A non-transgenic mouse model (icv-STZ mouse) of Alzheimer's disease: similarities to and differences from the transgenic model (3xTg-AD mouse).

Molecular neurobiology

Volumn 47, Issue 2, 2013, Pages 711-725

  Chen, Yanxing ^a   Liang, Zhihou ^b   Blanchard, Julie ^b   Dai, Chun Ling ^b   Sun, Shenggang ^b   Lee, Moon H ^b   Grundke Iqbal, Inge ^b   Iqbal, Khalid ^b   Liu, Fei ^b   Gong, Cheng Xin ^b  

^a NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

STREPTOZOCIN;

129 MOUSE; ALZHEIMER DISEASE; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; COGNITIVE DEFECT; COMPARATIVE STUDY; DISEASE MODEL; DRUG EFFECTS; GENETICS; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; MAZE TEST; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; TOXICITY; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; ANIMALS; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; INJECTIONS, INTRAVENTRICULAR; MAZE LEARNING; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, TRANSGENIC; STREPTOZOCIN;

EID: 84889263487     PISSN: None     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-012-8375-5     Document Type: Article

References (60)

1. 1. I Grundke-Iqbal K Iqbal YC Tung M Quinlan HM Wisniewski LI Binder 1986 Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology Proc Natl Acad Sci U S A 83 13 4913 4917 3088567 10.1073/pnas.83.13.4913 1:CAS:528:DyaL28XksFyqtrg%3D Grundke-Iqbal I, Iqbal K, Tung YC, Quinlan M, Wisniewski HM, Binder LI (1986) Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci U S A 83(13):4913–4917
2. 2. K Iqbal I Grundke-Iqbal 2010 Alzheimer’s disease, a multifactorial disorder seeking multitherapies Alzheimers Dement 6 5 420 424 10.1016/j.jalz.2010.04.006 20813343 10.1016/j.jalz.2010.04.006 1:CAS:528:DC%2BC3cXhtFWqtrnN Iqbal K, Grundke-Iqbal I (2010) Alzheimer’s disease, a multifactorial disorder seeking multitherapies. Alzheimers Dement 6(5):420–424. doi: 10.1016/j.jalz.2010.04.006
3. 3. SC Waring RN Rosenberg 2008 Genome-wide association studies in Alzheimer disease Arch Neurol 65 3 329 334 10.1001/archneur.65.3.329 18332245 10.1001/archneur.65.3.329 Waring SC, Rosenberg RN (2008) Genome-wide association studies in Alzheimer disease. Arch Neurol 65(3):329–334. doi: 10.1001/archneur.65.3.329
4. 4. S Oddo A Caccamo JD Shepherd MP Murphy TE Golde R Kayed R Metherate MP Mattson Y Akbari FM LaFerla 2003 Triple-transgenic model of Alzheimer’s disease with plaques and tangles: intracellular Abeta and synaptic dysfunction Neuron 39 3 409 421 12895417 10.1016/S0896-6273(03)00434-3 1:CAS:528:DC%2BD3sXmsFOksro%3D Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, LaFerla FM (2003) Triple-transgenic model of Alzheimer’s disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39(3):409–421
5. 5. S Oddo A Caccamo M Kitazawa BP Tseng FM LaFerla 2003 Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer’s disease Neurobiol Aging 24 8 1063 1070 14643377 10.1016/j.neurobiolaging.2003.08.012 1:CAS:528:DC%2BD3sXpt1Cjsrg%3D Oddo S, Caccamo A, Kitazawa M, Tseng BP, LaFerla FM (2003) Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer’s disease. Neurobiol Aging 24(8):1063–1070
6. 6. MC Janelsins MA Mastrangelo S Oddo FM LaFerla HJ Federoff WJ Bowers 2005 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 2 23 10.1186/1742-2094-2-23 16232318 10.1186/1742-2094-2-23 Janelsins MC, Mastrangelo MA, Oddo S, LaFerla FM, Federoff HJ, Bowers WJ (2005) 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 2:23. doi: 10.1186/1742-2094-2-23
7. 7. LM Billings S Oddo KN Green JL McGaugh FM LaFerla 2005 Intraneuronal Abeta causes the onset of early Alzheimer’s disease-related cognitive deficits in transgenic mice Neuron 45 5 675 688 10.1016/j.neuron.2005.01.040 15748844 10.1016/j.neuron.2005.01.040 1:CAS:528:DC%2BD2MXis1yrs7s%3D Billings LM, Oddo S, Green KN, McGaugh JL, LaFerla FM (2005) Intraneuronal Abeta causes the onset of early Alzheimer’s disease-related cognitive deficits in transgenic mice. Neuron 45(5):675–688. doi: 10.1016/j.neuron.2005.01.040
