Diabetes exacerbates amyloid and neurovascular pathology in aging-accelerated mice

Aging Cell

Volumn 11, Issue 6, 2012, Pages 1017-1026

  Currais, Antonio ^a   Prior, Marguerite ^a   Lo, David ^a   Jolivalt, Corinne ^b   Schubert, David ^a   Maher, Pamela ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Advanced glycation end products; Aging; Alzheimer's disease; Amyloid angiopathy; Diabetes; Neurovascular inflammation

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; TAU PROTEIN;

AGING; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BEHAVIOR; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE EXACERBATION; FEAR; GLUCOSE METABOLISM; HIPPOCAMPUS; IMMUNOREACTIVITY; MALE; MOUSE; NEUROPATHOLOGY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN GLYCOSYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SENESCENCE ACCELERATED MOUSE; WESTERN BLOTTING;

AGE FACTORS; AGING; AMYLOID BETA-PEPTIDES; ANIMALS; ASTROCYTES; BLOOD VESSELS; COGNITION DISORDERS; DIABETES MELLITUS, EXPERIMENTAL; GENE EXPRESSION; GLIAL FIBRILLARY ACIDIC PROTEIN; GLYCOSYLATION; GLYCOSYLATION END PRODUCTS, ADVANCED; HIPPOCAMPUS; HUMANS; MALE; MICE; MICE, TRANSGENIC; PHOSPHORYLATION; STREPTOZOCIN; TAU PROTEINS;

ANIMALIA; MUS;

EID: 84869179307     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12002     Document Type: Article

References (43)

