Central angiotensin II stimulation promotes β amyloid production in Sprague Dawley rats

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Zhu, Donglin ^a   Shi, Jingping ^a   Zhang, Yingdong ^a   Wang, Bianrong ^b   Liu, Wei ^a   Chen, Zhicong ^a   Tong, Qiang ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SECRETASE; AMYLOID BETA PROTEIN; ANGIOTENSIN II; BETA SECRETASE; GAMMA SECRETASE; STRESS HORMONE; AMYLOID PRECURSOR PROTEIN; ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN RECEPTOR ANTAGONIST; SECRETASE;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; MALE; NONHUMAN; PATHOGENESIS; PROTEIN ANALYSIS; PROTEIN FUNCTION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; ANIMAL; BIOSYNTHESIS; BRAIN VENTRICLE; METABOLISM; PHYSIOLOGICAL STRESS; SPRAGUE DAWLEY RAT;

ANIMALIA; RATTUS;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANGIOTENSIN II; ANGIOTENSIN RECEPTOR ANTAGONISTS; ANIMALS; CEREBRAL VENTRICLES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, ANGIOTENSIN, TYPE 1; STRESS, PHYSIOLOGICAL;

EID: 79551541587     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016037     Document Type: Article

References (89)

1. Wray S, Noble W (2009) Linking amyloid and tau pathology in Alzheimer's disease: the role of membrane cholesterol in Abeta-mediated tau toxicity. J Neurosci 29: 9665-9667.
2. Frykman S, Hur JY, Franberg J, Aoki M, Winblad B, et al. (2010) Synaptic and endosomal localization of active gamma-secretase in rat brain. PLoS One 5: e8948.
3. Salloway S, Correia S (2009) Alzheimer disease: time to improve its diagnosis and treatment. Cleve Clin J Med 76: 49-58.
4. Yang M, Teplow DB (2008) Amyloid beta-protein monomer folding: free-energy surfaces reveal alloform-specific differences. J Mol Biol 384: 450-464.
5. Postina R (2008) A closer look at alpha-secretase. Curr Alzheimer Res 5: 179-186.
6. Kuhn PH, Wang H, Dislich B, Colombo A, Zeitschel U, et al. (2010) ADAM10 is the physiologically relevant, constitutive alpha-secretase of the amyloid precursor protein in primary neurons. EMBO J 29: 3020-3032.
7. Hussain I, Powell D, Howlett DR, Tew DG, Meek TD, et al. (1999) Identification of a novel aspartic protease (Asp 2) as beta-secretase. Mol Cell Neurosci 14: 419-427.
8. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, et al. (1999) Betasecretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286: 735-741.
9. Yan R, Bienkowski MJ, Shuck ME, Miao H, Tory MC, et al. (1999) Membraneanchored aspartyl protease with Alzheimer's disease beta-secretase activity. Nature 402: 533-537.
10. Sinha S, Anderson JP, Barbour R, Basi GS, Caccavello R, et al. (1999) Purification and cloning of amyloid precursor protein beta-secretase from human brain. Nature 402: 537-540.
11. Lin X, Koelsch G, Wu S, Downs D, Dashti A, et al. (2000) Human aspartic protease memapsin 2 cleaves the beta-secretase site of beta-amyloid precursor protein. Proc Natl Acad Sci U S A 97: 1456-1460.
12. Luo Y, Bolon B, Kahn S, Bennett BD, Babu-Khan S, et al. (2001) Mice deficient in BACE1, the Alzheimer's beta-secretase, have normal phenotype and abolished beta-amyloid generation. Nat Neurosci 4: 231-232.
13. Wolfe MS (2006) The gamma-secretase complex: membrane-embedded proteolytic ensemble. Biochemistry 45: 7931-7939.
14. Carter DB, Dunn E, Pauley AM, McKinley DD, Fleck TJ, et al. (2008) Changes in gamma-secretase activity and specificity caused by the introduction of consensus aspartyl protease active motif in Presenilin 1. Mol Neurodegener 3: 6.
15. Mucke L (2009) Neuroscience: Alzheimer's disease. Nature 461: 895-897.
16. Rothman SM, Mattson MP (2010) Adverse stress, hippocampal networks, and Alzheimer's disease. Neuromolecular Med 12: 56-70.