8. 8. LK Clinton LM Billings KN Green A Caccamo J Ngo S Oddo JL McGaugh FM LaFerla 2007 Age-dependent sexual dimorphism in cognition and stress response in the 3xTg-AD mice Neurobiol Dis 28 1 76 82 10.1016/j.nbd.2007.06.013 17659878 10.1016/j.nbd.2007.06.013 1:CAS:528:DC%2BD2sXhtVOgur3M Clinton LK, Billings LM, Green KN, Caccamo A, Ngo J, Oddo S, McGaugh JL, LaFerla FM (2007) Age-dependent sexual dimorphism in cognition and stress response in the 3xTg-AD mice. Neurobiol Dis 28(1):76–82. doi: 10.1016/j.nbd.2007.06.013
9. 9. MA Mastrangelo WJ Bowers 2008 Detailed immunohistochemical characterization of temporal and spatial progression of Alzheimer’s disease-related pathologies in male triple-transgenic mice BMC Neurosci 9 81 10.1186/1471-2202-9-81 18700006 10.1186/1471-2202-9-81 Mastrangelo MA, Bowers WJ (2008) Detailed immunohistochemical characterization of temporal and spatial progression of Alzheimer’s disease-related pathologies in male triple-transgenic mice. BMC Neurosci 9:81. doi: 10.1186/1471-2202-9-81
10. 10. E Grunblatt M Salkovic-Petrisic J Osmanovic P Riederer S Hoyer 2007 Brain insulin system dysfunction in streptozotocin intracerebroventricularly treated rats generates hyperphosphorylated tau protein J Neurochem 101 3 757 770 10.1111/j.1471-4159.2006.04368.x 17448147 10.1111/j.1471-4159.2006.04368.x Grunblatt E, Salkovic-Petrisic M, Osmanovic J, Riederer P, Hoyer S (2007) Brain insulin system dysfunction in streptozotocin intracerebroventricularly treated rats generates hyperphosphorylated tau protein. J Neurochem 101(3):757–770. doi: 10.1111/j.1471-4159.2006.04368.x
11. 11. M Salkovic-Petrisic F Tribl M Schmidt S Hoyer P Riederer 2006 Alzheimer-like changes in protein kinase B and glycogen synthase kinase-3 in rat frontal cortex and hippocampus after damage to the insulin signalling pathway J Neurochem 96 4 1005 1015 10.1111/j.1471-4159.2005.03637.x 16412093 10.1111/j.1471-4159.2005.03637.x 1:CAS:528:DC%2BD28XivFWjsr8%3D Salkovic-Petrisic M, Tribl F, Schmidt M, Hoyer S, Riederer P (2006) Alzheimer-like changes in protein kinase B and glycogen synthase kinase-3 in rat frontal cortex and hippocampus after damage to the insulin signalling pathway. J Neurochem 96(4):1005–1015. doi: 10.1111/j.1471-4159.2005.03637.x
12. 12. T Szkudelski 2001 The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas Physiol Res 50 6 537 546 11829314 1:CAS:528:DC%2BD38Xhslartb0%3D Szkudelski T (2001) The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiol Res 50(6):537–546
13. 13. A Drzezga N Lautenschlager H Siebner M Riemenschneider F Willoch S Minoshima M Schwaiger A Kurz 2003 Cerebral metabolic changes accompanying conversion of mild cognitive impairment into Alzheimer’s disease: a PET follow-up study Eur J Nucl Med Mol Imaging 30 8 1104 1113 10.1007/s00259-003-1194-1 12764551 10.1007/s00259-003-1194-1 Drzezga A, Lautenschlager N, Siebner H, Riemenschneider M, Willoch F, Minoshima S, Schwaiger M, Kurz A (2003) Cerebral metabolic changes accompanying conversion of mild cognitive impairment into Alzheimer’s disease: a PET follow-up study. Eur J Nucl Med Mol Imaging 30(8):1104–1113. doi: 10.1007/s00259-003-1194-1
14. 14. WD Heiss B Szelies J Kessler K Herholz 1991 Abnormalities of energy metabolism in Alzheimer’s disease studied with PET Ann N Y Acad Sci 640 65 71 1776760 1:STN:280:DyaK387jtl2itw%3D%3D Heiss WD, Szelies B, Kessler J, Herholz K (1991) Abnormalities of energy metabolism in Alzheimer’s disease studied with PET. Ann N Y Acad Sci 640:65–71
