, Nordberg A, et al. (2007) Modulation of human neural stem cell differentiation in Alzheimer (APP23) transgenic mice by phenserine. Proc Natl Acad Sci U S A 104: 12506-12511.
27. Sugaya K, Kwak YD, Ohmitsu O, Marutle A, Greig NH, et al. (2007) Practical issues in stem cell therapy for Alzheimer's disease. Curr Alzheimer Res 4: 370-377.
28. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, et al. (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274: 99-102.
29. Luo Y, Kuo CC, Shen H, Chou J, Greig NH, et al. (2009) Delayed treatment with a p53 inhibitor enhances recovery in stroke brain. Ann Neurol 65: 520-530.
30. Lambert DG, Nahorski SR, (1990) Second-messenger responses associated with stimulation of neuronal muscarinic receptors expressed by a human neuroblastoma SH-SY5Y. Prog Brain Res 84: 31-42.
31. Vaughan PF, Peers C, Walker JH, (1995) The use of the human neuroblastoma SH-SY5Y to study the effect of second messengers on noradrenaline release. Gen Pharmacol 26: 1191-1201.
32. Su B, Wang X, Nunomura A, Moreira PI, Lee HG, et al. (2008) Oxidative stress signaling in Alzheimer's disease. Curr Alzheimer Res 5: 525-532.
33. Curtis MA, Low VF, Faull RL, (2012) Neurogenesis and progenitor cells in the adult human brain: A comparison between hippocampal and subventricular progenitor proliferation. Dev Neurobiol 72: 990-1005.
34. Francis F, Koulakoff A, Boucher D, Chafey P, Schaar B, et al. (1999) Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23: 247-256.
35. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O, (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8: 963-970.
36. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, et al. (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467: 1-10.
37. Jin K, Peel AL, Mao XO, Xie L, Cottrell BA, et al. (2004) Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci U S A 101: 343-347.
38. Ziabreva I, Perry E, Perry R, Minger SL, Ekonomou A, et al. (2006) Altered neurogenesis in Alzheimer's disease. J Psychosom Res 61: 311-316.
39. Wicklund L, Leao RN, Stromberg AM, Mousavi M, Hovatta O, et al. (2010) beta-Amyloid 1-42 Oligomers Impair Function of Human Embryonic Stem Cell-Derived Forebrain Cholinergic Neurons. PLoS One 5: e15600.
40. Autry AE, Monteggia LM, (2012) Brain-derived neurotrophic factor and neuropsychiatric disorders. Pharmacol Rev 64: 238-258.
41. Ming GL, Song H, (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28: 223-250.
42. Hock C, Heese K, Hulette C, Rosenberg C, Otten U, (2000) Region-specific neurotrophin imbalances in Alzheimer disease: decreased levels of brain-derived neurotrophic factor and increased levels of nerve growth factor in hippocampus and cortical areas. Arch Neurol 57: 846-851.
43. Narisawa-Saito M, Wakabayashi K, Tsuji S, Takahashi H, Nawa H, (1996) Regional specificity of alterations in NGF, BDNF and NT-3 levels in Alzheimer's disease. Neuroreport 7: 2925-2928.
44. Nagahara AH, Merrill DA, Coppola G, Tsukada S, Schroeder BE, et al. (2009) Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer's disease. Nat Med 15: 331-337.
45. Lu Y, Christian K, Lu B, (2008) BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol Learn Mem 89: 312-323.
46. Nikolaev A, McLaughlin T, O'Leary DD, Tessier-Lavigne M, (2009) APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 457: 981-989.
47. Vivar C, Potter MC, Choi J, Lee JY, Stringer TP, et al. (2012) Monosynaptic inputs to new neurons in the dentate gyrus. Nat Commun 3: 1107.
48. Jin K, Xie L, Mao XO, Greenberg DA, (2006) Alzheimer's disease drugs promote neurogenesis. Brain Res 1085: 183-188.
49. Skarpen E, Flinder LI, Rosseland CM, Orstavik S, Wierod L, et al. (2008) MEK1 and MEK2 regulate distinct functions by sorting ERK2 to different intracellular compartments. FASEB J 22: 466-476.
50. Ussar S, Voss T, (2004) MEK1 and MEK2, different regulators of the G1/S transition. J Biol Chem 279: 43861-43869.
51. Nelson TJ, Sun MK, Hongpaisan J, Alkon DL, (2008) Insulin, PKC signaling pathways and synaptic remodeling during memory storage and neuronal repair. Eur J Pharmacol 585: 76-87.
52. Perry G, Cash AD, Smith MA, (2002) Alzheimer Disease and Oxidative Stress. J Biomed Biotechnol 2: 120-123.
53. Mattson MP, (2004) Pathways towards and away from Alzheimer's disease. Nature 430: 631-639.
54. Bailey JA, Ray B, Greig NH, Lahiri DK, (2011) Rivastigmine lowers Abeta and increases sAPPalpha levels, which parallel elevated synaptic markers and metabolic activity in degenerating primary rat neurons. PLoS One 6: e21954.
55. Larson ME, Lesne SE, (2012) Soluble Abeta oligomer production and toxicity. J Neurochem 120Suppl 1: 125-139.
56. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, et al. (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440: 352-357.
57. Perry EK, Johnson M, Ekonomou A, Perry RH, Ballard C, et al. (2012) Neurogenic abnormalities in Alzheimer's disease differ between stages of neurogenesis and are partly related to cholinergic pathology. Neurobiol Dis.
58. Mattson MP, (2008) Glutamate and neurotrophic factors in neuronal plasticity and disease. Ann N Y Acad Sci 1144: 97-112.
59. Yu QS, Reale M, Kamal M, Holloway HW, Luo W, et al. (2013) Synthesis of the Alzheimer drug Posiphen into its primary metabolic products (+)-N1-norPosiphen, (+)-N8-norPosiphen and (+)-N1, N8-bisnorPosiphen, their inhibition of amyloid precursor protein, α-synuclein synthesis, interleukin-1β release, and cholinergic action. Anti-Inflamm Anti-Allergy Agents Med Chem in press.