Propargylamine-derived multitarget-directed ligands: Fighting Alzheimer's disease with monoamine oxidase inhibitors

Journal of Neural Transmission

Volumn 120, Issue 6, 2013, Pages 893-902

  Bolea, Irene ^a   Gella, Alejandro ^b   Unzeta, Mercedes ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSITAT INTERNACIONAL DE CATALUNYA   (Spain)

Author keywords

Alzheimer's disease; Cholinesterases; Monoamine oxidase; Multitarget directed ligand; Neuroprotection; Propargylamine

Indexed keywords

CARBAMIC ACID; DONEPEZIL; GALANTAMINE; INDOLEAMINE; IRON; LADOSTIGIL; LIGAND; MEMANTINE; MONOAMINE OXIDASE INHIBITOR; NEUROPROTECTIVE AGENT; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR AGONIST; PROPARGYLAMINE; RASAGLINE; RIVASTIGMINE; SELEGILINE; TACRINE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANTIOXIDANT ACTIVITY; ARTICLE; CLINICAL TRIAL (TOPIC); DRUG STRUCTURE; HUMAN; NEUROPROTECTION; NEUROTRANSMISSION; PRIORITY JOURNAL;

ACETYLCHOLINESTERASE; ALZHEIMER DISEASE; ANIMALS; CHOLINESTERASE INHIBITORS; HUMANS; LIGANDS; MONOAMINE OXIDASE INHIBITORS; PARGYLINE; PROPYLAMINES;

EID: 84878683397     PISSN: 03009564     EISSN: 14351463     Source Type: Journal    
DOI: 10.1007/s00702-012-0948-y     Document Type: Article

References (96)