17. Saavedra JM, Benicky J (2007) Brain and peripheral angiotensin II play a major role in stress. Stress 10: 185-193.
18. Ni Y, Zhao X, Bao G, Zou L, Teng L, et al. (2006) Activation of beta2- adrenergic receptor stimulates gamma-secretase activity and accelerates amyloid plaque formation. Nat Med 12: 1390-1396.
19. Yu NN, Wang XX, Yu JT, Wang ND, Lu RC, et al. (2010) Blocking beta2- adrenergic receptor attenuates acute stress-induced amyloid beta peptides production. Brain Res 1317: 305-310.
20. Green KN, Billings LM, Roozendaal B, McGaugh JL, LaFerla FM (2006) Glucocorticoids increase amyloid-beta and tau pathology in a mouse model of Alzheimer's disease. J Neurosci 26: 9047-9056.
21. Li WZ, Li WP, Yao YY, Zhang W, Yin YY, et al. (2010) Glucocorticoids increase impairments in learning and memory due to elevated amyloid precursor protein expression and neuronal apoptosis in 12-month old mice. Eur J Pharmacol 628: 108-115.
22. Saavedra JM (2005) Brain angiotensin II: new developments, unanswered questions and therapeutic opportunities. Cell Mol Neurobiol 25: 485-512.
23. Yang G, Wan Y, Zhu Y (1996) Angiotensin II-an important stress hormone. Biol Signals 5: 1-8.
24. Savaskan E, Höchli M, Ganten D, Chan-Palay V (1991) Angiotensin II Immunoreactivity in the Human Striatum and Hippocampus of Elderly Controls and Patients with Senile Dementia of the Alzheimer Type and Multi-Infarct Dementia. Dementia and Geriatric Cognitive Disorders 2: 314-323.
25. Savaskan E, Hock C, Olivieri G, Bruttel S, Rosenberg C, et al. (2001) CorticalC alterations of angiotensin converting enzyme, angiotensin II and AT1 receptorin Alzheimer's dementia. Neurobiol Aging 22: 541-546.
26. Barnes JM, Barnes NM, Costall B, Horovitz ZP, Naylor RJ (1989) Angiotensin II inhibits the release of [3H]acetylcholine from rat entorhinal cortex in vitro. Brain Res 491: 136-143.
27. Barnes JM, Barnes NM, Costall B, Horovitz ZP, Ironside JW, et al. (1990) Angiotensin II inhibits acetylcholine release from human temporal cortex: implications for cognition. Brain Res 507: 341-343.
28. Zimmerman MC, Lazartigues E, Lang JA, Sinnayah P, Ahmad IM, et al. (2002) Superoxide mediates the actions of angiotensin II in the central nervous system. Circ Res 91: 1038-1045.
29. Sumners C, Fleegal MA, Zhu M (2002) Angiotensin AT1 receptor signaling pathways in neurons. Clin Exp Pharmacol Physiol 29: 483-490.
30. Das UN (2005) Angiotensin-II behaves as an endogenous pro-inflammatory molecule. J Assoc Physicians India 53: 472-476.
31. Wosik K, Cayrol R, Dodelet-Devillers A, Berthelet F, Bernard M, et al. (2007) Angiotensin II controls occludin function and is required for blood brain barrier maintenance: relevance to multiple sclerosis. J Neurosci 27: 9032-9042.
32. Hamdi HK, Castellon R (2004) A genetic variant of ACE increases cell survival: a new paradigm for biology and disease. Biochem Biophys Res Commun 318: 187-191.
33. Zhu X, Lee HG, Raina AK, Perry G, Smith MA (2002) The role ofC itogenactivated protein kinase pathways in Alzheimer's disease. Neurosignals 11: 270-281.
34. Mattson MP (2004) Pathways towards and away from Alzheimer's disease. Nature 430: 631-639.
35. Tan ZS, Seshadri S (2010) Inflammation in the Alzheimer's disease cascade: culprit or innocent bystander? Alzheimers Res Ther 2: 6.
