ACE inhibition with captopril retards the development of signs of neurodegeneration in an animal model of Alzheimer's disease

International Journal of Molecular Sciences

Volumn 14, Issue 8, 2013, Pages 16917-16942

  AbdAlla, Said ^a   Langer, Andreas ^a   Fu, Xuebin ^a   Quitterer, Ursula ^a,b  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Alzheimer's disease; Amyloid precursor protein; Angiotensin converting enzyme; AT1 receptor; Captopril; Neurodegeneration; Tg2576 mouse model

Indexed keywords

AMYLOID BETA PROTEIN; BETA SECRETASE; CAPTOPRIL; DIPEPTIDYL CARBOXYPEPTIDASE; ENALAPRIL; GAMMA SECRETASE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DRUG EFFICACY; ELECTROENCEPHALOGRAM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION PROFILING; GENE SEQUENCE; HIPPOCAMPUS; MOUSE; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FUNCTION; TRANSGENIC MOUSE; TREATMENT DURATION; TREATMENT RESPONSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANGIOTENSIN II; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; CAPTOPRIL; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE REGENERATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATION-REDUCTION; PLAQUE, AMYLOID; PROTEIN TRANSPORT; REACTIVE OXYGEN SPECIES; RECEPTOR, ANGIOTENSIN, TYPE 1; TRANSCRIPTOME; UP-REGULATION;

EID: 84882730546     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140816917     Document Type: Article

References (58)

1. Abbott, A. Dementia: A problem of our age. Nature 2011, 475, S2-S4.
2. Holtzman, D.M.; Mandelkow, E.; Selkoe, D.J. Alzheimer disease in 2020. Cold Spring Harb. Perspect. Med. 2012, 2, doi:10.1101/cshperspect.a011585
3. Huang, Y.; Mucke, L. Alzheimer mechanisms and therapeutic strategies. Cell 2012, 148, 1204-1222.
4. Glenner, G.G.; Wong, C.W. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun. 1984, 120, 885-890.
5. Masters, C.L.; Simms, G.; Weinman, N.A.; Multhaup, G.; McDonald, B.L.; Beyreuther, K.; Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc. Natl. Acad. Sci. USA 1985, 82, 4245-4249.
6. Butterfield, D.A.; Swomley, A.M.; Sultana, R. Amyloid beta-peptide (1-42)-induced oxidative stress in Alzheimer disease: Importance in disease pathogenesis and progression. Antioxid. Redox. Signal. 2013, doi:10.1089/ars.2012.5027
7. Shen, C.; Chen, Y.; Liu, H.; Zhang, K.; Zhang, T.; Lin, A.; Jing, N. Hydrogen peroxide promotes Abeta production through JNK-dependent activation of gamma-secretase. J. Biol. Chem. 2008, 283, 17721-17730.
8. Murakami, K.; Murata, N.; Noda, Y.; Tahara, S.; Kaneko, T.; Kinoshita, N.; Hatsuta, H.; Murayama, S.; Barnham, K.J.; Irie, K., et al.; SOD1 (copper/zinc superoxide dismutase) deficiency drives amyloid beta protein oligomerization and memory loss in mouse model of Alzheimer disease. J. Biol. Chem. 2011, 286, 44557-44568.
9. Dumont, M.; Wille, E.; Stack, C.; Calingasan, N.Y.; Beal, M.F.; Lin, M.T. Reduction of oxidative stress, amyloid deposition, and memory deficit by manganese superoxide dismutase overexpression in a transgenic mouse model of Alzheimer's disease. FASEB J. 2009, 23, 2459-2466.
10. Murakami, K.; Murata, N.; Ozawa, Y.; Kinoshita, N.; Irie, K.; Shirasawa, T.; Shimizu, T.; Vitamin C restores behavioral deficits and amyloid-beta oligomerization without affecting plaque formation in a mouse model of Alzheimer's disease. J. Alzheimers. Dis. 2011, 26, 7-18.
