Age-dependent impairment of glucose tolerance in the 3xTg-AD mouse model of Alzheimer's disease

FASEB Journal

Volumn 29, Issue 10, 2015, Pages 4273-4284

  Vandal, Milene ^a,b,d   White, Phillip ^b,c,e,f   Chevrier, Geneviève ^c,f   Tremblay, Cyntia ^d   St Amour, Isabelle ^a,d   Planel, Emmanuel ^d   Marette, Andre ^b,c,f   Calon, Frederic ^a,b,d  

^a Faculte de Pharmacie   (France)

^b LAVAL UNIVERSITY   (Canada)

^c UNIVERSITÉ LAVAL   (Canada)

^d LAVAL UNIVERSITY   (Canada)

^e DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f LAVAL UNIVERSITY   (Canada)

Author keywords

Amyloid; Insulin; Pancreas

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; INSULIN; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (1-42); GLUCOSE BLOOD LEVEL; PEPTIDE FRAGMENT;

3XTG MOUSE; AGE DISTRIBUTION; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DETERIORATION; DIET RESTRICTION; FEMALE; GLYCEMIC CONTROL; IMPAIRED GLUCOSE TOLERANCE; INSULIN BLOOD LEVEL; INSULIN SENSITIVITY; MALE; METABOLIC PARAMETERS; MOUSE; NEUROPATHOLOGY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; 129 MOUSE; AGE; ANIMAL; BLOOD; BRAIN CORTEX; C57BL MOUSE; DISEASE MODEL; FLUORESCENCE MICROSCOPY; GENETICS; GLUCOSE BLOOD LEVEL; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE TEST; HUMAN; METABOLISM; PANCREAS ISLET; SEX DIFFERENCE; TRANSGENIC MOUSE; WESTERN BLOTTING;

AGE FACTORS; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BLOOD GLUCOSE; BLOTTING, WESTERN; CEREBRAL CORTEX; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; FEMALE; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE TEST; HUMANS; INSULIN; ISLETS OF LANGERHANS; MALE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; PEPTIDE FRAGMENTS; SEX FACTORS;

EID: 84946905083     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-268482     Document Type: Article

References (79)