36. Wang J, Ho L, Chen L, Zhao Z, Zhao W, et al. (2007) Valsartan lowers brain beta-amyloid protein levels and improves spatial learning in a mouse model of Alzheimer disease. J Clin Invest 117: 3393-3402.
37. Mogi M, Li JM, Tsukuda K, Iwanami J, Min LJ, et al. (2008) Telmisartan prevented cognitive decline partly due to PPAR-gamma activation. Biochem Biophys Res Commun 375: 446-449.
38. Takeda S, Sato N, Takeuchi D, Kurinami H, Shinohara M, et al. (2009) Angiotensin receptor blocker prevented beta-amyloid-induced cognitive impairment associated with recovery of neurovascular coupling. Hypertension 54: 1345-1352.
39. Tota S, Kamat PK, Awasthi H, Singh N, Raghubir R, et al. (2009) Candesartan improves memory decline in mice: involvement of AT1 receptors in memory deficit induced by intracerebral streptozotocin. Behav Brain Res 199: 235-240.
40. Danielyan L, Klein R, Hanson LR, Buadze M, Schwab M, et al. (2010) Protective effects of intranasal losartan in the APP/PS1 transgenic mouse model of Alzheimer disease. Rejuvenation Res 13: 195-201.
41. Huttunen HJ, Greco C, Kovacs DM (2007) Knockdown of ACAT-1 reduces amyloidogenic processing of APP. FEBS Lett 581: 1688-1692.
42. Tesco G, Koh YH, Kang EL, Cameron AN, Das S, et al. (2007) Depletion of GGA3 stabilizes BACE and enhances beta-secretase activity. Neuron 54: 721-737.
43. Nishida Y, Ito S, Ohtsuki S, Yamamoto N, Takahashi T, et al. (2009) Depletion of vitamin E increases amyloid beta accumulation by decreasing its clearances from brain and blood in a mouse model of Alzheimer disease. J Biol Chem 284: 33400-33408.
44. Thathiah A, Spittaels K, Hoffmann M, Staes M, Cohen A, et al. (2009) The orphan G protein-coupled receptor 3 modulates amyloid-beta peptide generation in neurons. Science 323: 946-951.
45. Saavedra JM, Benicky J, Zhou J (2006) Angiotensin II: multitasking in the brain. J Hypertens Suppl 24: S131-137.
46. Castren E, Saavedra JM (1988) Repeated stress increases the density of angiotensin II binding sites in rat paraventricular nucleus and subfornical organ. Endocrinology 122: 370-372.
47. Peng JF, Phillips MI (2001) Opposite regulation of brain angiotensin type 1 and type 2 receptors in cold-induced hypertension. Regul Pept 97: 91-102.
48. Yang G, Xi ZX, Wan Y, Wang H, Bi G (1993) Changes in circulating and tissue angiotensin II during acute and chronic stress. Biol Signals 2: 166-172.
49. Armando I, Carranza A, Nishimura Y, Hoe KL, Barontini M, et al. (2001) Peripheral administration of an angiotensin II AT(1) receptor antagonist decreases the hypothalamic-pituitary-adrenal response to isolation Stress. Endocrinology 142: 3880-3889.
50. Leong DS, Terron JA, Falcon-Neri A, Armando I, Ito T, et al. (2002) Restraint stress modulates brain, pituitary and adrenal expression of angiotensin II AT(1A), AT(1B) and AT(2) receptors. Neuroendocrinology 75: 227-240.
51. Aguilera G, Kiss A, Luo X (1995) Increased expression of type 1 angiotensin II receptors in the hypothalamic paraventricular nucleus following stress and glucocorticoid administration. J Neuroendocrinol 7: 775-783.
52. Moellenhoff E, Blume A, Culman J, Chatterjee B, Herdegen T, et al. (2001) Effect of repetitive icv injections of ANG II on c-Fos and AT(1)-receptor expression in the rat brain. Am J Physiol Regul Integr Comp Physiol 280: R1095-1104.
53. Wei SG, Yu Y, Zhang ZH, Weiss RM, Felder RB (2008) Mitogen-activated protein kinases mediate upregulation of hypothalamic angiotensin II type 1 receptors in heart failure rats. Hypertension 52: 679-686.