11. Lee, H.P.; Zhu, X.; Casadesus, G.; Castellani, R.J.; Nunomura, A.; Smith, M.A.; Lee, H.G.; Perry, G. Antioxidant approaches for the treatment of Alzheimer's disease Expert Rev. Neurother. 2010, 10, 1201-1208.
12. Vina, J.; Lloret, A.; Giraldo, E.; Badia, M.C.; Alonso, M.D. Antioxidant pathways in Alzheimer's disease: Possibilities of intervention. Curr. Pharm. Des. 2011, 17, 3861-3864.
13. Dikalova, A.; Clempus, R.; Lassegue, B.; Cheng, G.; McCoy, J.; Dikalov, S.; San Martin, A.; Lyle, A.; Weber, D.S.; Weiss, D., et al.; Nox1 overexpression potentiates angiotensin II-induced hypertension and vascular smooth muscle hypertrophy in transgenic mice. Circulation 2005, 112, 2668-2676.
14. Matsuno, K.; Yamada, H.; Iwata, K.; Jin, D.; Katsuyama, M.; Matsuki, M.; Takai, S.; Yamanishi, K.; Miyazaki, M.; Matsubara, H., et al.; Nox1 is involved in angiotensin II-mediated hypertension: A study in Nox1-deficient mice. Circulation 2005, 112, 2677-2685.
15. Jackman, K.A.; Miller, A.A.; Drummond, G.R.; Sobey, C.G. Importance of NOX1 for angiotensin II-induced cerebrovascular superoxide production and cortical infarct volume following ischemic stroke. Brain Res. 2009, 1286, 215-220.
16. Zimmerman, M.C.; Lazartigues, E.; Lang, J.A.; Sinnayah, P.; Ahmad, I.M.; Spitz, D.R.; Davisson, R.L. Superoxide mediates the actions of angiotensin II in the central nervous system. Circ. Res. 2002, 91, 1038-1045.
17. Campese, V.M.; Shaohua, Y.; Huiquin, Z. Oxidative stress mediates angiotensin II-dependent stimulation of sympathetic nerve activity. Hypertension 2005, 46, 533-539.
18. Pang, T.; Wang, J.; Benicky, J.; Sanchez-Lemus, E.; Saavedra, J.M.; Telmisartan directly ameliorates the neuronal inflammatory response to IL-1β partly through the JNK/c-Jun and NADPH oxidase pathways. J. Neuroinflamm. 2012, 9, 102.
19. Guimond, M.O.; Gallo-Payet, N. The angiotensin type 2 receptor in brain functions: An update. Int. J. Hypertens. 2012, 2012, 351758.
20. AbdAlla, S.; Lother, H.; el Missiry, A.; Langer, A.; Sergeev, P.; el Faramawy, Y.; Quitterer, U. Angiotensin II AT2 receptor oligomers mediate G-protein dysfunction in an animal model of Alzheimer disease. J. Biol. Chem. 2009, 284, 6554-6565.
21. AbdAlla, S.; Lother, H.; el Missiry, A.; Sergeev, P.; Langer, A.; el Faramawy, Y.; Quitterer, U. Dominant-negative AT2 receptor oligomers induce G-protein arrest and symptoms of neurodegeneration. J. Biol. Chem. 2009, 284, 6566-6574.
22. Wright, J.W.; Harding, J.W. The brain RAS and Alzheimer's disease. Exp. Neurol. 2010, 223, 326-333.
23. Kehoe, P.G.; Katzov, H.; Andreasen, N.; Gatz, M.; Wilcock, G.K.; Cairns, N.J.; Palmgren, J.; de Faire, U.; Brookes, A.J.; Pedersen, N.L.; et al. Common variants of ACE contribute to variable age-at-onset of Alzheimer's disease. Hum. Genet. 2004, 114, 478-483.
