Insulin-resistant brain state after intracerebroventricular streptozotocin injection exacerbates Alzheimer-like changes in Tg2576 AβPP-overexpressing mice

Journal of Alzheimer's Disease

Volumn 19, Issue 2, 2010, Pages 691-704

  Plaschke, Konstanze ^a   Kopitz, Juergen ^b   Siegelin, Markus ^b   Schliebs, Reinhard ^c   Salkovic Petrisic, Melita ^d   Riederer, Peter ^e   Hoyer, Siegfried ^b  

^a Department of Anesthesiology ^*  (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF LEIPZIG   (Germany)

^d UNIVERSITY OF ZAGREB   (Croatia)

^e UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

Author keywords

Amyloid ; Glycogen synthase kinase 3; Insulin; Sporadic Alzheimer's disease; Streptozotocin; Tau; Transgenic 2576 mice

Indexed keywords

AMYLOID PRECURSOR PROTEIN; GLUCOSE; GLYCOGEN SYNTHASE KINASE 3; STREPTOZOCIN; TAU PROTEIN;

AGING; ALZHEIMER DISEASE; AMNESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DISEASE; COGNITION; CONTROLLED STUDY; DISEASE EXACERBATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; INSULIN RESISTANT BRAIN STATE; MAZE TEST; MORTALITY; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PSYCHOMETRY; TRANSGENIC MOUSE;

EID: 77049100748     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2010-1270     Document Type: Article

References (56)

1. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science 274, 99-102.
2. Carlson GA, Borchelt DR, Dake A, Turner S, Danielson V, Coffin JD, Eckman C, Meiners J, Nilsen SP, Younkin SG, Hsiao KK (1997) Genetic modification of the phenotypes produced by amyloid precursor protein overexpression in transgenic mice. Hum Mol Genet 6, 1951-1959.
3. Irizarry MC, McNamara M, Fedorchak K, Hsiao K, Hyman BT (1997) APPSw transgenic mice develop age-related Aβ deposits and neuropil abnormalities, but no neuronal loss in CA1. J Neuropathol Exp Neurol 56, 965-973.
4. Chapman PF, White GL, Jones MW, Cooper-Blacketer D, Marshall VJ, Irizarry M, Younkin L, Good MA, Bliss TV, Hyman BT, Younkin SG, Hsiao KK (1999) Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 2, 271-276.
5. Kawarabayashi T, Younkin LH, Saido TC, Shoji M, Ashe KH, Younkin SG (2001) Age-dependent changes in brain, CSF, and plasma amyloid (beta) protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J Neurosci 21, 372-381.
6. Frautschy SA,Yang F, Irrizarry M, Hyman B, Saido TC, Hsiao K, Cole GM (1998) Microglial response to amyloid plaques in APPsw transgenic mice. Am J Pathol 152, 307-317.
7. Ashe KH (2001) Learning and memory in transgenic mice modeling Alzheimer's disease. Learn Mem 8, 301-308.
8. Westerman MA, Cooper-Blacketer D, Mariash A, Kotilinek L, Kawarabayashi T, Younkin LH, Carlson GA, Younkin SG, Ashe KH (2002) The relationship between Aβ and memory in the Tg2576 mouse model of Alzheimer's disease. J Neurosci 22, 1858-1867. (Pubitemid 35386304)
9. Kotilinek LA, Bacskai B, Westerman M, Kawarabayashi T, Younking L, Hyman BT, Younkin S, Ashe KH (2002) Reversible memory loss in a mouse transgenic model of Alzheimer's disease. J Neurosci 22, 6331-6335.
10. Leibson CL, Rocca WA, Hanson VA, Cha R, Kokmen E, O'Brien PC, Palumbo PJ (1997) Risk of dementia among persons with diabetes mellitus: a population-based cohort study. Am J Epidemiol 145, 301-308. (Pubitemid 27082028)
11. Stolk RP, Breteler MM, Ott A, Pols HA, Lamberts SW, Grobbee DE, Hofman A (1997) Insulin and cognitive function in an elderly population. The Rotterdam Study. Diabetes Care 20, 792-795.
12. Neumann KF, Rojo L, Navarrete LP, Faŕias G, Reyes P, Maccioni RB (2008) Insulin resistance and Alzheimer's disease: molecular links & clinical implications. Curr Alzheimer Res 5, 438-447.
13. Salkovic-Petrisic M, Osmanovic J, Grünblatt E, Riederer P, Hoyer S (2009) Modeling sporadic Alzheimer disease: the insulin resistant brain state generates multiple long-term morphobiological abnormalities inclusive hyperphosphorylated tau protein and amyloid. A synthesis. J Alzheimers Dis 18, 729-750.
14. Jones A, Kulozik P, Ostertag A, Herzig S (2009) Common pathological processes and transcriptional pathways in Alzheimer's disease and type 2 diabetes. J Alzheimers Dis 16, 787-808.
15. 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.
16. Blokland A, Jolles J (1993) Spatial learning deficit and reduced hippocampal ChAT activity in rats after an ICV injection of streptozotocin. Pharmacol Biochem Behav 44, 491-494.
17. Lannert H,Hoyer S (1998) Intracerebroventricular administration of streptozotocin causes long-term diminutions in learning and memory abilities and in cerebral energy metabolism in adult rats. Behav Neurosci 112, 1199-1208. (Pubitemid 28519002)
18. Sharma M, Gupta YK (2001) Intracerebroventricular injection of streptozotocin in rats produces both oxidative stress in the brain and cognitive impairment. Life Sci 68, 1021-1029.
19. Shoham S, Bejar C, Kovalev E, Weinstock M (2003) Intracerebroventricular injection of streptozotocin causes neurotoxicity to myelin that contributes to spatial memory deficits in rats. Exp Neurol 184, 1043-1052.
20. Nitsch R, Hoyer S (1991) Local action of the diabetogenic drug, streptozotocin, on glucose and energy metabolism in rat brain cortex. Neurosci Lett 128, 199-202.
21. HellwegR, Nitsch R, Hock C, JakschM, Hoyer S (1992) Nerve growth factor and choline acetyltransferase activity levels in the rat brain following experimental impairment of cerebral glucose and energy metabolism. J Neurosci Res 31, 479-486.
22. Plaschke K, Hoyer S (1993) Action of the diabetogenic drug streptozotocin on glycolytic and glycogenolytic metabolism in adult rat brain cortex and hippocampus. Int J Dev Neurosci 11, 477-483.
23. Grünblatt 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, 757-770.
24. 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, 1005-1015.
25. Leloup C, Arluison M, Lepetit N, Cartier N, Marfaing-Jallat P, Ferŕe P, Ṕenicaud L (1994) Glucose transporter 2 (GLUT 2): expression in specific brain nuclei. Brain Res 638, 221-226.
26. Havrankova J, Schmechel D, Roth J, Brownstein M (1978) Identification of insulin in rat brain. Proc Natl Acad Sci USA 75, 5737-5741.
27. Zhao L, Teter B, Morihara T, Lim GP, Ambegaokar SS, Ubeda OJ, Frautschy SA, ColeGM.(2004) Insulin-degrading enzyme as a downstream target of insulin receptor signaling cascade: implications for Alzheimer's disease intervention. J Neurosci 24, 11120-11126.
28. Franklin KBJ, Paxinos G (1998) The mouse brain stereotaxic coordinates, Academic Press, San Diego.
29. Plaschke K, Staub J, Ernst E, Marti HH (2008) VEGF overexpression improves mice cognitive abilities after unilateral common carotid artery occlusion. Exp Neurol 214, 285-292.