54. Wei SG, Yu Y, Zhang ZH, Felder RB (2009) Angiotensin II upregulates hypothalamic AT1 receptor expression in rats via the mitogen-activated protein kinase pathway. Am J Physiol Heart Circ Physiol 296: H1425-1433.
55. Mitra AK, Gao L, Zucker IH (2010) Angiotensin II-induced upregulation of AT(1) receptor expression: sequential activation of NF-kappaB and Elk-1 in neurons. Am J Physiol Cell Physiol 299: C561-569.
56. Parvathy S, Hussain I, Karran EH, Turner AJ, Hooper NM (1999) Cleavage of Alzheimer's amyloid precursor protein by alpha-secretase occurs at the surface of neuronal cells. Biochemistry 38: 9728-9734.
57. Farzan M, Schnitzler CE, Vasilieva N, Leung D, Choe H (2000) BACE2, a beta -secretase homolog, cleaves at the beta site and within the amyloid-beta region of the amyloid-beta precursor protein. Proc Natl Acad Sci U S A 97: 9712-9717.
58. Yan R, Munzner JB, Shuck ME, Bienkowski MJ (2001) BACE2 functions as an alternative alpha-secretase in cells. J Biol Chem 276: 34019-34027.
59. Cole SL, Vassar R (2007) The Alzheimer's disease beta-secretase enzyme, BACE1. Mol Neurodegener 2: 22.
60. Bourne KZ, Ferrari DC, Lange-Dohna C, Rossner S, Wood TG, et al. (2007) Differential regulation of BACE1 promoter activity by nuclear factor-kappaB in neurons and glia upon exposure to beta-amyloid peptides. J Neurosci Res 85: 1194-1204.
61. 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.
62. Chan SH, Wang LL, Tseng HL, Chan JY (2007) Upregulation of AT1 receptor gene on activation of protein kinase Cbeta/nicotinamide adenine dinucleotide diphosphate oxidase/ERK1/2/c-fos signaling cascade mediates long-term pressor effect of angiotensin II in rostral ventrolateral medulla. J Hypertens 25: 1845-1861.
63. Tamagno E, Bardini P, Obbili A, Vitali A, Borghi R, et al. (2002) Oxidative stress increases expression and activity of BACE in NT2 neurons. Neurobiol Dis 10: 279-288.
64. Tong Y, Zhou W, Fung V, Christensen MA, Qing H, et al. (2005) Oxidative stress potentiates BACE1 gene expression and Abeta generation. J Neural Transm 112: 455-469.
65. Cupers P, Bentahir M, Craessaerts K, Orlans I, Vanderstichele H, et al. (2001) The discrepancy between presenilin subcellular localization and gammasecretase processing of amyloid precursor protein. J Cell Biol 154: 731-740.
66. Li YM, Xu M, Lai MT, Huang Q, Castro JL, et al. (2000) Photoactivated gamma-secretase inhibitors directed to the active site covalently label presenilin 1. Nature 405: 689-694.
67. Tamagno E, Guglielmotto M, Aragno M, Borghi R, Autelli R, et al. (2008) Oxidative stress activates a positive feedback between the gamma- and betasecretase cleavages of the beta-amyloid precursor protein. J Neurochem 104: 683-695.
68. Lee S, Das HK (2010) Transcriptional regulation of the presenilin-1 gene controls gamma-secretase activity. Front Biosci (Elite Ed) 2: 22-35.
69. Kimberly WT, LaVoie MJ, Ostaszewski BL, Ye W, Wolfe MS, et al. (2003) Gamma-secretase is a membrane protein complex comprised of presenilin, nicastrin, Aph-1, and Pen-2. Proc Natl Acad Sci U S A 100: 6382-6387.
70. Mitsuda N, Ohkubo N, Tamatani M, Lee YD, Taniguchi M, et al. (2001) Activated cAMP-response element-binding protein regulates neuronal expression of presenilin-1. J Biol Chem 276: 9688-9698.
71. Lee S, Das HK (2008) Inhibition of basal activity of c-jun-NH2-terminal kinase (JNK) represses the expression of presenilin-1 by a p53-dependent mechanism. Brain Res 1207: 19-31.
