Effect of long-term treatment with rasagiline on cognitive deficits and related molecular cascades in aged mice

Neurobiology of Aging

Volumn 36, Issue 9, 2015, Pages 2628-2636

  Weinreb, Orly ^a   Badinter, Felix ^a   Amit, Tamar ^a   Bar Am, Orit ^a   Youdim, Moussa B H ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Aging; Antidepressant like behavior; Cognition; Neuroprotection; Neurotrophic parameters; Rasagiline

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CATALASE; DOPAMINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; MESSENGER RNA; MONOAMINE OXIDASE B INHIBITOR; PROTEIN BAX; PROTEIN BCL 2; RASAGILINE; SEROTONIN; SYNAPSIN I; AMINE OXIDASE (FLAVIN CONTAINING); CATECHOLAMINE; INDAN DERIVATIVE; NEUROPROTECTIVE AGENT;

AGED; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; CHRONIC DRUG ADMINISTRATION; COGNITIVE DEFECT; CONTROLLED STUDY; CORPUS STRIATUM; DEGENERATIVE DISEASE; DOPAMINE BRAIN LEVEL; DOPAMINE METABOLISM; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; GENE EXPRESSION REGULATION; LONG TERM CARE; MALE; MOOD DISORDER; MOUSE; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; SEROTONIN BRAIN LEVEL; SEROTONIN METABOLISM; SPATIAL LEARNING; SPATIAL MEMORY; UPREGULATION; ANIMAL; C57BL MOUSE; COGNITION DISORDERS; DISEASE MODEL; DRUG EFFECTS; EXPLORATORY BEHAVIOR; GENETICS; LONGITUDINAL STUDY; MAZE TEST; METABOLISM; PSYCHOLOGY; SIGNAL TRANSDUCTION; SWIMMING;

AGING; ANIMALS; CATECHOLAMINES; COGNITION DISORDERS; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; GENE EXPRESSION REGULATION; INDANS; LONGITUDINAL STUDIES; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MONOAMINE OXIDASE; NEUROPROTECTIVE AGENTS; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D2; SIGNAL TRANSDUCTION; SWIMMING;

EID: 84940467065     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2015.05.009     Document Type: Article

References (57)