1. Alvarez XA, Cacabelos R, Sampedro C, Couceiro V, Aleixandre M, Vargas M, Linares C, Granizo E, García-Fantini M, Baurecht W, Doppler E, Moessler H (2011) Combination treatment in Alzheimer's disease: results of a randomized controlled trial with cerebrolysin and donepezil. Curr Alzheimer Res 8:583-591
2. Amit T, Avramovich-Tirosh Y, Youdim MBH, Mandel S (2008) Targeting multiple Alzheimer's disease etiologies with multimodal neuroprotective and neurorestorative iron chelators. FASEB J 22:1296-1305
3. Annweiller C, Fantino B, Parot-Schinkel E, Thiery S, Gautier J, Beauchet O (2001) Alzheimer's disease - input of vitamin D with mEmantine assay (AD-IDEA trial): study protocol for a randomized controlled trial. Trials 12:230
4. Areosa SA, Sheriff F, Mc Shane R (2005) Memantine for dementia. Cochrane Database Syst Rev (2):CD003154
5. Avramovich-Tirosh Y, Amit T, Bar-Am O, Zheng H, Fridkin M, Youdim MB (2007) Therapeutic targets and potential of the novel brain-permeable multifunctional iron chelator-monoamine oxidase inhibitor drug, M30, for the treatment of Alzheimer's disease. J Neurochem 100(2):490-502
6. Baker GB, Reynolds GP (1989) Biogenic amines and their metabolites in Alzheimer's disease: noradrenaline, 5-hydroxytryptamine and 5-hydroxyindole-3- acetic acid are depleted in the hippocampus but not in substantia innominata. Neurosci Lett 100:335-339
7. Ballard C, Day S, Sharp S, Wing G, Sorensen S (2008) Neuropsychiatric symptoms in dementia: importance and treatment considerations. Int Rev Psychiatry 20(4):396-404 Review
8. Bar-Am O, Weinreb O, Amit T, Youdim MB (2005) Regulation of Bcl-2 family proteins, neurotrophic factors, and APP processing in the neurorescue activity of propargylamine. FASEB J 19:1899-1901
9. Bartus RT, Dean RL, Beer B, Lippa AS (1982) The cholinergic hypotheses of geriatric memory dysfunction. Science 217:408-414
10. Battaglia V, Sanz E, Salvi M, Unzeta M, Toninello A (2006) Protective effect of PF9601N on mitochondrial permeability transition pore. Cell Mol Life Sci 63:1440-1448
11. Bayer A, Reban J (2004) Alzheimer's disease and relative conditions. MEDEA Press, Czech Republic, pp 3-330
12. Binda C, Milczek EM, Bonivento D, Wang J, Mattevi A, Edmonson DE (2011) Lights and shadows on monoamine oxidase inhibition in neuroprotective pharmacological therapies. Curr Top Med Chem 11:2788-2796
13. Birks J and Harvey R (2006) Donepezil for dementia due to Alzheimer's disease. Cochrane Database Syst Rev (1):CD001190
14. Birks J, Grimley EJ, Iakovidou V, Tsolaki M (2000) Rivastigmine for Alzheimer's disease. Cochrane Database Syst Rev (4):CD001191
15. Bolea I, Juárez-Jiménez J, de Los Ríos C, Chioua M, Pouplana R, Luque FJ, Unzeta M, Marco-Contelles J, Samadi A (2011) Synthesis, biological evaluation and molecular modelling of donepezil and N-[(5-(benzyloxy)-1-methyl-1H-indol-2-yl)methyl]-N-methylprop-2-yn-1-amine hybrids as new multipotent cholinesterase/monoamine oxidase inhibitors for the treatment of Alzheimer's disease. J Med Chem 54:8251-8270
16. Bolognesi ML, Cavalli A, Melchiorre C (2009) Mamoquin: a multi-target directed ligand as an innovative therapeutic opportunity for Alzheimer's disease. Neurotherapeutics 6:152-162
17. Buccafusco JJ, Terry AV Jr (2000) Multiple central nervous system targets for eliciting beneficial effects on memory and cognition. J Pharmacol Exp Ther 295(2):438-446
18. Burke WJ, Li SW, Chung HD, Ruggiero DA, Kristal BS, Johnson EM, Lampe P, Kumar VB, Franko M, Williams EA, Zahm DS (2004) Neurotoxicity of MAO metabolites of catecholamine neurotransmitters: role in neurodegenerative diseases. Neurotoxicology 25:101-115
19. Callingham BA (1993) Drug interactions with reversible monoamine oxidase-A inhibitors. Clin Neuropharmacol 16:S42-S50