72. Quiroz-Baez R, Rojas E, Arias C (2009) Oxidative stress promotes JNKdependentC amyloidogenic processing of normally expressed human APP bydifferential modification of alpha-, beta- and gamma-secretase expression. Neurochem Int 55: 662-670.
73. Kuo LH, Hu MK, Hsu WM, Tung YT, Wang BJ, et al. (2008) Tumor necrosis factor-alpha-elicited stimulation of gamma-secretase is mediated by c-Jun Nterminal kinase-dependent phosphorylation of presenilin and nicastrin. Mol Biol Cell 19: 4201-4212.
74. Sumners C, Phillips MI (1983) Central injection of angiotensin II alters catecholamine activity in rat brain. Am J Physiol 244: R257-263.
75. Lichtenthaler SF, Wang R, Grimm H, Uljon SN, Masters CL, et al. (1999) Mechanism of the cleavage specificity of Alzheimer's disease gamma-secretaseidentified by phenylalanine-scanning mutagenesis of the transmembrane domain of the amyloid precursor protein. Proc Natl Acad Sci U S A 96: 3053-3058.
76. Shelton CC, Zhu L, Chau D, Yang L, Wang R, et al. (2009) Modulation of gamma-secretase specificity using small molecule allosteric inhibitors. Proc Natl Acad Sci U S A 106: 20228-20233.
77. Kuperstein I, Broersen K, Benilova I, Rozenski J, Jonckheere W, et al. (2010) Neurotoxicity of Alzheimer's disease Abeta peptides is induced by small changes in the Abeta42 to Abeta40 ratio. EMBO J 29: 3408-3420.
78. Skoog I, Lernfelt B, Landahl S, Palmertz B, Andreasson LA, et al. (1996) 15-year longitudinal study of blood pressure and dementia. Lancet 347: 1141-1145.
79. Skoog I, Gustafson D (2006) Update on hypertension and Alzheimer's disease. Neurol Res 28: 605-611.
80. Raghavendra V, Chopra K, Kulkarni SK (2001) Comparative studies on theC memory-enhancing actions of captopril and losartan in mice using inhibitoryshock avoidance paradigm. Neuropeptides 35: 65-69.
81. Fogari R, Mugellini A, Zoppi A, Derosa G, Pasotti C, et al. (2003) Influence ofC losartan and atenolol on memory function in very elderly hypertensive patients.J Hum Hypertens 17: 781-785.
82. Tedesco MA, Ratti G, Mennella S, Manzo G, Grieco M, et al. (1999) Comparison of losartan and hydrochlorothiazide on cognitive function and quality of life in hypertensive patients. Am J Hypertens 12: 1130-1134.
83. Poon IO (2008) Effects of antihypertensive drug treatment on the risk of dementia and cognitive impairment. Pharmacotherapy 28: 366-375.
84. de la Torre JC (2004) Is Alzheimer's disease a neurodegenerative or a vascular disorder? Data, dogma, and dialectics. Lancet Neurol 3: 184-190.
85. de la Torre JC (2010) Basics of Alzheimer's disease prevention. J Alzheimers Dis 20: 687-688.
86. Pan YX, Gao L, Wang WZ, Zheng H, Liu D, et al. (2007) Exercise training prevents arterial baroreflex dysfunction in rats treated with central angiotensin II. Hypertension 49: 519-527.
87. Lu J, Zhang Y, Shi J (2008) Effects of intracerebroventricular infusion of angiotensin-(1-7) on bradykinin formation and the kinin receptor expression after focal cerebral ischemia-reperfusion in rats. Brain Res 1219: 127-135.
88. Liu L, Orozco IJ, Planel E, Wen Y, Bretteville A, et al. (2008) A transgenic rat that develops Alzheimer's disease-like amyloid pathology, deficits in synaptic plasticity and cognitive impairment. Neurobiol Dis 31: 46-57.
89. Zou L, Wang Z, Shen L, Bao GB, Wang T, et al. (2007) Receptor tyrosine kinases positively regulate BACE activity and Amyloid-beta production through enhancing BACE internalization. Cell Res 17: 389-401.