1. Akao Y., Maruyama W., Shimizu S., Yi H., Nakagawa Y., Shamoto-Nagai M., Youdim M.B., Tsujimoto Y., Naoi M. Mitochondrial permeability transition mediates apoptosis induced by N- methyl(R)salsolinol, an endogenous neurotoxin, and is inhibited by Bcl- 2 and rasagiline, N-propargyl-1(R)-aminoindan. J.Neurochem. 2002, 82:913-923.
2. Akao Y., Maruyama W., Yi H., Shamoto-Nagai M., Youdim M.B.H., Naoi M. An anti-Parkinson's disease drug, N-propargyl-1(R)-aminoindan (rasagiline), enhances expression of anti-apoptotic Bcl-2 in human dopaminergic SH-SY5Y cells. Neurosci. Lett. 2002, 326:105-108.
3. Bar-Am O., Weinreb O., Amit T., Youdim M.B. Regulation of Bcl-2 family proteins, neurotrophic factors, and APP processing in the neurorescue activity of propargylamine. FASEB J. 2005, 19:1899-1901.
4. Bar-Am O., Weinreb O., Amit T., Youdim M.B. The novel cholinesterase-monoamine oxidase inhibitor and antioxidant, ladostigil, confers neuroprotection in neuroblastoma cells and aged rats. J.Mol. Neurosci. 2009, 37:135-145.
5. Bar-Am O., Weinreb O., Amit T., Youdim M.B. The neuroprotective mechanism of 1-(R)-aminoindan, the major metabolite of the anti-parkinsonian drug rasagiline. J.Neurochem. 2010, 112:1131-1137.
6. Baudonnat M., Huber A., David V., Walton M.E. Heads for learning, tails for memory: reward, reinforcement and a role of dopamine in determining behavioral relevance across multiple timescales. Front. Neurosci. 2013, 7:175.
7. Berton O., Nestler E.J. New approaches to antidepressant drug discovery: beyond monoamines. Nat. Rev. Neurosci. 2006, 7:137-151.
8. Blandini F. Neuroprotection by rasagiline: a new therapeutic approach to Parkinson's disease?. CNS Drug Rev. 2005, 11:183-194.
9. Borsini F., Meli A. Is the forced swimming test a suitable model for revealing antidepressant activity?. Psychopharmacology (Berl) 1988, 94:147-160.
10. Bromley-Brits K., Deng Y., Song W. Morris water maze test for learning and memory deficits in Alzheimer's disease model mice. J.Vis. Exp. 2011, 53:1-5.
11. Carrillo M.C., Minami C., Kitani K., Maruyama W., Ohashi K., Yamamoto T., Naoi M., Kanai S., Youdim M.B.H. Enhancing effect of rasagiline on superoxide dismutase and catalase activities in the dopaminergic system in the rat. Life Sci. 2000, 67:577-585.
12. Cryan J.F., Mombereau C., Vassout A. The tail suspension test as a model for assessing antidepressant activity: review of pharmacological and genetic studies in mice. Neurosci. Biobehav. Rev. 2005, 29:571-625.
13. de Lima M.N., Polydoro M., Laranja D.C., Bonatto F., Bromberg E., Moreira J.C., Dal-Pizzol F., Schroder N. Recognition memory impairment and brain oxidative stress induced by postnatal iron administration. Eur. J. Neurosci. 2005, 21:2521-2528.
14. de Lima M.N., Presti-Torres J., Garcia V.A., Guimaraes M.R., Scalco F.S., Roesler R., Schroder N. Amelioration of recognition memory impairment associated with iron loading or aging by the type 4-specific phosphodiesterase inhibitor rolipram in rats. Neuropharmacology 2008, 55:788-792.
15. Driscoll I., Sutherland R.J. The aging hippocampus: navigating between rat and human experiments. Rev. Neurosci. 2005, 16:87-121.
16. Finberg J.P., Gillman K. Selective inhibitors of monoamine oxidase type B and the "cheese effect". Int. Rev. Neurobiol. 2011, 100:169-190.
17. Gal S., Zheng H., Fridkin M., Youdim M.B. Novel multifunctional neuroprotective iron chelator-monoamine oxidase inhibitor drugs for neurodegenerative diseases. Invivo selective brain monoamine oxidase inhibition and prevention of MPTP-induced striatal dopamine depletion. J.Neurochem. 2005, 95:79-88.
18. Gardoni F., Zianni E., Eramo A., Canonico P.L., Di Luca M. Effect of rasagiline on the molecular composition of the excitatory postsynaptic density. Eur. J. Pharmacol. 2011, 670:458-463.
19. Green A.R., Youdim M.B.H. Effects of monoamine oxidase inhibition by clorgyline, deprenil or tranylcypromine on 5-hydroxytryptamine concentrations in rat brain and hyperactivity following subsequent tryptophan administration. Br. J. Pharmacol. 1975, 55:415-422.