15. 15. AI Duarte PI Moreira CR Oliveira 2012 Insulin in central nervous system: more than just a peripheral hormone J Aging Res 2012 384017 10.1155/2012/384017 22500228 Duarte AI, Moreira PI, Oliveira CR (2012) Insulin in central nervous system: more than just a peripheral hormone. J Aging Res 2012:384017. doi: 10.1155/2012/384017
16. 16. Y Liu F Liu I Grundke-Iqbal K Iqbal CX Gong 2011 Deficient brain insulin signalling pathway in Alzheimer’s disease and diabetes J Pathol 225 1 54 62 10.1002/path.2912 21598254 10.1002/path.2912 1:CAS:528:DC%2BC3MXpt1Cns78%3D Liu Y, Liu F, Grundke-Iqbal I, Iqbal K, Gong CX (2011) Deficient brain insulin signalling pathway in Alzheimer’s disease and diabetes. J Pathol 225(1):54–62. doi: 10.1002/path.2912
17. 17. E Steen BM Terry EJ Rivera JL Cannon TR Neely R Tavares XJ Xu JR Wands SM Monte de la 2005 Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer’s disease—is this type 3 diabetes? J Alzheimers Dis 7 1 63 80 15750215 1:CAS:528:DC%2BD2MXhvVSrtL8%3D Steen E, Terry BM, Rivera EJ, Cannon JL, Neely TR, Tavares R, Xu XJ, Wands JR, de la Monte SM (2005) Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer’s disease—is this type 3 diabetes? J Alzheimers Dis 7(1):63–80
18. 18. K Talbot HY Wang H Kazi LY Han KP Bakshi A Stucky RL Fuino KR Kawaguchi AJ Samoyedny RS Wilson Z Arvanitakis JA Schneider BA Wolf DA Bennett JQ Trojanowski SE Arnold 2012 Demonstrated brain insulin resistance in Alzheimer’s disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline J Clin Invest 122 4 1316 1338 10.1172/jci59903 22476197 10.1172/JCI59903 1:CAS:528:DC%2BC38Xlt1egtbY%3D Talbot K, Wang HY, Kazi H, Han LY, Bakshi KP, Stucky A, Fuino RL, Kawaguchi KR, Samoyedny AJ, Wilson RS, Arvanitakis Z, Schneider JA, Wolf BA, Bennett DA, Trojanowski JQ, Arnold SE (2012) Demonstrated brain insulin resistance in Alzheimer’s disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J Clin Invest 122(4):1316–1338. doi: 10.1172/jci59903
19. 19. M Salkovic-Petrisic S Hoyer 2007 Central insulin resistance as a trigger for sporadic Alzheimer-like pathology: an experimental approach J Neural Transm Suppl 72 217 233 17982898 10.1007/978-3-211-73574-9_28 1:CAS:528:DC%2BD2sXhsVKns7bN Salkovic-Petrisic M, Hoyer S (2007) Central insulin resistance as a trigger for sporadic Alzheimer-like pathology: an experimental approach. J Neural Transm Suppl 72:217–233
20. 20. M Salkovic-Petrisic J Osmanovic E Grunblatt P Riederer S Hoyer 2009 Modeling sporadic Alzheimer’s disease: the insulin resistant brain state generates multiple long-term morphobiological abnormalities including hyperphosphorylated tau protein and amyloid-beta J Alzheimers Dis 18 4 729 750 10.3233/jad-2009-1184 19661616 1:CAS:528:DC%2BD1MXhsFynsrnK Salkovic-Petrisic M, Osmanovic J, Grunblatt E, Riederer P, Hoyer S (2009) Modeling sporadic Alzheimer’s disease: the insulin resistant brain state generates multiple long-term morphobiological abnormalities including hyperphosphorylated tau protein and amyloid-beta. J Alzheimers Dis 18(4):729–750. doi: 10.3233/jad-2009-1184
21. 21. Y Tatebayashi K Iqbal I Grundke-Iqbal 1999 Dynamic regulation of expression and phosphorylation of tau by fibroblast growth factor-2 in neural progenitor cells from adult rat hippocampus J Neurosci 19 13 5245 5254 10377336 1:CAS:528:DyaK1MXktlOqtbs%3D Tatebayashi Y, Iqbal K, Grundke-Iqbal I (1999) Dynamic regulation of expression and phosphorylation of tau by fibroblast growth factor-2 in neural progenitor cells from adult rat hippocampus. J Neurosci 19(13):5245–5254
22. 22. JJ Pei CX Gong K Iqbal I Grundke-Iqbal QL Wu B Winblad RF Cowburn 1998 Subcellular distribution of protein phosphatases and abnormally phosphorylated tau in the temporal cortex from Alzheimer’s disease and control brains J Neural Transm 105 1 69 83 9588762 10.1007/s007020050039 1:CAS:528:DyaK1cXivVylsrs%3D Pei JJ, Gong CX, Iqbal K, Grundke-Iqbal I, Wu QL, Winblad B, Cowburn RF (1998) Subcellular distribution of protein phosphatases and abnormally phosphorylated tau in the temporal cortex from Alzheimer’s disease and control brains. J Neural Transm 105(1):69–83