20. Caraci F, Copani A, Nicoletti F, Drago F (2010) Depression and Alzheimer's disease: neurobiological links and common pharmacological targets. Eur J Pharmacol 626:64-71
21. Carradori S, Secci D, Bolasco A, Chimenti P, D'Ascenzio M (2012) Patent-related survey on new monoamine oxidase inhibitors and their therapeutic potential. Expert Opin Ther Pat 22:759-801
22. Carrillo MC, Minami C, Kitani K, Mayurama W, Ohashi K, Yamamoto T, Naoi M, Kanai S, Youdim MB (2000) Enhancing effect of rasagiline on superoxide dismutase and catalase activities in the dopaminergic system in the rat. Life Sci 67:577-585
23. Cavalli A, Bolognesi ML, Minarini A, Rosini M, Tumiatti V, Melchiorre C (2008) Multi-target-directed ligands to combat neurodegenerative diseases. J Med Chem 51(3):347-372
24. Cesura AM, Pletscher A (1992) The new generation of moamine oxidase inhibitors. Prog Drug Res 38:171-297
25. Chen JJ, Swope DM, Dashtipour K (2007) Comprehensive review of rasagiline, a second-generation monoamine oxidase inhibitor, for the treatment of Parkinson's disease. Clin Ther 29:1825-1849
26. Cho W, Maruff P, Connell J, Gargano C, Calder N, Doran S, Fox-Bosetti S, Hassan A, Renger J, Herman G, Lines C, Verma A (2011) Additive effects of a cholinesterase inhibitor and histamine inverse agonist on scopolamine deficits in humans. Psychopharmacology 218:513-524
27. Coyle JT, Puttfarcken P (1993) Oxidative stress, glutamate and neurodegenerative disorders. Science 262:689-695
28. Cross AJ (1990) Serotonin in Alzheimer type dementia and other dementing illnesses. Ann N Y Acad Sci 600:405-415
29. Cutillas B, Ambrosio S, Unzeta M (2002) Neuroprotective effect of the monoamine oxidase inhibitor PF9601N on rat nigral neurons after 6-hydroxydopamine-striatal lesion. Neurosci Letters 329:165-168
30. Davies P, Maloney AJ (1976) Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet 2:1403
31. De Ferrari GV, Canales MA, Shin I, Weiner LM, Silman I, Inestrosa NC (2001) A structural motif of acetylcholinesterase that promotes amyloid beta-peptide fibril formation. Biochemistry 40:10447-10457
32. Dinamarca MC, Sagal JP, Quintanilla RA, Godoy JA, Arrázola MS, Inestrosa NC (2010) Amyloid-beta-acetylcholinesterase complexes potentiate neurodegenerative changes induced by the abeta peptide. Implications for the pathogenesis of Alzheimer's disease. Mol Neurodegener 5:4
33. 2 muscarinic receptor. J Med Chem 50:5685-5695
34. Fang L, Appenroth D, Decker M, Kiehntopf M, Roegler C, Deufel T, Fleck C, Peng S, Zhang Y, Lehmann J (2008) Synthesis and biological evaluation of NO-donor-tacrine hybrids as hepatoprotective anti-Alzheimer drug candidates. J Med Chem 51:713-716
35. Fink DM, Palermo MG, Bores GM et al (1996) Imino 1,2,3,4- tetrahydrocyclopent[b]indole carbamates as dual inhibitors of acetylcholinesterase and monoamine oxidase. Bioorg Med Chem Lett 6:625-630
36. Gal S, Zheng H, Fridkin M, Youdim MB (2005) Novel multifunctional neuroprotective iron-chelator-monoamine oxidase inhibitor drugs for neurodegenerative diseases. In vivo selective brain monoamine oxidase inhibition and prevention of MPTP-induced striatal dopamine depletion. J Neurochem 95:79-88
37. Gella A and Bolea I (2011) Oxidative stress in Alzheimer's disease: pathogenesis, biomarkers and therapy, Alzheimer's disease pathogenesis-core concepts, shifting paradigms and therapeutic targets, Suzanne De La Monte (Ed.), ISBN: 978-953-307-690-4, InTech, Available from: http://www.intechopen.com/ books/alzheimer-s-disease-pathogenesis-core-concepts-shifting-paradigms-and- therapeutic-targets/oxidative-stress-in-alzheimer-s-disease-pathogenesis- biomarkers-and-therapy
38. Gella A, Durany N (2009) Oxidative stress in Alzheimer's disease. Cell Adh Migr 3:88-93