20. Halbach O.B. Involvement of BDNF in age-dependent alterations in the hippocampus. Front. Aging Neurosci. 2010, 2:1-11.
21. Harman D. Free radical theory of aging. Mutat. Res. 1992, 275:257-266.
22. Jaber M., Robinson S.W., Missale C., Caron M.G. Dopamine receptors and brain function. Neuropharmacology 1996, 35:1503-1519.
23. Khaldy H., Escames G., Leon J., Vives F., Luna J.D., Acuna-Castroviejo D. Comparative effects of melatonin, L-deprenyl, Trolox and ascorbate in the suppression of hydroxyl radical formation during dopamine autoxidation invitro. J.Pineal Res. 2000, 29:100-107.
24. Kitani K., Minami C., Yamamoto T., Maruyama W., Kanai S., Ivy G.O., Carrillo M.C. Do antioxidant strategies work against aging and age-associated disorders? Propargylamines: a possible antioxidant strategy. Ann. N. Y. Acad. Sci. 2001, 928:248-260.
25. Kupershmidt L., Weinreb O., Amit T., Mandel S., Bar-Am O., Youdim M.B. Novel molecular targets of the multi-functional brain-permeable iron chelating drug M30 in mouse brain. Neuroscience 2011, 189:345-358.
26. Lamensdorf I., Youdim M.B., Finberg J.P. Effect of long-term treatment with selective monoamine oxidase A and B inhibitors on dopamine release from rat striatum invivo. J.Neurochem. 1996, 67:1532-1539.
27. Lauber J., Waldmeier P.C. Determination of 2-phenylethylamine in rat brain after MAO inhibitors, and in human CSF and urine by capillary GC and chemical ionization MS. J.Neural Transm. 1984, 60:247-264.
28. Markowska A.L., Spangler E.L., Ingram D.K. Behavioral assessment of the senescence-accelerated mouse (SAM P8 and R1). Physiol. Behav. 1998, 64:15-26.
29. Maruyama W., Akao Y., Youdim M.B., Davis B.A., Naoi M. Transfection-enforced Bcl-2 overexpression and an anti-Parkinson drug, rasagiline, prevent nuclear accumulation of glyceraldehyde-3-phosphate dehydrogenase induced by an endogenous dopaminergic neurotoxin, N-methyl(R)salsolinol. J.Neurochem. 2001, 78:727-735.
30. Maruyama W., Akao Y., Youdim M.B.H., Naoi M. Neurotoxins induce apoptosis in dopamine neurons: protection by N- propargylamine-1(R)- and (S)-aminoindan, rasagiline and TV1022. J.Neural Transm. Suppl. 2000, 60:171-186.
31. Maruyama W., Naoi M. "70th Birthday Professor Riederer" induction of glial cell line-derived and brain-derived neurotrophic factors by rasagiline and (-)deprenyl: a way to a disease-modifying therapy?. J.Neural Transm. 2013, 120:83-89.
32. Maruyama W., Nitta A., Shamoto-Nagai M., Hirata Y., Akao Y., Youdim M.B.H., Furukawa S., Nabeshima T., Naoi M. N-Propargyl-1 (R)-aminoindan, rasagiline, increases glial cell line-derived neurotrophic factor (GDNF) in neuroblastoma SH-SY5Y cells through activation of NF-kappaB transcription factor. Neurochem. Int. 2004, 44:393-400.
33. Maruyama W., Yamamoto T., Kitani K., Carrillo M.C., Youdim M.B.H., Naoi M. Mechanism underlying anti-apoptotic activity of a (-) deprenyl-related propargylamine, rasagiline. Mech. Ageing Dev. 2000, 116:181-191.
34. Maruyama W., Youdim M.B.H., Naoi M. Antiapoptotic properties of rasagiline, N-propargylamine-1(R)-aminoindan, and its optical (S)-isomer, TV1022. Ann. N. Y. Acad. Sci. 2001, 939:320-329.
35. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J.Neurosci. Methods 1984, 11:47-60.
36. Naoi M., Maruyama W. Monoamine oxidase inhibitors as neuroprotective agents in age-dependent neurodegenerative disorders. Curr. Pharm. Des. 2010, 16:2799-2817.
37. Olanow C.W., Hauser R.A., Jankovic J., Langston W., Lang A., Poewe W., Tolosa E., Stocchi F., Melamed E., Eyal E., Rascol O. Arandomized, double-blind, placebo-controlled, delayed start study to assess rasagiline as a disease modifying therapy in Parkinson's disease (the ADAGIO study): rationale, design, and baseline characteristics. Mov. Disord. 2008, 23:2194-2201.
38. Olanow C.W., Rascol O., Hauser R., Feigin P.D., Jankovic J., Lang A., Langston W., Melamed E., Poewe W., Stocchi F., Tolosa E. Adouble-blind, delayed-start trial of rasagiline in Parkinson's disease. N.Engl. J. Med. 2009, 361:1268-1278.