23. 23. F Sargolini P Roullet A Oliverio A Mele 2003 Effects of intra-accumbens focal administrations of glutamate antagonists on object recognition memory in mice Behav Brain Res 138 2 153 163 12527446 10.1016/S0166-4328(02)00238-3 1:CAS:528:DC%2BD3sXjtF2hug%3D%3D Sargolini F, Roullet P, Oliverio A, Mele A (2003) Effects of intra-accumbens focal administrations of glutamate antagonists on object recognition memory in mice. Behav Brain Res 138(2):153–163
24. 24. RG Morris P Garrud JN Rawlins J O’Keefe 1982 Place navigation impaired in rats with hippocampal lesions Nature 297 5868 681 683 7088155 10.1038/297681a0 1:STN:280:DyaL383itVSguw%3D%3D Morris RG, Garrud P, Rawlins JN, O’Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297(5868):681–683
25. 25. A Bensadoun D Weinstein 1976 Assay of proteins in the presence of interfering materials Anal Biochem 70 1 241 250 1259145 10.1016/S0003-2697(76)80064-4 1:CAS:528:DyaE28Xos1emsA%3D%3D Bensadoun A, Weinstein D (1976) Assay of proteins in the presence of interfering materials. Anal Biochem 70(1):241–250
26. 26. J Blanchard L Wanka YC Tung C Cardenas-Aguayo Mdel FM LaFerla K Iqbal I Grundke-Iqbal 2010 Pharmacologic reversal of neurogenic and neuroplastic abnormalities and cognitive impairments without affecting Abeta and tau pathologies in 3xTg-AD mice Acta Neuropathol 120 5 605 621 20697724 10.1007/s00401-010-0734-6 1:CAS:528:DC%2BC3cXhtlSjtrfE Blanchard J, Wanka L, Tung YC, Cardenas-Aguayo Mdel C, LaFerla FM, Iqbal K, Grundke-Iqbal I (2010) Pharmacologic reversal of neurogenic and neuroplastic abnormalities and cognitive impairments without affecting Abeta and tau pathologies in 3xTg-AD mice. Acta Neuropathol 120(5):605–621
27. 27. S Pellow P Chopin SE File M Briley 1985 Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat J Neurosci Methods 14 3 149 167 2864480 10.1016/0165-0270(85)90031-7 1:STN:280:DyaL28%2Fht12htw%3D%3D Pellow S, Chopin P, File SE, Briley M (1985) Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14(3):149–167
28. 28. T Wyss-Coray J Rogers 2012 Inflammation in Alzheimer disease—a brief review of the basic science and clinical literature Cold Spring Harb Perspect Med 2 1 a006346 10.1101/cshperspect.a006346 22315714 Wyss-Coray T, Rogers J (2012) Inflammation in Alzheimer disease—a brief review of the basic science and clinical literature. Cold Spring Harb Perspect Med 2(1):a006346. doi: 10.1101/cshperspect.a006346
29. 29. SC Correia RX Santos G Perry X Zhu PI Moreira MA Smith 2011 Insulin-resistant brain state: the culprit in sporadic Alzheimer’s disease? Ageing Res Rev 10 2 264 273 10.1016/j.arr.2011.01.001 21262392 10.1016/j.arr.2011.01.001 1:CAS:528:DC%2BC3MXjtFWjtbw%3D Correia SC, Santos RX, Perry G, Zhu X, Moreira PI, Smith MA (2011) Insulin-resistant brain state: the culprit in sporadic Alzheimer’s disease? Ageing Res Rev 10(2):264–273. doi: 10.1016/j.arr.2011.01.001
30. 30. J Prickaerts T Fahrig A Blokland 1999 Cognitive performance and biochemical markers in septum, hippocampus and striatum of rats after an i.c.v. injection of streptozotocin: a correlation analysis Behav Brain Res 102 1–2 73 88 10403017 10.1016/S0166-4328(98)00158-2 1:CAS:528:DyaK1MXjslOqsbg%3D Prickaerts J, Fahrig T, Blokland A (1999) Cognitive performance and biochemical markers in septum, hippocampus and striatum of rats after an i.c.v. injection of streptozotocin: a correlation analysis. Behav Brain Res 102(1–2):73–88
