Donepezil improves learning and memory deficits in APP/PS1 mice by inhibition of microglial activation

Neuroscience

Volumn 290, Issue , 2015, Pages 530-542

  Guo, H B ^a   Cheng, Y F ^a   Wu, J G ^a   Wang, C M ^a   Wang, H T ^a   Zhang, C ^a   Qiu, Z K ^a   Xu, J P ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

Alzheimer's disease; Amyloid ; Donepezil; Insulin degrading enzyme; Microglia; Neuroinflammation

Indexed keywords

AMYLOID; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; CD68 ANTIGEN; CONGO RED; DONEPEZIL; INTERLEUKIN 1BETA; PRESENILIN 1; TUMOR NECROSIS FACTOR ALPHA; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (1-42); APP PROTEIN, HUMAN; CD68 PROTEIN, MOUSE; CYTOKINE; DIFFERENTIATION ANTIGEN; INDAN DERIVATIVE; LEUKOCYTE ANTIGEN; NOOTROPIC AGENT; PEPTIDE FRAGMENT; PIPERIDINE DERIVATIVE; PSEN1 PROTEIN, HUMAN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIINFLAMMATORY ACTIVITY; ARTICLE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LEARNING DISORDER; LONG TERM CARE; MALE; MEMORY DISORDER; MICROGLIA; MORRIS WATER MAZE TEST; MOUSE; MOUSE STRAIN; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; PATHOGENESIS; PROTEIN EXPRESSION; TRANSGENIC MOUSE; ANIMAL; BRAIN; C57BL MOUSE; DRUG EFFECTS; GENETICS; LEARNING DISORDERS; MAZE TEST; MEMORY DISORDERS; METABOLISM; NEURITE; PATHOPHYSIOLOGY; PHYSIOLOGY; PLAQUE, AMYLOID; RANDOMIZATION; RECOGNITION;

AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; BRAIN; CYTOKINES; INDANS; LEARNING DISORDERS; MALE; MAZE LEARNING; MEMORY DISORDERS; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; NEURITES; NOOTROPIC AGENTS; PEPTIDE FRAGMENTS; PIPERIDINES; PLAQUE, AMYLOID; PRESENILIN-1; RANDOM ALLOCATION; RECOGNITION (PSYCHOLOGY);

EID: 84922971674     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.01.058     Document Type: Article

References (50)