1. Abbott NJ, Ronnback L, Hansson E (2006) Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev.7, 41-53.
2. Akter K, Lanza EA, Martin SA, Myronyuk N, Rua M, Raffa RB (2011) Diabetes mellitus and Alzheimer's disease: shared pathology and treatment?Br. J. Clin. Pharmacol.71, 365-376.
3. Berg L, McKeel Jr DW, Miller JP, Storandt M, Rubin EH, Morris JC, Baty J, Coats M, Norton J, Goate AM, Price JL, Gearing M, Mirra SS, Saunders AM (1998) Clinicopathologic studies in cognitively healthy aging and Alzheimer's disease: relation of histologic markers to dementia severity, age, sex, and apolipoprotein E genotype. Arch. Neurol.55, 326-335.
4. Biessels GJ, Deary IJ, Ryan CM (2008) Cognition and diabetes: a lifespan perspective. Lancet Neurol.7, 184-190.
5. Bishop NA, Lu T, Yankner BA (2010) Neural mechanisms of ageing and cognitive decline. Nature464, 529-535.
6. Buettner GR (2011) Superoxide dismutase in redox biology: the roles of superoxide and hydrogen peroxide. Anticancer Agents Med. Chem.11, 341-346.
7. Burdo JR, Chen Q, Calcutt NA, Schubert D (2009) The pathological interaction between diabetes and presymptomatic Alzheimer's disease. Neurobiol. Aging30, 1910-1917.
8. Canudas AM, Gutierrez-Cuesta J, Rodriguez MI, Acuna-Castroviejo D, Sureda FX, Camins A, Pallas M (2005) Hyperphosphorylation of microtubule-associated protein tau in senescence-accelerated mouse (SAM). Mech. Ageing Dev.126, 1300-1304.
9. Deane R, Zlokovic BV (2007) Role of the blood-brain barrier in the pathogenesis of Alzheimer's disease. Curr. Alzheimer Res.4, 191-197.
10. Del Valle J, Duran-Vilaregut J, Manich G, Casadesus G, Smith MA, Camins A, Pallas M, Pelegri C, Vilaplana J (2010) Early amyloid accumulation in the hippocampus of SAMP8 mice. J. Alzheimers Dis.19, 1303-1315.
11. Del Valle J, Duran-Vilaregut J, Manich G, Pallas M, Camins A, Vilaplana J, Pelegri C (2011) Cerebral amyloid angiopathy, blood-brain barrier disruption and amyloid accumulation in SAMP8 mice. Neurodegener. Dis.8, 421-429.
12. Duvernoy HM (2005). The Human Hippocampus: Functional Anatomy, Vascularization and Serial Sections with MRI, 3rd edn. New York: Springer.
13. Dyer DG, Dunn JA, Thorpe SR, Bailie KE, Lyons TJ, McCance DR, Baynes JW (1993) Accumulation of Maillard reaction products in skin collagen in diabetes and aging. J. Clin. Invest.91, 2463-2469.
14. Gerich JE (1986) Insulin-dependent diabetes mellitus: pathophysiology. Mayo Clin. Proc.61, 787-791.
15. Giannakopoulos P, Kovari E, Gold G, von Gunten A, Hof PR, Bouras C (2009) Pathological substrates of cognitive decline in Alzheimer's disease. Front Neurol. Neurosci.24, 20-29.
16. Grammas P (2011) Neurovascular dysfunction, inflammation and endothelial activation: implications for the pathogenesis of Alzheimer's disease. J. Neuroinflammation8, 26.
17. Greenberg ME, Xu B, Lu B, Hempstead BL (2009) New insights in the biology of BDNF synthesis and release: implications in CNS function. J. Neurosci.29, 12764-12767.
18. Hoozemans JJ, Rozemuller JM, van Haastert ES, Veerhuis R, Eikelenboom P (2008) Cyclooxygenase-1 and -2 in the different stages of Alzheimer's disease pathology. Curr. Pharm. Des.14, 1419-1427.
19. Huber JD, VanGilder RL, Houser KA (2006) Streptozotocin-induced diabetes progressively increases blood-brain barrier permeability in specific brain regions in rats. Am. J. Physiol. Heart Circ. Physiol.291, H2660-H2668.
20. Ikura Y, Kudo T, Tanaka T, Tanii H, Grundke-Iqbal I, Iqbal K, Takeda M (1998) Levels of tau phosphorylation at different sites in Alzheimer disease brain. NeuroReport9, 2375-2379.
21. Jolivalt CG, Lee CA, Beiswenger KK, Smith JL, Orlov M, Torrance MA, Masliah E (2008) Defective insulin signaling pathway and increased glycogen synthase kinase-3 activity in the brain of diabetic mice: parallels with Alzheimer's disease and correction by insulin. J. Neurosci. Res.86, 3265-3274.
22. Jolivalt CG, Hurford R, Lee CA, Dumaop W, Rockenstein E, Masliah E (2010) Type 1 diabetes exaggerates features of Alzheimer's disease in APP transgenic mice. Exp. Neurol.223, 422-431.
23. Kim B, Backus C, Oh S, Hayes JM, Feldman EL (2009) Increased tau phosphorylation and cleavage in mouse models of type 1 and type 2 diabetes. Endocrinology150, 5294-5301.
24. Kuhla B, Boeck K, Schmidt A, Ogunlade V, Arendt T, Munch G, Luth HJ (2007) Age- and stage-dependent glyoxalase I expression and its activity in normal and Alzheimer's disease brains. Neurobiol. Aging28, 29-41.
25. Kumar VB, Farr SA, Flood JF, Kamlesh V, Franko M, Banks WA, Morley JE (2000) Site-directed antisense oligonucleotide decreases the expression of amyloid precursor protein and reverses deficits in learning and memory in aged SAMP8 mice. Peptides21, 1769-1775.
26. Li C, Zhao R, Gao K, Wei Z, Yin MY, Lau LT, Chui D, Hoi Yu AC (2011) Astrocytes: implications for neuroinflammatory pathogenesis of Alzheimer's disease. Curr. Alzheimer Res.8, 67-80.
27. Maher PA, Schubert DR (2009) Metabolic links between diabetes and Alzheimer's disease. Expert Rev. Neurother.9, 617-630.
28. Mazzone T, Chait A, Plutzky J (2008) Cardiovascular disease risk in type 2 diabetes mellitus: insights from mechanistic studies. Lancet371, 1800-1809.
29. Mulder SD, Veerhuis R, Blankenstein MA, Nielsen HM (2011) The effect of amyloid associated proteins on the expression of genes involved in amyloid-beta clearance by adult human astrocytes. Exp. Neurol.233, 373-379.
30. Pallas M, Camins A, Smith MA, Perry G, Lee HG, Casadesus G (2008) From aging to Alzheimer's disease: unveiling "the switch" with the senescence-accelerated mouse model (SAMP8). J. Alzheimers Dis.15, 615-624.
31. Roriz-Filho JS, Sa-Roriz TM, Rosset I, Camozzato AL, Santos AC, Chaves ML, Moriguti JC, Roriz-Cruz M (2009) (Pre)diabetes, brain aging, and cognition. Biochim. Biophys. Acta1792, 432-443.
32. Schleicher ED, Wagner E, Nerlich AG (1997) Increased accumulation of the glycoxidation product N(epsilon)-(carboxymethyl)lysine in human tissues in diabetes and aging. J. Clin. Invest.99, 457-468.
33. Shoji M, Okada M, Ohta A, Higuchi K, Hosokawa M, Honda Y (1998) A morphological and morphometrical study of the retina in aging SAM mice. Ophthalmic Res.30, 172-179.
34. Singh R, Barden A, Mori T, Beilin L (2001) Advanced glycation end-products: a review. Diabetologia44, 129-146.
35. Srikanth V, Maczurek A, Phan T, Steele M, Westcott B, Juskiw D, Munch G (2011) Advanced glycation endproducts and their receptor RAGE in Alzheimer's disease. Neurobiol. Aging32, 763-777.
36. Swerdlow RH (2007) Is aging part of Alzheimer's disease, or is Alzheimer's disease part of aging?Neurobiol. Aging28, 1465-1480.
37. Takeda T (2009) Senescence-accelerated mouse (SAM) with special references to neurodegeneration models, SAMP8 and SAMP10 mice. Neurochem. Res.34, 639-659.
38. Takeda S, Sato N, Uchio-Yamada K, Sawada K, Kunieda T, Takeuchi D, Kurinami H, Shinohara M, Rakugi H, Morishita R (2010) Diabetes-accelerated memory dysfunction via cerebrovascular inflammation and Abeta deposition in an Alzheimer mouse model with diabetes. Proc. Natl Acad. Sci. U.S.A.107, 7036-7041.
39. Thinakaran G, Koo EH (2008) Amyloid precursor protein trafficking, processing, and function. J. Biol. Chem.283, 29615-29619.
40. Thornalley PJ (1996) Pharmacology of methylglyoxal: formation, modification of proteins and nucleic acids, and enzymatic detoxification - a role in pathogenesis and antiproliferative chemotherapy. Gen. Pharmacol.27, 565-573.
41. Utter S, Tamboli IY, Walter J, Upadhaya AR, Birkenmeier G, Pietrzik CU, Ghebremedhin E, Thal DR (2008) Cerebral small vessel disease-induced apolipoprotein E leakage is associated with Alzheimer disease and the accumulation of amyloid beta-protein in perivascular astrocytes. J. Neuropathol. Exp. Neurol.67, 842-856.
42. Wrighten SA, Piroli GG, Grillo CA, Reagan LP (2009) A look inside the diabetic brain: contributors to diabetes-induced brain aging. Biochim. Biophys. Acta1792, 444-453.
43. Xue M, Rabbani N, Thornalley PJ (2011) Glyoxalase in ageing. Semin. Cell Dev. Biol.22, 293-301.