31. 31. L Gimenez-Llort G Blazquez T Canete B Johansson S Oddo A Tobena FM LaFerla A Fernandez-Teruel 2007 Modeling behavioral and neuronal symptoms of Alzheimer’s disease in mice: a role for intraneuronal amyloid Neurosci Biobehav Rev 31 1 125 147 10.1016/j.neubiorev.2006.07.007 17055579 10.1016/j.neubiorev.2006.07.007 1:CAS:528:DC%2BD28Xht12ksL%2FP Gimenez-Llort L, Blazquez G, Canete T, Johansson B, Oddo S, Tobena A, LaFerla FM, Fernandez-Teruel A (2007) Modeling behavioral and neuronal symptoms of Alzheimer’s disease in mice: a role for intraneuronal amyloid. Neurosci Biobehav Rev 31(1):125–147. doi: 10.1016/j.neubiorev.2006.07.007
32. 32. J Dou C Cui F Dufour DL Alkon WQ Zhao 2003 Gene expression of alpha-endosulfine in the rat brain: correlative changes with aging, learning and stress J Neurochem 87 5 1086 1100 14622089 10.1046/j.1471-4159.2003.02094.x 1:CAS:528:DC%2BD3sXps1Ohs74%3D Dou J, Cui C, Dufour F, Alkon DL, Zhao WQ (2003) Gene expression of alpha-endosulfine in the rat brain: correlative changes with aging, learning and stress. J Neurochem 87(5):1086–1100
33. 33. G Mayer R Nitsch S Hoyer 1990 Effects of changes in peripheral and cerebral glucose metabolism on locomotor activity, learning and memory in adult male rats Brain Res 532 1–2 95 100 2149302 10.1016/0006-8993(90)91747-5 1:CAS:528:DyaK3MXitFGmuw%3D%3D Mayer G, Nitsch R, Hoyer S (1990) Effects of changes in peripheral and cerebral glucose metabolism on locomotor activity, learning and memory in adult male rats. Brain Res 532(1–2):95–100
34. 34. J Cerejeira L Lagarto EB Mukaetova-Ladinska 2012 Behavioral and psychological symptoms of dementia Front Neurol 3 73 10.3389/fneur.2012.00073 22586419 10.3389/fneur.2012.00073 1:STN:280:DC%2BC38njt1aitg%3D%3D Cerejeira J, Lagarto L, Mukaetova-Ladinska EB (2012) Behavioral and psychological symptoms of dementia. Front Neurol 3:73. doi: 10.3389/fneur.2012.00073
35. 35. R Sterniczuk MC Antle FM Laferla RH Dyck 2010 Characterization of the 3xTg-AD mouse model of Alzheimer’s disease: part 2. Behavioral and cognitive changes Brain Res 1348 149 155 10.1016/j.brainres.2010.06.011 20558146 10.1016/j.brainres.2010.06.011 1:CAS:528:DC%2BC3cXptlWmu7s%3D Sterniczuk R, Antle MC, Laferla FM, Dyck RH (2010) Characterization of the 3xTg-AD mouse model of Alzheimer’s disease: part 2. Behavioral and cognitive changes. Brain Res 1348:149–155. doi: 10.1016/j.brainres.2010.06.011
36. 36. S Pinton JT Rocha da BM Gai CW Nogueira 2011 Sporadic dementia of Alzheimer’s type induced by streptozotocin promotes anxiogenic behavior in mice Behav Brain Res 223 1 1 6 10.1016/j.bbr.2011.04.014 21515307 10.1016/j.bbr.2011.04.014 Pinton S, da Rocha JT, Gai BM, Nogueira CW (2011) Sporadic dementia of Alzheimer’s type induced by streptozotocin promotes anxiogenic behavior in mice. Behav Brain Res 223(1):1–6. doi: 10.1016/j.bbr.2011.04.014
37. 37. EG McGeer PL McGeer 2003 Inflammatory processes in Alzheimer’s disease Prog Neuropsychopharmacol Biol Psychiatry 27 5 741 749 10.1016/s0278-5846(03)00124-6 12921904 10.1016/S0278-5846(03)00124-6 1:CAS:528:DC%2BD3sXmt1Kjt74%3D McGeer EG, McGeer PL (2003) Inflammatory processes in Alzheimer’s disease. Prog Neuropsychopharmacol Biol Psychiatry 27(5):741–749. doi: 10.1016/s0278-5846(03)00124-6
38. 38. JE Simpson PG Ince G Lace G Forster PJ Shaw F Matthews G Savva C Brayne SB Wharton 2010 Astrocyte phenotype in relation to Alzheimer-type pathology in the ageing brain Neurobiol Aging 31 4 578 590 10.1016/j.neurobiolaging.2008.05.015 18586353 10.1016/j.neurobiolaging.2008.05.015 1:CAS:528:DC%2BC3cXhvFGgsbY%3D Simpson JE, Ince PG, Lace G, Forster G, Shaw PJ, Matthews F, Savva G, Brayne C, Wharton SB (2010) Astrocyte phenotype in relation to Alzheimer-type pathology in the ageing brain. Neurobiol Aging 31(4):578–590. doi: 10.1016/j.neurobiolaging.2008.05.015
39. 39. J Prickaerts J Vente De W Honig H Steinbusch MMV Ittersum A Blokland HW Steinbusch 2000 Nitric oxide synthase does not mediate neurotoxicity after an i.c.v. injection of streptozotocin in the rat J Neural Transm 107 7 745 766 11005541 10.1007/s007020070056 1:CAS:528:DC%2BD3cXntV2hur0%3D Prickaerts J, De Vente J, Honig W, Steinbusch H, Ittersum MMV, Blokland A, Steinbusch HW (2000) Nitric oxide synthase does not mediate neurotoxicity after an i.c.v. injection of streptozotocin in the rat. J Neural Transm 107(7):745–766