1. Affholter J.A., Hsieh C.L., Francke U., Roth R.A. Insulin-degrading enzyme: stable expression of the human complementary DNA, characterization of its protein product, and chromosomal mapping of the human and mouse genes. Mol Endocrinol 1990, 4:1125-1135.
2. Ballard C.G., Chalmers K.A., Todd C., McKeith I.G., O'Brien J.T., Wilcock G., Love S., Perry E.K. Cholinesterase inhibitors reduce cortical Abeta in dementia with Lewy bodies. Neurology 2007, 68:1726-1729.
3. Bloom G.S. Amyloid-beta and tau: the trigger and bullet in Alzheimer disease pathogenesis. JAMA Neurol 2014, 71:505-508.
4. Borovikova L.V., Ivanova S., Zhang M., Yang H., Botchkina G.I., Watkins L.R., Wang H., Abumrad N., Eaton J.W., Tracey K.J. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000, 405:458-462.
5. Breitner J.C., Haneuse S.J., Walker R., Dublin S., Crane P.K., Gray S.L., Larson E.B. Risk of dementia and AD with prior exposure to NSAIDs in an elderly community-based cohort. Neurology 2009, 72:1899-1905.
6. Cook D.G., Leverenz J.B., McMillan P.J., Kulstad J.J., Ericksen S., Roth R.A., Schellenberg G.D., Jin L.W., Kovacina K.S., Craft S. Reduced hippocampal insulin-degrading enzyme in late-onset Alzheimer's disease is associated with the apolipoprotein E-epsilon4 allele. Am J Pathol 2003, 162:313-319.
7. Cote S., Carmichael P.H., Verreault R., Lindsay J., Lefebvre J., Laurin D. Nonsteroidal anti-inflammatory drug use and the risk of cognitive impairment and Alzheimer's disease. Alzheimers Dement 2012, 8:219-226.
8. Cutuli D., De Bartolo P., Caporali P., Tartaglione A.M., Oddi D., D'Amato F.R., Nobili A., D'Amelio M., Petrosini L. Neuroprotective effects of donepezil against cholinergic depletion. Alzheimers Res Ther 2013, 5:50.
9. Easton A., Sankaranarayanan S., Tanghe A., Terwel D., Lin A.X., Hoque N., Bourin C., Gu H., Ahlijanian M., Bristow L. Effects of sub-chronic donepezil on brain Abeta and cognition in a mouse model of Alzheimer's disease. Psychopharmacology 2013, 230:279-289.
10. Farris W., Mansourian S., Leissring M.A., Eckman E.A., Bertram L., Eckman C.B., Tanzi R.E., Selkoe D.J. Partial loss-of-function mutations in insulin-degrading enzyme that induce diabetes also impair degradation of amyloid beta-protein. Am J Pathol 2004, 164:1425-1434.
11. Frackowiak J., Wisniewski H.M., Wegiel J., Merz G.S., Iqbal K., Wang K.C. Ultrastructure of the microglia that phagocytose amyloid and the microglia that produce beta-amyloid fibrils. Acta Neuropathol 1992, 84:225-233.
12. Garcia-Alloza M., Robbins E.M., Zhang-Nunes S.X., Purcell S.M., Betensky R.A., Raju S., Prada C., Greenberg S.M., Bacskai B.J., Frosch M.P. Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol Dis 2006, 24:516-524.
13. Giunta B., Ehrhart J., Townsend K., Sun N., Vendrame M., Shytle D., Tan J., Fernandez F. Galantamine and nicotine have a synergistic effect on inhibition of microglial activation induced by HIV-1 gp120. Brain Res Bull 2004, 64:165-170.
14. Hayden K.M., Zandi P.P., Khachaturian A.S., Szekely C.A., Fotuhi M., Norton M.C., Tschanz J.T., Pieper C.F., Corcoran C., Lyketsos C.G., Breitner J.C., Welsh-Bohmer K.A. Does NSAID use modify cognitive trajectories in the elderly? The Cache County study. Neurology 2007, 69:275-282.
15. He P., Zhong Z., Lindholm K., Berning L., Lee W., Lemere C., Staufenbiel M., Li R., Shen Y. Deletion of tumor necrosis factor death receptor inhibits amyloid beta generation and prevents learning and memory deficits in Alzheimer's mice. J Cell Biol 2007, 178:829-841.
16. Hein A.M., Stasko M.R., Matousek S.B., Scott-McKean J.J., Maier S.F., Olschowka J.A., Costa A.C., O'Banion M.K. Sustained hippocampal IL-1beta overexpression impairs contextual and spatial memory in transgenic mice. Brain Behav Immun 2010, 24:243-253.
17. Heneka M.T., O'Banion M.K., Terwel D., Kummer M.P. Neuroinflammatory processes in Alzheimer's disease. J Neural Transm 2010, 117:919-947.