1. Akomolafe, A., Beiser, A., Meigs, J. B., Au, R., Green, R. C., Farrer, L. A., Wolf, P. A., and Seshadri, S. (2006) Diabetes mellitus and risk of developing Alzheimer disease: results from the Framingham Study. Arch. Neurol. 63,1551-1555
2. Ott,A.,Stolk,R.P.,vanHarskamp,F.,Pols,H.A.,Hofman,A.,and Breteler, M. M. (1999) Diabetes mellitus and the risk of dementia: The Rotterdam Study. Neurology 53, 1937-1942
3. Profenno, L. A., Porsteinsson, A. P., and Faraone, S. V. (2010) Metaanalysis of Alzheimer's disease risk with obesity, diabetes, and related disorders. Biol. Psychiatry 67,505-512
4. Luchsinger, J. A., Cheng, D., Tang, M. X., Schupf, N., and Mayeux, R. (2012) Central obesity in the elderly is related to late-onset Alzheimer disease. Alzheimer Dis. Assoc. Disord. 26, 101-105
5. Whitmer, R. A., Gustafson, D. R., Barrett-Connor, E., Han, M. N., Gunderson, E. P., and Yaffe, K. (2008) Central obesity and increased risk of dementia more than three decades later. Neurology 71, 1057-1064
6. Schrijvers,E.M.,Witteman,J.C.,Sijbrands,E.J.,Hofman,A.,KoudstAl, P. J., and Breteler, M. M. (2010) Insulinmetabolism andtherisk of Alzheimer disease: the Rotterdam Study. Neurology 75, 1982-1987
7. Forti, P., Pisacane, N., Rietti, E., Lucicesare, A., Olivelli, V., Mariani, E., Mecocci, P., and Ravaglia, G. (2010) Metabolic syndrome and risk of dementia in older adults. J. Am. Geriatr. Soc. 58,487-492
8. Raffaitin, C., Gin, H., Empana, J. P., Helmer, C., Berr, C., Tzourio, C., Portet, F., Dartigues, J. F., Alpérovitch, A., and Barberger-Gateau, P. (2009) Metabolic syndrome and riskfor incident Alzheimer's disease or vascular dementia: the Three-City Study. Diabetes Care 32, 169-174
9. El Khoury, N. B., Gratuze, M., Papon, M. A., Bretteville, A., and Planel, E. (2014) Insulin dysfunction and tau pathology. Front. Cell. Neurosci. 8,22
10. Papon, M. A., El Khoury, N. B., Marcouiller, F., Julien, C., Morin, F., Bretteville, A., Petry, F. R., Gaudreau, S., Amrani, A., Mathews, P. M., Hébert, S. S., and Planel, E. (2013) Deregulation of protein phosphatase 2A and hyperphosphorylation of τ protein following onset of diabetes in NOD mice. Diabetes 62, 609-617
11. Planel,E.,Tatebayashi,Y.,Miyasaka,T.,Liu,L.,Wang,L.,Herman, M., Yu, W. H., Luchsinger, J. A., Wadzinski, B., Duff, K. E., and Takashima, A. (2007) Insulin dysfunction induces in vivo tau hyperphosphorylation through distinct mechanisms. J. Neurosci. 27, 13635-13648
12. Ho, L., Qin, W., Pompl, P. N., Xiang, Z., Wang, J., Zhao, Z., Peng, Y., Cambareri, G., Rocher, A., Mobbs,C. V., Hof, P. R., and Pasinetti, G. M. (2004) Diet-induced insulin resistance promotes amyloidosis in a transgenic mouse model of Alzheimer's disease. FASEB J. 18, 902-904
13. Julien, C., Tremblay, C., Phivilay, A., Berthiaume, L., Emond, V., Julien, P., and Calon, F. (2010) High-fat diet aggravates amyloid-beta and tau pathologies in the 3xTg-AD mouse model. Neurobiol. Aging 31,1516-1531
14. Takeda, S., Sato, N., Uchio-Yamada, K., Sawada, K., Kunieda, T., Takeuchi, D., Kurinami, H., Shinohara, M., Rakugi, H., and Morishita, R. (2010) Diabetes-accelerated memory dysfunction via cerebrovascular inflammation and Abeta deposition in an Alzheimer mouse model with diabetes. Proc.Natl.Acad.Sci.USA107,7036-7041
15. Kalaria, R. N. (2009) Neurodegenerative disease: diabetes, microvascular pathology and Alzheimer disease. Nat. Rev. Neurol. 5, 305-306
16. Sonnen, J. A., Larson, E. B., Brickell, K., Crane, P. K., Woltjer, R., Montine, T. J., and Craft, S. (2009) Different patterns of cerebral injury in dementia with or without diabetes. Arch. Neurol. 66, 315-322