30. Schenk EA, Churukian C, Willis C, Stotz E (1983) Staining problems with eosin Y: a note from the Biological Stain Commission. Stain Technol 58, 377-379.
31. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356.
32. Hoyer S (1998) Risk factors for Alzheimer's disease during aging. Impacts of glucose/energy metabolism. J Neural Transm Suppl 54, 187-194.
33. Jacobsen JS, Wu CC, Redwine JM, Comery TA, Arias R, Bowlby M, Martone R, Morrison JH, Pangalos MN, Reinhart PH, Bloom FE (2006) Early-onset behavioral and synaptic deficits in a mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 103, 5161-5166.
34. Middei S, Daniele S, Caprioli A, Ghirardi O, Ammassari-Teule M (2006) Progressive cognitive decline in a transgenic mouse model of Alzheimer's disease overexpressing mutant hAPPswe. Genes Brain Behav 5, 249-256.
35. Plaschke K, Yun SW, Martin E, Hoyer S, Bardenheuer HJ (2000) Linear relation between cerebral phosphocreatine con centration and memory capacities during permanent brain vessel occlusions in rats. Ann N Y Acad Sci 903, 299-306.
36. Benfenati F (2007) Synaptic plasticity and the neurobiology of learning and memory. Acta Biomed 78 (Suppl 1), 58-66.
37. Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10, 434-445.
38. Bigl M, Apelt J, Eschrich K, Schliebs R (2003) Cortical glucose metabolism is altered in aged transgenic Tg2576 mice that demonstrate Alzheimer plaque pathology. J Neural Transm 110, 77-94
39. Apelt J, Bigl M, Wunderlich P, Schliebs R (2004) Agingrelated increase in oxidative stress correlates with developmental pattern of beta-secretase activity and beta-amyloid plaque formation in transgenic Tg2576 mice with Alzheimerlike pathology. Int J Dev Neurosci 22, 475-484.
40. Schliebs R (2005) Basal forebrain cholinergic dysfunction in Alzheimer's disease-interrelationship with beta-amyloid, inflammation and neurotrophin signaling. Neurochem Res 30, 895-908.
41. Braak H, Braak E (1997) Diagnostic criteria for neuropathologic assessment of Alzheimer's disease. Neurobiol Aging 18 (4 Suppl), S85-S88.
42. Markesbery WR (1997) Neuropathological criteria for the diagnosis of Alzheimer's disease. Neurobiol Aging18 (Suppl), S13-S19.
43. Noda-Saita K, Terai K, Iwai A, Tsukamoto M, Shitaka Y, Kawabata S, Okada M, Yamaguchi T (2004) Exclusive association and simultaneous appearance of congophilic plaques and AT8-positive dystrophic neurites in Tg2576 mice suggest a mechanism of senile plaque formation and progression of neuritic dystrophy in Alzheimer's disease. Acta Neuropathol 108, 435-442.
44. Planel E, Tatebayashi Y, Miyasaka T, Liu L, Wang L, Herman M, Yu WH, Luchsinger JA, Wadzinski B, Duff KE, Takashima A (2007) Insulin dysfunction induces in vivo tau hyperphosphorylation through distinct mechanisms. J Neurosci 27, 13635-13648.
45. Alonso AC, Li B, Grundke-Iqbal I, Iqbal K (2008) Mechanism of tau-induced neurodegeneration in Alzheimer disease and related tauopathies. Curr Alzheimer Res 5, 375-384.
46. Myers A, Holmans P, Marshall H, Kwon J, Meyer D, Ramic D, Shears S, Booth J, DeVrieze FW, Crook R, Hamshere M, Abraham R, Tunstall N, Rice F, Carty S, Lillystone S, Kehoe P, Rudrasingham V, Jones L, Lovestone S, Perez-Tur J, Williams J, Owen MJ, Hardy J, Goate AM(2000) Susceptibility locus for Alzheimer's disease on chromosome 10. Science 290, 2304-2305.
47. Phiel CJ, Wilson CA, Lee VM, Klein PS (2003) GSK-3alpha regulates production of Alzheimer's disease amyloid-beta peptides. Nature 423, 435-439.
48. Rankin CA, Sun Q, Gamblin TC (2007) Tau phosphorylation by GSK-3beta promotes tangle-like filament morphology. Mol Neurodegener 2, 12.
49. Resende R, Ferreiro E, Pereira C, Oliveira CR (2008) ER stress is involved in Abeta-induced GSK-3beta activation and tau phosphorylation. J Neurosci Res 86, 2091-2099.
50. LeroyK, Boutajangout A, Authelet M,Woodgett JR, Anderton BH, Brion JP (2002) The active form of glycogen synthase kinase-3beta is associated with granulovacuolar degeneration in neurons in Alzheimer's disease. Acta Neuropathol 103, 91-99.
51. Pei JJ, Khatoon S, An WL, Nordlinder M, Tanaka T, Braak H, Tsujio I, Takeda M, Alafuzoff I, Winblad B, Cowburn RF, Grundke-Iqbal I, Iqbal K (2003) Role of protein kinase B in Alzheimer's neurofibrillary pathology. Acta Neuropathol 105, 381-392.
52. Griffin RJ, Moloney A, Kelliher M, Johnston JA, Ravid R, Dockery P, O'Connor R, O'Neill C (2005) Activation of Akt/PKB, increased phosphorylation of Akt substrates and loss and altered distribution of Akt and PTEN are features of Alzheimer's disease pathology. J Neurochem 93, 105-117.
53. Pei JJ, Tanaka T, Tung YC, Braak E, Iqbal K, Grundke-Iqbal I (1997) Distribution, levels, and activity of glycogen synthase kinase-3 in the Alzheimer disease brain. J Neuropathol Exp Neurol 56, 70-78.
54. Steen E, Terry MB, Riviera JE, Cannon LJ, Neely RT, Tavares R, Xu JX, Wandas RJ, de la Monte MS (2005) Impaired insulin and insulin-like growth factor expresion and signaling mechanisms in Alzheimer's disease-is this type 3 diabetes? J Alzheimers Dis 7, 63-80.
55. Preece P,Virley DJ, Costandi M, Coombes R, Moss SJ, Mudge AW, Jazin E, Cairns NJ (2003) Beta-secretase (BACE) and GSK-3 mRNA levels in Alzheimer's disease. Brain Res Mol Brain Res 116, 155-158.
56. Hye A, Kerr F, Archer N, Foy C, Poppe M, Brown R, Hamilton G, Powell J, Anderton B, Lovestone S (2005) Glycogen synthase kinase-3 is increased in white cells early in Alzheimer's disease. Neurosci Lett 373, 1-4.