24. Nirmal, S.; Tripathi, M.; Shastri, S.S.; Sagar, R.; Vivekanandhan, S.; Association of Angiotensin-converting enzyme insertion(I)/deletion (D) genotype in Alzheimer's disease patients of north Indian population. Int. J. Neurosci. 2011, 121, 557-561.
25. Zhang, Z.; Deng, L.; Yu, H.; Shi, Y.; Bai, F.; Xie, C.; Yuan, Y.; Jia, J.; Zhang, Z.; Association of angiotensin-converting enzyme functional gene I/D polymorphism with amnestic mild cognitive impairment. Neurosci. Lett. 2012, 514, 131-135.
26. Arregui, A.; Perry, E.K.; Rossor, M.; Tomlinson, B.E.; Angiotensin converting enzyme in Alzheimer's disease increased activity in caudate nucleus and cortical areas. J. Neurochem. 1982, 38, 1490-1492.
27. Savaskan, E.; Hock, C.; Olivieri, G.; Bruttel, S.; Rosenberg, C.; Hulette, C.; Müller-Spahn, F.; Cortical alterations of angiotensin converting enzyme, angiotensin II and AT1 receptor in Alzheimer's dementia. Neurobiol. Aging 2001, 22, 541-546.
28. Miners, J.S.; Ashby, E.; Van Helmond, Z.; Chalmers, K.A.; Palmer, L.E.; Love, S.; Kehoe, P.G. Angiotensin-converting enzyme (ACE) levels and activity in Alzheimer's disease, and relationship of perivascular ACE-1 to cerebral amyloid angiopathy. Neuropathol. Appl. Neurobiol. 2008, 34, 181-193.
29. Hemming, M.L.; Selkoe, D.J.; Amyloid beta-protein is degraded by cellular angiotensin-converting enzyme (ACE) and elevated by an ACE inhibitor. J. Biol. Chem. 2005, 280, 37644-37650.
30. Eckman, E.A.; Adams, S.K.; Troendle, F.J.; Stodola, B.A.; Kahn, M.A.; Faug, A.H.; Xiao, H.D.; Bernstein, K.E.; Eckman, C.B.; Regulation of steady-state beta-amyloid levels in the brain by neprilysin and endothelin-converting enzyme but not angiotensin-converting enzyme. J. Biol. Chem. 2006, 281, 30471-30478.
31. Hemming, M.L.; Selkoe, D.J.; Farris, W. Effects of prolonged angiotensin-converting enzyme inhibitor treatment on amyloid beta-protein metabolism in mouse models of Alzheimer disease. Neurobiol. Dis. 2007, 26, 273-281.
32. Ferrington, L.; Palmer, L.E.; Love, S.; Horsburgh, K.J.; Kelly, P.A.; Kehoe, P.G. Angiotensin II-inhibition: Effect on Alzheimer's pathology in the aged triple transgenic mouse. Am. J. Transl. Res. 2012, 4, 151-164.
33. Khachaturian, A.S.; Zandi, P.P.; Lyketsos, C.G.; Hayden, K.M.; Skoog, I.; Norton, M.C.; Tschanz, J.T.; Mayer, L.S.; Welsh-Bohmer, K.A.; Breitner, J.C.; Antihypertensive medication use and incident Alzheimer disease: The Cache County Study. Arch. Neurol. 2006, 63, 686-692.
34. Ohrui, T.; Tomita, N.; Sato-Nakagawa, T.; Matsui, T.; Maruyama, M.; Niwa, K.; Arai, H.; Sasaki, H. Effects of brain-penetrating ACE inhibitors on Alzheimer disease progression. Neurology 2004, 63, 1324-1325.
35. Sink, K.M.; Leng, X.; Williamson, J.; Kritchevsky, S.B.; Yaffe, K.; Kuller, L.; Yasar, S.; Atkinson, H.; Robbins, M.; Psaty, B.; et al. Angiotensin-converting enzyme inhibitors and cognitive decline in older adults with hypertension: Results from the Cardiovascular Health Study. Arch. Intern. Med. 2009, 169, 1195-1202.