18. Hoozemans J.J., Veerhuis R., Rozemuller J.M., Eikelenboom P. Neuroinflammation and regeneration in the early stages of Alzheimer's disease pathology. Int J Dev Neurosci 2006, 24:157-165.
19. Hwang J., Hwang H., Lee H.W., Suk K. Microglia signaling as a target of donepezil. Neuropharmacology 2010, 58:1122-1129.
20. Ito S., Ohtsuki S., Murata S., Katsukura Y., Suzuki H., Funaki M., Tachikawa M., Terasaki T. Involvement of insulin-degrading enzyme in insulin- and atrial natriuretic peptide-sensitive internalization of amyloid-beta peptide in mouse brain capillary endothelial cells. J Alzheimers Dis 2014, 38:185-200.
21. Janelsins M.C., Mastrangelo M.A., Oddo S., LaFerla F.M., Federoff H.J., Bowers W.J. Early correlation of microglial activation with enhanced tumor necrosis factor-alpha and monocyte chemoattractant protein-1 expression specifically within the entorhinal cortex of triple transgenic Alzheimer's disease mice. J Neuroinflammation 2005, 2:23.
22. Janelsins M.C., Mastrangelo M.A., Park K.M., Sudol K.L., Narrow W.C., Oddo S., LaFerla F.M., Callahan L.M., Federoff H.J., Bowers W.J. Chronic neuron-specific tumor necrosis factor-alpha expression enhances the local inflammatory environment ultimately leading to neuronal death in 3xTg-AD mice. Am J Pathol 2008, 173:1768-1782.
23. Jankowsky J.L., Slunt H.H., Ratovitski T., Jenkins N.A., Copeland N.G., Borchelt D.R. Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol Eng 2001, 17:157-165.
24. Kim H.G., Moon M., Choi J.G., Park G., Kim A.J., Hur J., Lee K.T., Oh M.S. Donepezil inhibits the amyloid-beta oligomer-induced microglial activation in vitro and in vivo. Neurotoxicology 2014, 40:23-32.
25. Lahmy V., Meunier J., Malmstrom S., Naert G., Givalois L., Kim S.H., Villard V., Vamvakides A., Maurice T. Blockade of Tau hyperphosphorylation and Abeta(1)(-)(4)(2) generation by the aminotetrahydrofuran derivative ANAVEX2-73, a mixed muscarinic and sigma(1) receptor agonist, in a nontransgenic mouse model of Alzheimer's disease. Neuropsychopharmacology 2013, 38:1706-1723.
26. Leal M.C., Dorfman V.B., Gamba A.F., Frangione B., Wisniewski T., Castano E.M., Sigurdsson E.M., Morelli L. Plaque-associated overexpression of insulin-degrading enzyme in the cerebral cortex of aged transgenic tg2576 mice with Alzheimer pathology. J Neuropathol Exp Neurol 2006, 65:976-987.
27. Leissring M.A., Farris W., Chang A.Y., Walsh D.M., Wu X., Sun X., Frosch M.P., Selkoe D.J. Enhanced proteolysis of beta-amyloid in APP transgenic mice prevents plaque formation, secondary pathology, and premature death. Neuron 2003, 40:1087-1093.
28. Li Q., Chen M., Liu H., Yang L., Yang G. Expression of APP, BACE1, AChE and ChAT in an AD model in rats and the effect of donepezil hydrochloride treatment. Mol Med Rep 2012, 6:1450-1454.
29. Lim G.P., Yang F., Chu T., Chen P., Beech W., Teter B., Tran T., Ubeda O., Ashe K.H., Frautschy S.A., Cole G.M. Ibuprofen suppresses plaque pathology and inflammation in a mouse model for Alzheimer's disease. J Neurosci 2000, 20:5709-5714.
30. Mastrangelo M.A., Sudol K.L., Narrow W.C., Bowers W.J. Interferon-{gamma} differentially affects Alzheimer's disease pathologies and induces neurogenesis in triple transgenic-AD mice. Am J Pathol 2009, 175:2076-2088.
31. Michelucci A., Heurtaux T., Grandbarbe L., Morga E., Heuschling P. Characterization of the microglial phenotype under specific pro-inflammatory and anti-inflammatory conditions: effects of oligomeric and fibrillar amyloid-beta. J Neuroimmunol 2009, 210:3-12.
32. Miners J.S., Baig S., Tayler H., Kehoe P.G., Love S. Neprilysin and insulin-degrading enzyme levels are increased in Alzheimer disease in relation to disease severity. J Neuropathol Exp Neurol 2009, 68:902-914.