39. Geula C and Mesulam MM (1999) In: Terry R, Katzman R, Bick K, Sisodia SS (eds) Alzheimer disease, 2nd edn. Lippincot Williams & Wilkins, Philadelphia, pp 269-292
40. Glenner GG, Murphy MA (1989) Amyloidosis of the nervous system. J Neurol Sci 94(1-3):1-28
41. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA (1989) Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3(4):519-526
42. Greig NH, Utsuki T, Ingram DK, Wang Y, Pepeu G, Scali C, Yu QS, Mamczarz J, Holloway HW, Giordano T, Chen D, Furukawa K, Sambamurti K, Brossi A, Lahiri DK (2005) Selective butyrylcholinesterase inhibition elevates brain acetylcholine, augments learning and lowers Alzheimer beta-amyloid peptide in rodent. Proc Natl Acad Sci USA 102(47):17213-17218
43. Grundke-Iqbal I, Iqbal K, Tung YC, Quinlan M, Wisniewski HM, Ll Binder (1986) Abnormal phosphorylation of the microtubule-associated protein τ (tau) in Alzheimer cystoskeletal pathology. Proc Natl Acad Sci USA 83(13):4913-4917
44. Gualtiery CT, Morgan DW (2008) The frequency of cognitive impairment in patients with anxiety, depression, and bipolar disorder: an unaccounted source of variance in clinical trials. J Clin Psychiatry 69(7):1122-1130
45. Harrington C, sawchak S, Chiang C, Davies J, Donovan C, Saunders AM, Irizarry M, Jeter B, Zvartau-Hind M, van Dyck CH, Gold M (2011) Rosiglitazone does not improve cognition or global functions when used as adjunctive therapy to AchE inhibitors in mild-to-moderate Alzheimer's disease: two-phase studies. Curr Alzheimer Res 8:592-606
46. Huang X, Moir RD, Tanzi RE, Bush AI, Rogers JT (2004) Redox-active metals, oxidative stress and Alzheimer's disease pathology. Ann Y Acad Sci 1012:153-163
47. Inestrosa NC, Alvarez A, Pérez CA, Moreno RD, Vicente M, Linker C, Casanueva OI, Soto C, Garrido J (1996) Acetylcholinestearse accelerates assembly of amyloid-beta-peptides into Alzheimer's fibrils: possible role of the peripheral site of the enzyme. Neuron 16:881-891
48. Johnston JP (1968) Some observations upon a new inhibitor of monoamine oxidase in brain tissue. Biochem Pharmacol 17(7):1285-1297
49. Kristal BS, Conway AD, Brown AM, Jain JC, Ulluci PA, Li SW, Burke WJ (2001) Selective dopaminergic vulnerability: 3,4-dihydroxyphenylacetaldehyde targets mitochondria. Free Radic Biol Med 30:924-931
50. Lamensdorf I, Eisenhofer G, Harvey-White J, Nechustan A, Kirk K, Kopin IJ (2000) 3,4-dihydroxyphenylacetaldehyde potentiates the toxic effects of metabolic stress in PC12 cells. Brain Res 868:191-201
51. Loy C and Schneider L (2004) Galantamine for Alzheimer's disease. Cochrane Database Syst Rev (4):CD001747
52. Mattson MP (2004) Metal-catalysed disruption of membrane protein and lipid signalling in the pathogenesis of neurodegenerative disorders. Ann N Y Acad Sci 1012:37-50
53. ®-aminoindan, and its optical (S)-isomer, TV1022. Ann NY Acad Sci 939:320-329
54. Mishizen-Eberz AJ, Rissman RA, Carter TL, Ikonomovic MD, Wolfe BB, Armstrong DM (2004) Biochemical and molecular studies of NMDA receptor subunits NR1/2A/2B in hippocampal subregions throughout progression of Alzheimer's disease pathology. Neurobiol Dis 15:80-92
55. Morris MC, Evans DA, Tagney CC (2005) Relation of the tocopherol forms to incident Alzheimer disease and to cognitive change. Am J Clin Nutr 81:508-514
56. Naoi M, Maruyama W, Yi H, Akao Y, Yamaoka Y, Shamoto-Nagai M (2007) Neuroprotection by propargylamines in Parkinson's disease: intracellular mechanism underlying the anti-apoptotic function and search for clinical markers. J Neural Transm Suppl 72:121-131
57. Patel L, Grossberg GT (2011) Combination therapy for Alzheimer's disease. Drugs Aging 28:539-546
58. Pérez V, Unzeta M (2003) PF9601N, a new MAO-B inhibitor, attenuates MPTP-induced depletion of striatal dopamine levels in C57/BL6 mice. Neurochem Int 42:221-239