36. Dong, Y.F.; Kataoka, K.; Tokutomi, Y.; Nako, H.; Nakamura, T.; Toyama, K.; Sueta, D.; Koibuchi, N.; Yamamoto, E.; Ogawa, H.; Kim-Mitsuyama, S. Perindopril, a centrally active angiotensin-converting enzyme inhibitor, prevents cognitive impairment in mouse models of Alzheimer's disease. FASEB J. 2011, 25, 2911-2920.
37. Hsiao, K.; Chapman, P.; Nilsen, S.; Eckman, C.; Harigaya, Y.; Younkin, S.; Yang, F.; Cole, G. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 1996, 274, 99-102.
38. Abd Alla, J.; Langer, A.; Elzahwy, S.S.; Arman-Kalcek, G.; Streichert, T.; Quitterer, U. Angiotensin-converting enzyme inhibition down-regulates the pro-atherogenic chemokine receptor 9 (CCR9)-chemokine ligand 25 (CCL25) axis. J. Biol. Chem. 2010, 285, 23496-23505.
39. Fu, X.; Koller, S.; Abd Alla, J.; Quitterer, U. Inhibition of G-protein-coupled receptor kinase 2 (GRK2) triggers the growth-promoting mitogen-activated protein kinase (MAPK) pathway. J. Biol. Chem. 2013, 288, 7738-7755.
40. Simon, A.M, de Maturana, R.L.; Ricobaraza, A.; Escribano, L.; Schiapparelli, L.; Cuadrado-Tejedor, M.; Perez-Mediavilla, A.; Avila, J.; Del Rio, J.; Frechilla, D.; Early changes in hippocampal Eph receptors precede the onset of memory decline in mouse models of Alzheimer's disease. J. Alzheimers. Dis. 2009, 17, 773-786.
41. Verret, L.; Mann, E.O.; Hang, G.B.; Barth, A.M.; Cobos, I.; Ho, K.; Devidze, N.; Masliah, E.; Kreitzer, A.C.; Mody, I., et al.; Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 2012, 149, 708-721.
42. Boda, E.; Hoxha, E.; Pini, A.; Montarolo, F.; Tempia, F. Brain expression of Kv3 subunits during development, adulthood and aging and in a murine model of Alzheimer's disease. J. Mol. Neurosci. 2012, 46, 606-615.
43. Miners, S.; Ashby, E.; Baig, S.; Harrison, R.; Tayler, H.; Speedy, E.; Prince, J.A.; Love, S.; Kehoe, P.G. Angiotensin-converting enzyme levels and activity in Alzheimer's disease: Differences in brain and CSF ACE and association with ACE1 genotypes. Am. J. Transl. Res. 2009, 1, 163-177.
44. Hou, D.R.; Wang, Y.; Zhou, L.; Chen, K.; Tian, Y.; Song, Z.; Bao, J.; Yang, Q.D.; Altered angiotensin-converting enzyme and its effects on the brain in a rat model of Alzheimer disease. Chin. Med. J. (Engl.) 2008, 121, 2320-2323.
45. Zhu, D.; Shi, J.; Zhang, Y.; Wang, B.; Liu, W.; Chen, Z.; Tong, Q. Central angiotensin II stimulation promotes beta amyloid production in Sprague Dawley rats. PLoS One 2011, 6, e16037.
46. Castegna, A.; Thongboonkerd, V.; Klein, J.B.; Lynn, B.; Markesbery, W.R.; Butterfield, D.A. Proteomic identification of nitrated proteins in Alzheimer's disease brain. J. Neurochem. 2003, 85, 1394-1401.
47. Tan, J.L.; Li, Q.X.; Ciccotosto, G.D.; Crouch, P.J.; Culvenor, J.G.; White, A.R.; Evin, G. Mild oxidative stress induces redistribution of BACE1 in non-apoptotic conditions and promotes the amyloidogenic processing of Alzheimer's disease amyloid precursor protein. PLoS One 2013, 8, e61246.