40. 40. M Weinstock S Shoham 2004 Rat models of dementia based on reductions in regional glucose metabolism, cerebral blood flow and cytochrome oxidase activity J Neural Transm 111 3 347 366 10.1007/s00702-003-0058-y 14991459 10.1007/s00702-003-0058-y 1:CAS:528:DC%2BD2cXhsFequ7c%3D Weinstock M, Shoham S (2004) Rat models of dementia based on reductions in regional glucose metabolism, cerebral blood flow and cytochrome oxidase activity. J Neural Transm 111(3):347–366. doi: 10.1007/s00702-003-0058-y
41. 41. L Rodrigues R Biasibetti A Swarowsky MC Leite A Quincozes-Santos JA Quilfeldt M Achaval CA Goncalves 2009 Hippocampal alterations in rats submitted to streptozotocin-induced dementia model are prevented by aminoguanidine J Alzheimers Dis 17 1 193 202 10.3233/jad-2009-1034 19494442 1:CAS:528:DC%2BD1MXmsFKgu78%3D Rodrigues L, Biasibetti R, Swarowsky A, Leite MC, Quincozes-Santos A, Quilfeldt JA, Achaval M, Goncalves CA (2009) Hippocampal alterations in rats submitted to streptozotocin-induced dementia model are prevented by aminoguanidine. J Alzheimers Dis 17(1):193–202. doi: 10.3233/jad-2009-1034
42. 42. S Shoham C Bejar E Kovalev D Schorer-Apelbaum M Weinstock 2007 Ladostigil prevents gliosis, oxidative–nitrative stress and memory deficits induced by intracerebroventricular injection of streptozotocin in rats Neuropharmacology 52 3 836 843 10.1016/j.neuropharm.2006.10.005 17123555 10.1016/j.neuropharm.2006.10.005 1:CAS:528:DC%2BD2sXhvVyqt7k%3D Shoham S, Bejar C, Kovalev E, Schorer-Apelbaum D, Weinstock M (2007) Ladostigil prevents gliosis, oxidative–nitrative stress and memory deficits induced by intracerebroventricular injection of streptozotocin in rats. Neuropharmacology 52(3):836–843. doi: 10.1016/j.neuropharm.2006.10.005
43. 43. N Lester-Coll EJ Rivera SJ Soscia K Doiron JR Wands SM Monte de la 2006 Intracerebral streptozotocin model of type 3 diabetes: relevance to sporadic Alzheimer’s disease J Alzheimers Dis 9 1 13 33 16627931 1:CAS:528:DC%2BD28Xjs1Kltb0%3D Lester-Coll N, Rivera EJ, Soscia SJ, Doiron K, Wands JR, de la Monte SM (2006) Intracerebral streptozotocin model of type 3 diabetes: relevance to sporadic Alzheimer’s disease. J Alzheimers Dis 9(1):13–33
44. 44. M Kitazawa S Oddo TR Yamasaki KN Green FM LaFerla 2005 Lipopolysaccharide-induced inflammation exacerbates tau pathology by a cyclin-dependent kinase 5-mediated pathway in a transgenic model of Alzheimer’s disease J Neurosci 25 39 8843 8853 10.1523/jneurosci.2868-05.2005 16192374 10.1523/JNEUROSCI.2868-05.2005 1:CAS:528:DC%2BD2MXhtVOqs7rP Kitazawa M, Oddo S, Yamasaki TR, Green KN, LaFerla FM (2005) Lipopolysaccharide-induced inflammation exacerbates tau pathology by a cyclin-dependent kinase 5-mediated pathway in a transgenic model of Alzheimer’s disease. J Neurosci 25(39):8843–8853. doi: 10.1523/jneurosci.2868-05.2005
45. 45. N Takasu I Komiya T Asawa Y Nagasawa T Yamada 1991 Streptozocin-and alloxan-induced H 2 O 2 generation and DNA fragmentation in pancreatic islets. H 2 O 2 as mediator for DNA fragmentation Diabetes 40 9 1141 1145 1834504 10.2337/diabetes.40.9.1141 1:CAS:528:DyaK3MXmtVCqt70%3D Takasu N, Komiya I, Asawa T, Nagasawa Y, Yamada T (1991) Streptozocin-and alloxan-induced H 2 O 2 generation and DNA fragmentation in pancreatic islets. H 2 O 2 as mediator for DNA fragmentation. Diabetes 40(9):1141–1145