17. Craft, S., Asthana, S., Schellenberg, G., Cherrier, M., Baker, L. D., Newcomer, J., Plymate, S., Latendresse, S., Petrova, A., Raskind, M., Peskind, E., Lofgreen, C., and Grimwood, K. (1999) Insulin metabolism in Alzheimer's disease differs according to apolipoprotein E genotype and gender. Neuroendocrinology 70, 146-152
18. Leibson, C. L., Rocca, W. A., Hanson, V. A., Cha, R., Kokmen, E., O'Brien, P. C., and Palumbo, P. J. (1997) Risk of dementia among persons with diabetes mellitus: a population-based cohort study. Am. J. Epidemiol. 145,301-308
19. Craft, S., Peskind, E., Schwartz, M. W., Schellenberg, G. D., Raskind, M., and Porte, D., Jr. (1998) Cerebrospinal fluid and plasma insulin levels in Alzheimer's disease: relationship to severity of dementia and apolipoprotein E genotype. Neurology 50,164-168
20. Janson, J., Laedtke, T., Parisi, J. E., O'Brien, P., Petersen, R. C., and Butler, P. C. (2004) Increased risk of type 2 diabetes in Alzheimer disease. Diabetes 53, 474-481
21. Frölich, L., Blum-Degen, D., Bernstein, H. G., Engelsberger, S., Humrich, J., Laufer, S., Muschner, D., Thalheimer, A., Türk, A., Hoyer, S., Zöchling, R., Boissl, K. W., Jellinger, K., and Riederer, P. (1998) Brain insulin and insulin receptors in aging and sporadic Alzheimer'sdisease.J. Neural Transm. 105,423-438
22. Steen, E., Terry, B. M., Rivera, E. J., Cannon, J. L., Neely, T. R., Tavares, R., Xu, X. J., Wands, J. R., and de la Monte, S. M. (2005) Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease: is this type 3 diabetes? J. Alzheimers Dis. 7,63-80
23. Talbot, K., Wang, H. Y., Kazi, H., Han, L. Y., Bakshi, K. P., Stucky, A., Fuino, R. L., Kawaguchi, K. R., Samoyedny, A. J., Wilson, R. S., Arvanitakis, Z., Schneider, J. A., Wolf, B. A., Bennett, D. A., Trojanowski, J. Q., and Arnold, S. E. (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, 1316-1338
24. Pedersen, W. A., and Flynn, E. R. (2004) Insulin resistance contributes to aberrant stress responses in the Tg2576 mouse model of Alzheimer's disease.Neurobiol. Dis. 17,500-506
25. Oddo, S., Caccamo, A., Shepherd, J. D., Murphy, M. P., Golde, T. E., Kayed, R., Metherate, R., Mattson, M. P., Akbari, Y., andLaFerla, F. M. (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39, 409-421
26. Lebbadi, M., Julien, C., Phivilay, A., Tremblay, C., Emond, V., Kang, J. X., and Calon, F. (2011) Endogenous conversion of omega-6 into omega-3 fatty acids improves neuropathology in an animal model of Alzheimer'sdisease.J. Alzheimers Dis. 27,853-869
27. Bories, C., Guitton, M. J., Julien, C., Tremblay, C., Vandal, M., Msaid, M., De Koninck, Y., and Calon, F. (2012) Sex-dependent alterations in social behaviour and cortical synaptic activity coincide at different ages in a model of Alzheimer's disease. PLoS ONE 7, e46111
28. Hirata-Fukae,C.,Li,H.F.,Hoe,H.S.,Gray,A.J.,Minami,S.S.,Hamada, K.,Niikura,T.,Hua,F.,Tsukagoshi-Nagai,H.,Horikoshi-Sakuraba,Y., Mughal,M.,Rebeck,G.W.,LaFerla,F.M.,Mattson,M.P.,Iwata,N., Saido, T. C., Klein, W. L., Duff, K. E., Aisen, P. S., and Matsuoka, Y. (2008) Females exhibit more extensive amyloid, but not tau, pathology in an Alzheimer transgenic model. Brain Res. 1216,92-103
29. Mastrangelo, M. A., and Bowers, W. J. (2008) Detailed immunohistochemical characterization of temporal and spatial progression of Alzheimer's disease-related pathologies in male triple-transgenic mice. BMC Neurosci. 9, 81
30. España, J., Giménez-Llort, L., Valero, J., Miñano, A., Rábano, A., Rodriguez-Alvarez, J., LaFerla, F. M., and Saura, C. A. (2010)