48. Li, H.; Wang, B.; Wang, Z.; Guo, Q.; Tabuchi, K.; Hammer, R.E.; Südhof, T.C.; Zheng, H. Soluble amyloid precursor protein (APP) regulates transthyretin and Klotho gene expression without rescuing the essential function of APP. Proc. Natl. Acad. Sci. USA 2010, 107, 17362-17367.
49. Ghosal, K.; Vogt, D.L.; Liang, M.; Shen, Y.; Lamb, B.T.; Pimplikar, S.W. Alzheimer's disease-like pathological features in transgenic mice expressing the APP intracellular domain. Proc. Natl. Acad. Sci. USA 2009, 106, 18367-18372.
50. Müller, T.; Concannon, C.G.; Ward, M.W.; Walsh, C.M.; Tirniceriu, A.L.; Tribl, F.; Kögel, D.; Prehn, J.H.; Egensperger, R.; Modulation of gene expression and cytoskeletal dynamics by the amyloid precursor protein intracellular domain (AICD). Mol. Biol. Cell 2007, 18, 201-210.
51. Da Cunha, V.; Tham, D.M.; Martin-McNulty, B.; Deng, G.; Ho, J.J.; Wilson, D.W.; Rutledge, J.C.; Vergona, R.; Sullivan, M.E.; Wang, Y.X. Enalapril attenuates angiotensin II-induced atherosclerosis and vascular inflammation. Atherosclerosis 2005, 178, 9-17.
52. Reddy, P.H.; McWeeney, S.; Park, B.S.; Manczak, M.; Gutala, R.V.; Partovi, D.; Jung, Y.; Yau, V.; Searles, R.; Mori, M., et al.; Gene expression profiles of transcripts in amyloid precursor protein transgenic mice: Up-regulation of mitochondrial metabolism and apoptotic genes is an early cellular change in Alzheimer's disease. Hum. Mol. Genet. 2004, 13, 1225-1240.
53. Stein, T.D.; Anders, N.J.; DeCarli, C.; Chan, S.L.; Mattson, M.P., Johnson, J.A.; Neutralization of transthyretin reverses the neuroprotective effects of secreted amyloid precursor protein (APP) in APPSW mice resulting in tau phosphorylation and loss of hippocampal neurons: Support for the amyloid hypothesis. J. Neurosci. 2004, 24, 7707-7717.
54. Tan, L.; Wang, X.; Ni, Z.F.; Zhu, X.; Wu, W.; Zhu, L.Q.; Liu, D. A systematic analysis of genomic changes in Tg2576 mice. Mol. Neurobiol. 2013, 47, 883-891.
55. Mei, N.; Fuscoe, J.C.; Lobenhofer, E.K.; Guo, L. Application of microarray-based analysis of gene expression in the field of toxicogenomics. Methods Mol. Biol. 2010, 597, 227-241.
56. Guo, L.; Lobenhofer, E.K.; Wang, C.; Shippy, R.; Harris, S.C.; Zhang, L.; Mei, N.; Chen, T.; Herman, D.; Goodsaid, F.M., et al.; Rat toxicogenomic study reveals analytical consistency across microarray plaforms. Nat. Biotechnol. 2006, 24, 1162-1169.
57. AbdAlla, S.; Lother, H.; Langer, A.; el Faramawy, Y.; Quitterer, U. Factor XIIIA transglutaminase crosslinks AT1 receptor dimers of monocytes at the onset of atherosclerosis. Cell 2004, 119, 343-354.
58. Butterfield, D.A.; Reed, T.T.; Perluigi, M.; de Marco, C.; Coccia, R.; Keller, J.N.; Markesbery, W.R.; Sultana, R.; Elevated levels of 3-nitrotyrosine in brain from subjects with amnestic mild cognitive impairment: Implications for the role of nitration in the progression of Alzheimer's disease. Brain Res. 2007, 1148, 243-248.