39. Pirondi S., Kuteeva E., Giardino L., Ferraro L., Antonelli T., Bartfai T., Ogren S.O., Hokfelt T., Calza L. Behavioral and neurochemical studies on brain aging in galanin overexpressing mice. Neuropeptides 2005, 39:305-312.
40. Poon H.F., Calabrese V., Calvani M., Butterfield D.A. Proteomics analyses of specific protein oxidation and protein expression in aged rat brain and its modulation by L-acetylcarnitine: insights into the mechanisms of action of this proposed therapeutic agent for CNS disorders associated with oxidative stress. Antioxid. Redox Signal. 2006, 8:381-394.
41. Porsolt R.D., Bertin A., Jalfre M. Behavioral despair in mice: a primary screening test for antidepressants. Arch. Int. Pharmacodyn. Ther. 1977, 229:327-336.
42. Sagi Y., Mandel S., Amit T., Youdim M.B. Activation of tyrosine kinase receptor signaling pathway by rasagiline facilitates neurorescue and restoration of nigrostriatal dopamine neurons in post-MPTP-induced parkinsonism. Neurobiol. Dis. 2007, 25:35-44.
43. Schulze E.T., Geary E.K., Susmaras T.M., Paliga J.T., Maki P.M., Little D.M. Anatomical correlates of age-related working memory declines. J.Aging Res. 2011, 2011:606871.
44. Shohamy D., Adcock R.A. Dopamine and adaptive memory. Trends Cogn. Sci. 2010, 14:464-472.
45. Tapia-Arancibia L., Aliaga E., Silhol M., Arancibia S. New insights into brain BDNF function in normal aging and Alzheimer disease. Brain Res. Rev. 2008, 59:201-220.
46. Twist E.C., Mitchell S.N., Corn T.H., Campbell I.C. Effect of chronic ritanserin or clorgyline on amine and metabolite levels in rat frontal cortex. Eur. J. Pharmacol. 1991, 196:157-160.
47. Venkateshappa C., Harish G., Mahadevan A., Srinivas Bharath M.M., Shankar S.K. Elevated oxidative stress and decreased antioxidant function in the human hippocampus and frontal cortex with increasing age: implications for neurodegeneration in Alzheimer's disease. Neurochem. Res. 2012, 37:1601-1614.
48. Waldmeier P.C. Amine oxidases and their endogenous substrates (with special reference to monoamine oxidase and the brain). J.Neural Transm. Suppl. 1987, 23:55-72.
49. Weinreb O., Amit T., Bar-Am O., Youdim M.B. Rasagiline: a novel anti-Parkinsonian monoamine oxidase-B inhibitor with neuroprotective activity. Prog. Neurobiol. 2010, 92:330-344.
50. Weinreb O., Amit T., Riederer P., Youdim M.B., Mandel S.A. Neuroprotective profile of the multitarget drug rasagiline in Parkinson's disease. Int. Rev. Neurobiol. 2011, 100:127-149.
51. Weinreb O., Amit T., Sagi Y., Drigues N., Youdim M.B. Genomic and proteomic study to survey the mechanism of action of the anti-Parkinson's disease drug, rasagiline compared with selegiline, in the rat midbrain. J.Neural Transm. 2009, 116:1457-1472.
52. Weinreb O., Bar-Am O., Amit T., Chillag-Talmor O., Youdim M.B.H. Neuroprotection via pro-survival protein kinase C isoforms associated with Bcl-2 family members. FASEB J. 2004, 18:1471-1473.
53. Weinreb O., Drigues N., Sagi Y., Reznick A.Z., Amit T., Youdim M.B. The application of proteomics and genomics to the study of age-related neurodegeneration and neuroprotection. Antioxid. Redox Signal. 2007, 9:169-179.
54. Wiescholleck V., Emma Andre M.A., Manahan-Vaughan D. Early age-dependent impairments of context-dependent extinction learning, object recognition, and object-place learning occur in rats. Hippocampus 2014, 24:270-279.
55. Yogev-Falach M., Amit T., Bar-AM O., Youdim M.B.H. The importance of propargylamine moiety in the anti-Parkinson drug rasagiline and its derivatives for MAPK-dependent amyloid precursor protein processing. FASEB J. 2003, 17:2325-2327.
56. Yogev-Falach M., Bar-Am O., Amit T., Weinreb O., Youdim M.B. Amultifunctional, neuroprotective drug, ladostigil (TV3326), regulates holo-APP translation and processing. FASEB J. 2006, 20:2177-2179.
57. Youdim M.B.H., Gross A., Finberg J.P.M. Rasagiline [N-Propargyl-1R(+)-aminoindant], A selective and potent inhibitor of mitochondrial monoamine oxidase B. Br. J. Pharmacol. 2001, 132:500-506.