31. Intraneuronal beta-amyloid accumulation in the amygdala enhances fear and anxiety in Alzheimer's disease transgenic mice. Biol. Psychiatry 67,513-521
32. Pietropaolo, S., Feldon, J., and Yee, B. K. (2008) Age-dependent phenotypic characteristics of a triple transgenic mouse model of Alzheimer disease. Behav. Neurosci. 122, 733-747
33. Sterniczuk, R., Antle, M. C., Laferla, F. M., and Dyck, R. H. (2010) Characterization of the 3xTg-AD mouse model of Alzheimer's disease: part 2: behavioral and cognitive changes. Brain Res. 1348, 149-155
34. Mody, N., Agouni, A., McIlroy,G. D.,Platt, B., andDelibegovic, M. (2011) Susceptibility to diet-induced obesity and glucose intolerance in the APP (SWE)/PSEN1 (A246E) mouse model of Alzheimer's disease is associated with increased brain levels of protein tyrosine phosphatase 1B (PTP1B) and retinol-binding protein 4 (RBP4), and basal phosphorylation of S6 ribosomal protein. Diabetologia 54, 2143-2151
35. Janson, J., Soeller, W. C., Roche, P. C., Nelson, R. T., Torchia, A. J., Kreutter, D. K., and Butler, P. C. (1996) Spontaneous diabetes mellitus intransgenic mice expressing humanislet amyloid polypeptide. Proc. Natl. Acad. Sci. USA 93, 7283-7288
36. Westermark, P., Andersson, A., and Westermark, G. T. (2011) Islet amyloid polypeptide, islet amyloid, and diabetes mellitus. Physiol. Rev. 91, 795-826
37. Nugent, D. A., Smith, D. M., and Jones, H. B. (2008) A review of islet of Langerhans degeneration in rodent models of type 2 diabetes. Toxicol. Pathol. 36,529-551
38. Halban, P. A., Polonsky, K. S., Bowden, D. W., Hawkins, M. A., Ling, C., Mather, K. J., Powers, A. C., Rhodes, C. J., Sussel, L., and Weir, G. C. (2014) β-cell failure in type 2 diabetes: postulated mechanisms and prospectsforprevention and treatment. J. Clin. Endocrinol. Metab. 99, 1983-1992
39. Götz, J., Ittner, L. M., and Lim, Y. A. (2009) Common features between diabetes mellitus and Alzheimer's disease.Cell. Mol. Life Sci. 66, 1321-1325
40. Lorenzo,A.,Razzaboni,B.,Weir,G.C.,andYankner,B.A.(1994) Pancreatic islet cell toxicity of amylin associated with type-2 diabetes mellitus. Nature 368, 756-760
41. Montane, J., Klimek-Abercrombie, A., Potter, K. J., Westwell-Roper, C., and Bruce Verchere, C. (2012) Metabolic stress, IAPP and islet amyloid. Diabetes Obes. Metab. 14(Suppl 3), 68-77
42. Miklossy, J., Qing, H., Radenovic, A., Kis, A., Vileno, B., Làszló, F., Miller, L., Martins, R. N., Waeber, G., Mooser, V., Bosman, F., Khalili, K., Darbinian, N., and McGeer, P. L. (2010) Beta amyloid and hyperphosphorylated tau deposits in the pancreas in type 2 diabetes. Neurobiol. Aging 31,1503-1515
43. Vandal, M., White, P. J., Tremblay, C., St-Amour, I., Chevrier, G., Emond,V.,Lefrançois,D.,Virgili,J.,Planel,E.,Giguere,Y.,Marette, A., and Calon, F. (2014) Insulin reverses the high-fat diet-induced increase in brain Aβ and improves memory in an animal model of Alzheimer disease. Diabetes 63, 4291-4301
44. Jiménez-Palomares, M., Ramos-Rodríguez, J. J., López-Acosta, J. F., Pacheco-Herrero, M., Lechuga-Sancho, A. M., Perdomo, G., García-Alloza, M., and Cózar-Castellano, I. (2012) Increased Ab production prompts the onset of glucose intolerance and insulin resistance. Am. J. Physiol. Endocrinol. Metab. 302, E1373-E1380
45. Callahan, M. J., Lipinski, W. J., Bian, F., Durham, R. A., Pack, A., and Walker, L. C. (2001) Augmented senile plaque load in aged female beta-amyloid precursor protein-transgenic mice. Am. J. Pathol. 158, 1173-1177