59. Pérez V, Romera M, Lizcano JM, Marco JL, Unzeta M (2003) Protective effect PF9601N, a novel MAO-B inhibitor, on dopamine-lesioned PC12 cultured cells. J Pharm Pharmacol 55:713-716
60. Perry EK, Perry RH, Blessed G, Tomlinson BE (1977) Necropsy evidence of central cholinergic deficits in senile dementia. Lancet 1:189
61. Perry G, Raina AK, Nunomura A, Wataya T, Sayre LM, Smith MA (2000) How important is oxidative damage? Lessons from Alzheimer's disease. Free Radic Biol Med 28(5):831-834
62. Prat G, Perez V, Rubi A, Casas M, Unzeta M (2000) The novel type B MAO inhibitor PF9601N enhances the duration of l-DOPA-induced contralateral turning in 6-hydroxydopamine lesioned rats. J Neural Transm 107:409-417
63. Rapp MA, Schnaider-Beeri M, Purohit DP, Perl DP, Haroutunian V, Sano M (2008) Increased neurofibrillary tangles in patients with Alzheimer's disease with comorbid depression. Am J Geriatr Psychiatry 16(2):168-174
64. Riederer P, Danyelczyk W, Grunblat E (2004) Monoamine oxidase inhibition in Alzheimer's disease. Neurotoxicology 25:271-277
65. Rodríguez-Franco MI, Fernández-Bachiller MI, Pérez C, Castro A, Martínez A (2005) Design and synthesis of N-benzylpiperidine-purine derivatives as new dual inhibitors of acetyl- and butyrylcholinesterase. Bioorg Med Chem 13:6795-6802
66. 1- adrenoreceptors. J Med Chem 46:4895-4903
67. Sagi Y, Weinstock M, Youdim MB (2003) Attenuation of MPTP-induced dopaminergic neurotoxicity by TV3326, a cholinesterase-monoamine oxidase inhibitor. J Neurochem 86(2):290-297
68. +-treated SH-SY5Y human dopaminergic cells. J Neurochem 105:2404-2417
69. Sanz E, Quintana A, Hidalgo J, Marco JL, Unzeta M (2009) PF9601N confers MAO-B independent neuroprotection in ER-stress-induced cell death. Mol Cell Neurosci 41:19-31
70. Saura J, Andres N, Andrade C et al (1997) Biphasic and region-specific MAO-B response to aging in normal human brain. Neurobiol Aging 18:497-507
71. Shoham S, Youdim BMH (2000) Iron involvement in neural damage and microgliosis in models of neurodegenerative diseases. Cell Mol Biol 46:743-760
72. Sterling J, Herzig Y, Goren T, Finkelstein N, Lerner D, Goldenberg W, Mikcolczi I, Molnar S, Rantal F, Tamas T, Toth G, Zagyva A, Zekany A, Finberg J, Lavian G, Gross A, Friedman R, Razin M, Huang W, Krais B, Chorev M, Youdim MB, Weinstock M (2002) Novel dual inhibitors of AChE and MAO derived from hydroxy aminoindan and phenethylamine as potential treatment for Alzheimer's disease. J Med Chem 54:5260-5279
73. Swerdlow RH, Khan SM (2009) The Alzheimer's disease mitochondrial cascade hypotheses: an update. Exp Neurol 218:308-315
74. Tatton W, Chalmers-Redman R, Tatton N (2003) Neuroprotection by deprenyl and other propargylamines: glyceraldehyde-3-phosphate dehydrogenase rather than monoamine oxidase B. J Neural Transm 110:509-515
75. Terry RD, Gonatas NK, Weiss M (1964) Ultrastructural studies in Alzheimer's presenile dementia. Ann J Pathol 44:269-297
76. Thomas T (2000) Monoamine oxidase B inhibitors in the treatment of Alzheimer's disease. Neurobiol Aging 21(2):343-348 Review
77. Tipton KF, Boyce S, O'Sullivan J, Davey GP, Healey J (2004) Monoamine oxidases: certainties and uncertainties. Curr Med Chem 11:1965-1982
78. Tsolaki M, Kokarida K, Iakovidou V, Stilopoulus E, Meimaris J, Kazis A (2001) Extrapyramidal symptoms and signs in Alzheimer's disease: prevalence and correlation with the first symptom. Am J Alzheimer Dis Other Demen 16:268-278
79. Tsunekawa H, Noda Y, Mouri A, Yoneda F, Nameshiba T (2008) Synergistic effects of selegiline and donepezil on cognitive impaitment induced by amyloid beta (25-35). Behav Brain Res 190:224-232
80. Valoti M (2007) CYP-dependent metabolism of PF9601N, a new monoamine oxidase-B inhibitor, by C57BL/6 mouse and human liver microsomes. J Pharm Pharm Sci 10:473-485