46. 46. H Javed MM Khan A Ahmad K Vaibhav ME Ahmad A Khan M Ashafaq F Islam MS Siddiqui MM Safhi 2012 Rutin prevents cognitive impairments by ameliorating oxidative stress and neuroinflammation in rat model of sporadic dementia of Alzheimer type Neuroscience 210 340 352 10.1016/j.neuroscience.2012.02.046 22441036 10.1016/j.neuroscience.2012.02.046 1:CAS:528:DC%2BC38Xntlahtb4%3D Javed H, Khan MM, Ahmad A, Vaibhav K, Ahmad ME, Khan A, Ashafaq M, Islam F, Siddiqui MS, Safhi MM (2012) Rutin prevents cognitive impairments by ameliorating oxidative stress and neuroinflammation in rat model of sporadic dementia of Alzheimer type. Neuroscience 210:340–352. doi: 10.1016/j.neuroscience.2012.02.046
47. 47. AT Isik T Celik G Ulusoy O Ongoru B Elibol H Doruk E Bozoglu H Kayir MR Mas S Akman 2009 Curcumin ameliorates impaired insulin/IGF signalling and memory deficit in a streptozotocin-treated rat model Age (Dordr) 31 1 39 49 10.1007/s11357-008-9078-8 10.1007/s11357-008-9078-8 1:CAS:528:DC%2BD1MXit1elsrg%3D Isik AT, Celik T, Ulusoy G, Ongoru O, Elibol B, Doruk H, Bozoglu E, Kayir H, Mas MR, Akman S (2009) Curcumin ameliorates impaired insulin/IGF signalling and memory deficit in a streptozotocin-treated rat model. Age (Dordr) 31(1):39–49. doi: 10.1007/s11357-008-9078-8
48. 48. G Saxena IK Patro C Nath 2011 ICV STZ induced impairment in memory and neuronal mitochondrial function: a protective role of nicotinic receptor Behav Brain Res 224 1 50 57 10.1016/j.bbr.2011.04.039 21620901 10.1016/j.bbr.2011.04.039 1:CAS:528:DC%2BC3MXptVOltro%3D Saxena G, Patro IK, Nath C (2011) ICV STZ induced impairment in memory and neuronal mitochondrial function: a protective role of nicotinic receptor. Behav Brain Res 224(1):50–57. doi: 10.1016/j.bbr.2011.04.039
49. 49. H Javed MM Khan A Khan K Vaibhav A Ahmad G Khuwaja ME Ahmed SS Raza M Ashafaq R Tabassum MS Siddiqui OM El-Agnaf MM Safhi F Islam 2011 S-allyl cysteine attenuates oxidative stress associated cognitive impairment and neurodegeneration in mouse model of streptozotocin-induced experimental dementia of Alzheimer’s type Brain Res 1389 133 142 10.1016/j.brainres.2011.02.072 21376020 10.1016/j.brainres.2011.02.072 1:CAS:528:DC%2BC3MXltFaisbw%3D Javed H, Khan MM, Khan A, Vaibhav K, Ahmad A, Khuwaja G, Ahmed ME, Raza SS, Ashafaq M, Tabassum R, Siddiqui MS, El-Agnaf OM, Safhi MM, Islam F (2011) S-allyl cysteine attenuates oxidative stress associated cognitive impairment and neurodegeneration in mouse model of streptozotocin-induced experimental dementia of Alzheimer’s type. Brain Res 1389:133–142. doi: 10.1016/j.brainres.2011.02.072
50. 50. T Ishrat K Parveen MM Khan G Khuwaja MB Khan S Yousuf A Ahmad P Shrivastav F Islam 2009 Selenium prevents cognitive decline and oxidative damage in rat model of streptozotocin-induced experimental dementia of Alzheimer’s type Brain Res 1281 117 127 10.1016/j.brainres.2009.04.010 19374888 10.1016/j.brainres.2009.04.010 1:CAS:528:DC%2BD1MXotFCitLk%3D Ishrat T, Parveen K, Khan MM, Khuwaja G, Khan MB, Yousuf S, Ahmad A, Shrivastav P, Islam F (2009) Selenium prevents cognitive decline and oxidative damage in rat model of streptozotocin-induced experimental dementia of Alzheimer’s type. Brain Res 1281:117–127. doi: 10.1016/j.brainres.2009.04.010
51. 51. T Ishrat MN Hoda MB Khan S Yousuf M Ahmad MM Khan A Ahmad F Islam 2009 Amelioration of cognitive deficits and neurodegeneration by curcumin in rat model of sporadic dementia of Alzheimer’s type (SDAT) Eur Neuropsychopharmacol 19 9 636 647 10.1016/j.euroneuro.2009.02.002 19329286 10.1016/j.euroneuro.2009.02.002 1:CAS:528:DC%2BD1MXptVGkurs%3D Ishrat T, Hoda MN, Khan MB, Yousuf S, Ahmad M, Khan MM, Ahmad A, Islam F (2009) Amelioration of cognitive deficits and neurodegeneration by curcumin in rat model of sporadic dementia of Alzheimer’s type (SDAT). Eur Neuropsychopharmacol 19(9):636–647. doi: 10.1016/j.euroneuro.2009.02.002
52. 52. DK Dhull A Jindal RK Dhull S Aggarwal D Bhateja SS Padi 2012 Neuroprotective effect of cyclooxygenase inhibitors in ICV-STZ induced sporadic Alzheimer’s disease in rats J Mol Neurosci 46 1 223 235 10.1007/s12031-011-9583-6 21701788 10.1007/s12031-011-9583-6 1:CAS:528:DC%2BC38XosFKisA%3D%3D Dhull DK, Jindal A, Dhull RK, Aggarwal S, Bhateja D, Padi SS (2012) Neuroprotective effect of cyclooxygenase inhibitors in ICV-STZ induced sporadic Alzheimer’s disease in rats. J Mol Neurosci 46(1):223–235. doi: 10.1007/s12031-011-9583-6