46. Lewis, J., Dickson, D. W., Lin, W. L., Chisholm, L., Corral, A., Jones, G., Yen, S. H., Sahara, N., Skipper, L., Yager, D., Eckman, C., Hardy, J., Hutton, M., and McGowan, E. (2001) Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 293, 1487-1491
47. Clinton, L. K., Billings, L. M., Green, K. N., Caccamo, A., Ngo, J., Oddo, S., McGaugh, J. L., and LaFerla, F. M. (2007) Age-dependent sexual dimorphism in cognition and stress response in the 3xTg-AD mice. Neurobiol. Dis. 28,76-82
48. Bomba, M., Ciavardelli, D., Silvestri, E., Canzoniero, L. M., Lattanzio, R., Chiappini, P., Piantelli, M., Di Ilio, C., Consoli, A., and Sensi, S. L. (2013) Exenatide promotes cognitive enhancement and positive brain metabolic changes in PS1-KI mice but has no effects in 3xTg-AD animals. Cell Death Dis. 4, e612
49. Masciopinto, F., Di Pietro, N., Corona, C., Bomba, M., Pipino, C., Curcio, M., Di Castelnuovo, A., Ciavardelli, D., Silvestri, E., Canzoniero, L. M., Sekler, I., Pandolfi, A., and Sensi, S. L. (2012) Effects of long-term treatment with pioglitazone on cognition and glucose metabolism of PS1-KI, 3xTg-AD, and wild-type mice. Cell Death Dis. 3,e448
50. Faber,O. K., Hagen, C., Binder, C., Markussen, J., Naithani, V. K., Blix, P. M., Kuzuya, H., Horwitz, D. L., Rubenstein, A. H., and Rossing, N. (1978) Kinetics of human connecting peptide in normal and diabetic subjects. J. Clin. Invest. 62,197-203
51. Ferrannini, E., Wahren, J., Faber, O. K., Felig, P., Binder, C., and DeFronzo, R. A. (1983) Splanchnic and renal metabolism of insulin in human subjects: a dose-response study. Am.J.Physiol.244, E517-E527
52. Brandt, M. R., Kehlet, H., Faber, O., and Binder Chr. (1977) C-peptide and insulin during blockade of the hyperglycaemic response to surgery by epidural analgesia. Clin. Endocrinol. (Oxf.) 6, 167-170
53. Johnston, D. G., Alberti, K. G., Faber, O. K., and Binder, C. (1977) Hyperinsulinism of hepatic cirrhosis: Diminished degradation or hypersecretion? Lancet 309,10-13
54. Hardy, J., and Selkoe, D. J. (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356
55. Habicht, G., Haupt, C., Friedrich, R. P., Hortschansky, P., Sachse, C., Meinhardt, J., Wieligmann, K., Gellermann, G. P., Brodhun, M., Götz, J., Halbhuber, K. J., Röcken, C., Horn, U., and Fändrich, M. (2007) Directed selection of a conformational antibody domain that prevents mature amyloid fibril formation by stabilizing Abeta protofibrils. Proc. Natl. Acad. Sci. USA 104, 19232-19237
56. Harper,J.D.,Wong,S.S.,Lieber,C.M.,andLansbury,P.T.(1997) Observation of metastable Abeta amyloid protofibrils by atomic force microscopy. Chem. Biol. 4,119-125
57. Kayed, R., Head, E., Thompson, J. L., McIntire, T. M., Milton, S. C., Cotman,C.W.,andGlabe,C.G.(2003)Commonstructureofsoluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489
58. Lesné,S.,Koh,M.T.,Kotilinek,L.,Kayed,R.,Glabe,C.G.,Yang,A., Gallagher, M., and Ashe, K. H. (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440,352-357
59. Rijal Upadhaya, A., Capetillo-Zarate, E., Kosterin, I., Abramowski, D., Kumar, S., Yamaguchi, H., Walter, J., Fändrich, M., Staufenbiel, M., and Thal, D. R. (2012) Dispersible amyloid β-protein oligomers, protofibrils, and fibrils represent diffusible but not soluble aggregates: their role in neurodegeneration in amyloid precursor protein (APP) transgenic mice. Neurobiol. Aging 33, 2641-2660
60. Shankar, G. M., Li, S., Mehta, T. H., Garcia-Munoz, A., Shepardson, N. E., Smith, I., Brett, F. M., Farrell, M. A., Rowan, M. J., Lemere, C. A., Regan, C. M., Walsh, D. M., Sabatini, B. L., and Selkoe, D. J. (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 14,837-842