81. Van der Schyf CJ, Gal S, Geldenhuys WJ, Youdim MBH (2006) Multifunctional neuroprotective drugs targeting monoamine oxidase inhibition, iron chelation, adenosine receptors, and cholinergic and glutamatergic action for neurodegenerative disorders. Expert Opin Investig Drugs 15(8):873-886
82. Viayna E, Gómez T, Galdeano C, Ramírez L, Ratia M, Badia A, Clos MV, Verdaguer E, Junyent F, Camins A, Pallàs M, Bartolini M, Mancini F, Andrisano V, Arce MP, Rodríguez-Franco MI, Bidon-Chanal A, Luque FJ, Camps P, Muñoz-Torrero D (2010) Novel huprine derivatives with inhibitory activity toward β-amyloid aggregation and formation as disease-modifying anti-Alzheimer drug candidates. Chem Med Chem 5:1855-1870
83. Waldholdz M (1993) FDA approves sale of Cognex for Alzheimer's, WSJ. 10 Sep, B5
84. Weinreb O, Amit T, Bar-Am O, Sagi Y, Mandel S, Youdim MB (2006) Involvement of multiple survival signal transduction pathways in the neuroprotective, neurorescue and APP processing activity of rasagiline and its propargyl moiety. J Neural Transm Suppl 70:457-465
85. Weinstock M, Gorodetsky E, Poltyrev T, Gross A, Sagi Y, Youdim M (2003) A novel cholinesterase and brain-selective monoamine oxidase inhibitor for the treatment of dementia comorbid with depression and Parkinson's disease. Prog Neuropsychopharmacol Biol Psychiatry 27(4):555-561 Review
86. Wimo A, Jönsson L, Gustavsson A, McDaid D, Ersek K (2010) The economic impact of dementia in Europe in 2008-cost estimates from the Eurocode project. Int J Ger Psychiatr 26:825-832
87. Yogev-Falach M, Amit T, Bar-Am O, Weinstock M, Youdim MB (2002) Involvement of MAP kinase in the regulation of amyloid precursor protein processing by novel cholinesterase inhibitors derived from rasagiline. FASEB J 16(12):1674-1676
88. Yoshiije Y, Tanemura K, Murayama O, Akagi T, Murayama M, Sato S, Sun X, Tanaka N, Takashima A (2001) New insights on how metals disrupt amyloid β aggregation and their effects on amyloid β cytotoxicity. J Biol Chem 276:32293-32299
89. Youdim MHB, Buccafusco JJ (2005) CNS Targets for multi-functional drugs in the treatment of Alzheimer's and Parkinson's diseases. J Neural Transm 112(4):519-537
90. Youdim MBH, Weinstock M (2001) Molecular basis of neuroprotective activities of rasagiline and the anti-Alzheimer drug TV3326 [(N-propargyl-(3R) aminoindan-5-yl)-ethyl methyl carbamate]. Cell Mol Neurobiol 21:555-573
91. Youdim MBH, Finberg JPM, Tipton KF (1988) Monoamine oxidase. In: Tredelenburg U, Weiner N (eds) Handbook of experimental pharmacology. Springer, Berlin, pp 119-192
92. Youdim MB, Fridkin M, Zheng H (2004) Novel bifunctional drugs targeting monoamine oxidase inhibition and iron chelation as an approach to neuroprotection in Parkinson's disease and other neurodegenerative diseases. J Neural Transm 111:1455-1471
93. Youdim MB, Amit T, Bar-Am O, Weinreb O, Yogev-Falach M (2006) Implications of co-morbidity for etiology and treatment of neurodegenerative diseases with multifunctional neuroprotective-neurorescue drugs: ladostigil. Neurotoxic Res 10:181-192
94. Zheng H, Gal S, Weiner LM, Bar-Am O, Warshawsky A, Fridkin M, Youdim MB (2005) Novel multifunctional neuroprotective iron chelator-monoamine oxidase inhibitor drugs for neurodegenerative diseases: in vitro studies on antioxidant activity, prevention of lipid peroxide formation and monoamine oxidase inhibition. J Neurochem 95:68-78
95. Zheng H, Youdim MBH, Fridkin M (2009) Site-activated multifunctional chelator with acetylcholinesterase and neuroprotective/neurorestorative moieties for Alzheimer's therapy. J Med Chem 52:4095-4098
96. Zheng H, Youdim MB, Fridkin M (2010) Site-activated chelators targeting AChE and MAO for Alzheimer's therapy. ACS Chem Biol 5:603