33. Montgomery S.L., Mastrangelo M.A., Habib D., Narrow W.C., Knowlden S.A., Wright T.W., Bowers W.J. Ablation of TNF-RI/RII expression in Alzheimer's disease mice leads to an unexpected enhancement of pathology: implications for chronic pan-TNF-alpha suppressive therapeutic strategies in the brain. Am J Pathol 2011, 179:2053-2070.
34. Moore A.H., Wu M., Shaftel S.S., Graham K.A., O'Banion M.K. Sustained expression of interleukin-1beta in mouse hippocampus impairs spatial memory. Neuroscience 2009, 164:1484-1495.
35. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 1984, 11:47-60.
36. Myskiw J.C., Rossato J.I., Bevilaqua L.R., Medina J.H., Izquierdo I., Cammarota M. On the participation of mTOR in recognition memory. Neurobiol Learn Mem 2008, 89:338-351.
37. Nagakura A., Shitaka Y., Yarimizu J., Matsuoka N. Characterization of cognitive deficits in a transgenic mouse model of Alzheimer's disease and effects of donepezil and memantine. Eur J Pharmacol 2013, 703:53-61.
38. Nizri E., Irony-Tur-Sinai M., Faranesh N., Lavon I., Lavi E., Weinstock M., Brenner T. Suppression of neuroinflammation and immunomodulation by the acetylcholinesterase inhibitor rivastigmine. J Neuroimmunol 2008, 203:12-22.
39. Pavlov V.A., Ochani M., Gallowitsch-Puerta M., Ochani K., Huston J.M., Czura C.J., Al-Abed Y., Tracey K.J. Central muscarinic cholinergic regulation of the systemic inflammatory response during endotoxemia. Proc Natl Acad Sci U S A 2006, 103:5219-5223.
40. Qiu W.Q., Walsh D.M., Ye Z., Vekrellis K., Zhang J., Podlisny M.B., Rosner M.R., Safavi A., Hersh L.B., Selkoe D.J. Insulin-degrading enzyme regulates extracellular levels of amyloid beta-protein by degradation. J Biol Chem 1998, 273:32730-32738.
41. Saijo K., Winner B., Carson C.T., Collier J.G., Boyer L., Rosenfeld M.G., Gage F.H., Glass C.K. A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell 2009, 137:47-59.
42. Sha S., Xing X.N., Cao Y.P. Active immunotherapy facilitates Abeta plaque removal following through microglial activation without obvious T cells infiltrating the CNS. J Neuroimmunol 2014, 274:62-70.
43. Shaftel S.S., Kyrkanides S., Olschowka J.A., Miller J.N., Johnson R.E., O'Banion M.K. Sustained hippocampal IL-1 beta overexpression mediates chronic neuroinflammation and ameliorates Alzheimer plaque pathology. J Clin Invest 2007, 117:1595-1604.
44. Shytle R.D., Mori T., Townsend K., Vendrame M., Sun N., Zeng J., Ehrhart J., Silver A.A., Sanberg P.R., Tan J. Cholinergic modulation of microglial activation by alpha 7 nicotinic receptors. J Neurochem 2004, 89:337-343.
45. Vepsalainen S., Hiltunen M., Helisalmi S., Wang J., van Groen T., Tanila H., Soininen H. Increased expression of Abeta degrading enzyme IDE in the cortex of transgenic mice with Alzheimer's disease-like neuropathology. Neurosci Lett 2008, 438:216-220.
46. Wyss-Coray T., Lin C., Yan F., Yu G.Q., Rohde M., McConlogue L., Masliah E., Mucke L. TGF-beta1 promotes microglial amyloid-beta clearance and reduces plaque burden in transgenic mice. Nat Med 2001, 7:612-618.
47. Xiong J., Wang C., Chen H., Hu Y., Tian L., Pan J., Geng M. Abeta-induced microglial cell activation is inhibited by baicalin through the JAK2/STAT3 signaling pathway. Int J Neurosci 2014, 124:609-620.
48. Yoshiyama Y., Kojima A., Ishikawa C., Arai K. Anti-inflammatory action of donepezil ameliorates tau pathology, synaptic loss, and neurodegeneration in a tauopathy mouse model. J Alzheimers Dis 2010, 22:295-306.
49. Zhang R., Xue G., Wang S., Zhang L., Shi C., Xie X. Novel object recognition as a facile behavior test for evaluating drug effects in AbetaPP/PS1 Alzheimer's disease mouse model. J Alzheimers Dis 2012, 31:801-812.
50. Zhang W., Bai M., Xi Y., Hao J., Liu L., Mao N., Su C., Miao J., Li Z. Early memory deficits precede plaque deposition in APPswe/PS1dE9 mice: involvement of oxidative stress and cholinergic dysfunction. Free Radic Biol Med 2012, 52:1443-1452.