53. 53. T Arendt 2009 Synaptic degeneration in Alzheimer’s disease Acta Neuropathol 118 1 167 179 10.1007/s00401-009-0536-x 19390859 10.1007/s00401-009-0536-x Arendt T (2009) Synaptic degeneration in Alzheimer’s disease. Acta Neuropathol 118(1):167–179. doi: 10.1007/s00401-009-0536-x
54. 54. RD Terry E Masliah DP Salmon N Butters R DeTeresa R Hill LA Hansen R Katzman 1991 Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment Ann Neurol 30 4 572 580 10.1002/ana.410300410 1789684 10.1002/ana.410300410 1:STN:280:DyaK387mtFOntw%3D%3D Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R (1991) Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 30(4):572–580. doi: 10.1002/ana.410300410
55. 55. DJ Selkoe 2002 Alzheimer’s disease is a synaptic failure Science 298 5594 789 791 10.1126/science.1074069 12399581 10.1126/science.1074069 1:CAS:528:DC%2BD38XotFSnur0%3D Selkoe DJ (2002) Alzheimer’s disease is a synaptic failure. Science 298(5594):789–791. doi: 10.1126/science.1074069
56. 56. CA Barnes 1999 Do synaptic markers provide a window on synaptic effectiveness in the aged hippocampus? Neurobiol Aging 20 3 349 351 10588584 10.1016/S0197-4580(99)00074-3 1:STN:280:DC%2BD3c%2Fltlyjtw%3D%3D discussion 359–360 Barnes CA (1999) Do synaptic markers provide a window on synaptic effectiveness in the aged hippocampus? Neurobiol Aging 20(3):349–351, discussion 359–360
57. 57. MM Nicolle M Gallagher M McKinney 1999 No loss of synaptic proteins in the hippocampus of aged, behaviorally impaired rats Neurobiol Aging 20 3 343 348 10588583 10.1016/S0197-4580(99)00054-8 1:STN:280:DC%2BD3c%2Fltlyjtg%3D%3D Nicolle MM, Gallagher M, McKinney M (1999) No loss of synaptic proteins in the hippocampus of aged, behaviorally impaired rats. Neurobiol Aging 20(3):343–348
58. 58. Y Deng B Li Y Liu K Iqbal I Grundke-Iqbal CX Gong 2009 Dysregulation of insulin signaling, glucose transporters, O-GlcNAcylation, and phosphorylation of tau and neurofilaments in the brain: implication for Alzheimer’s disease Am J Pathol 175 5 2089 2098 10.2353/ajpath.2009.090157 19815707 10.2353/ajpath.2009.090157 1:CAS:528:DC%2BC3cXhslSjtb0%3D Deng Y, Li B, Liu Y, Iqbal K, Grundke-Iqbal I, Gong CX (2009) Dysregulation of insulin signaling, glucose transporters, O-GlcNAcylation, and phosphorylation of tau and neurofilaments in the brain: implication for Alzheimer’s disease. Am J Pathol 175(5):2089–2098. doi: 10.2353/ajpath.2009.090157
59. 59. S Oddo A Caccamo D Cheng B Jouleh R Torp FM LaFerla 2007 Genetically augmenting tau levels does not modulate the onset or progression of Abeta pathology in transgenic mice J Neurochem 102 4 1053 1063 10.1111/j.1471-4159.2007.04607.x 17472708 10.1111/j.1471-4159.2007.04607.x 1:CAS:528:DC%2BD2sXhtVOqtL%2FJ Oddo S, Caccamo A, Cheng D, Jouleh B, Torp R, LaFerla FM (2007) Genetically augmenting tau levels does not modulate the onset or progression of Abeta pathology in transgenic mice. J Neurochem 102(4):1053–1063. doi: 10.1111/j.1471-4159.2007.04607.x
60. 60. M Salkovic-Petrisic J Osmanovic-Barilar MK Bruckner S Hoyer T Arendt P Riederer 2011 Cerebral amyloid angiopathy in streptozotocin rat model of sporadic Alzheimer’s disease: a long-term follow up study J Neural Transm 118 5 765 772 10.1007/s00702-011-0651-4 21533606 10.1007/s00702-011-0651-4 1:CAS:528:DC%2BC3MXlvFSqs70%3D Salkovic-Petrisic M, Osmanovic-Barilar J, Bruckner MK, Hoyer S, Arendt T, Riederer P (2011) Cerebral amyloid angiopathy in streptozotocin rat model of sporadic Alzheimer’s disease: a long-term follow up study. J Neural Transm 118(5):765–772. doi: 10.1007/s00702-011-0651-4