61. Walsh, D. M., Lomakin, A., Benedek, G. B., Condron, M. M., and Teplow, D. B. (1997) Amyloid beta-protein fibrillogenesis. Detection of a protofibrillar intermediate. J. Biol. Chem. 272, 22364-22372
62. Näslund, J., Haroutunian, V., Mohs, R., Davis, K. L., Davies, P., Greengard, P., and Buxbaum, J. D. (2000) Correlation between elevated levels of amyloid beta-peptide in the brain and cognitive decline. JAMA 283, 1571-1577
63. Nelson,P.T.,Alafuzoff,I.,Bigio,E.H.,Bouras,C.,BrAk,H.,Cairns, N.J.,Castellani,R.J.,Crain,B.J.,Davies,P.,DelTredici,K.,Duyckaerts, C.,Frosch,M.P.,Haroutunian,V.,Hof,P.R.,Hulette,C.M.,Hyman, B. T., Iwatsubo, T., Jellinger, K. A., Jicha, G. A., Kövari, E., Kukull, W. A., Leverenz,J.B.,Love,S.,Mackenzie,I.R.,Mann,D.M.,Masliah,E., McKee,A.C.,Montine,T.J.,Morris,J.C.,Schneider,J.A.,Sonnen, J.A.,Thal, D.R.,Trojanowski,J.Q.,Troncoso,J.C.,Wisniewski,T., Woltjer, R. L., and Beach, T. G. (2012) Correlation of Alzheimer disease neuropathologic changes with cognitive status: a review of the literature. J. Neuropathol. Exp. Neurol. 71,362-381
64. Tremblay, C., Pilote, M., Phivilay, A., Emond, V., Bennett, D. A., and Calon, F. (2007) Biochemical characterization of Abeta and tau pathologies in mild cognitive impairment and Alzheimer's disease. J. Alzheimers Dis. 12,377-390
65. Hyman,B.T.,Phelps,C.H.,Beach,T.G.,Bigio,E.H.,Cairns,N.J., Carrillo, M. C., Dickson, D. W., Duyckaerts, C., Frosch, M. P., Masliah, E.,Mirra,S.S.,Nelson,P.T.,Schneider,J.A.,Thal,D.R.,Thies,B., Trojanowski, J. Q., Vinters, H. V., and Montine, T. J. (2012) National Institute on Aging-Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease. Alzheimers Dement. 8, 1-13
66. Westermark, P. (1972) Quantitative studies on amyloid in the islets of Langerhans. Ups. J. Med. Sci. 77, 91-94
67. Cooper, G. J., Willis, A. C., Clark, A., Turner, R. C., Sim, R. B., and Reid, K. B. (1987) Purification and characterization of a peptide from amyloid-rich pancreases of type 2 diabetic patients. Proc. Natl. Acad. Sci. USA 84, 8628-8632
68. Jhamandas, J. H., Li, Z., Westaway, D., Yang, J., Jassar, S., and MacTavish, D. (2011) Actions of β-amyloid protein on human neurons are expressed through the amylin receptor. Am. J. Pathol. 178,140-149
69. Kimura, R., MacTavish, D., Yang, J., Westaway, D., and Jhamandas, J. H. (2012) Beta amyloid-induced depression of hippocampal longterm potentiation is mediated through the amylin receptor. J. Neurosci. 32, 17401-17406
70. Lim,Y.A.,Rhein,V.,Baysang,G.,Meier,F.,Poljak,A.,Raftery,M.J., Guilhaus,M.,Ittner,L.M.,Eckert,A.,andGötz, J. (2010) Abeta and human amylin share a common toxicity pathway via mitochondrial dysfunction. Proteomics 10, 1621-1633
71. Seeliger, J., Weise, K., Opitz, N., and Winter, R. (2012) The effect of Aβ on IAPP aggregation in the presence of an isolated β-cell membrane. J. Mol. Biol. 421, 348-363
72. Yan, L. M., Velkova, A., and Kapurniotu, A. (2014) Molecular characterization of the hetero-assembly of β-amyloid peptide with islet amyloid polypeptide. Curr.Pharm.Des.20, 1182-1191
73. Schwartz, P. (1965) Senile cerebral, pancreatic insular and cardiac amyloidosis. Trans. N. Y. Acad. Sci. 27, 393-413
74. Aguzzi, A., and Rajendran, L. (2009) The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 64,783-790
75. Eisele, Y. S., Obermüller, U., Heilbronner, G., Baumann, F., Kaeser, S. A., Wolburg, H., Walker, L. C., Staufenbiel, M., Heikenwalder, M., and Jucker, M. (2010) Peripherally applied Abeta-containing inoculates induce cerebral beta-amyloidosis. Science 330, 980-982
76. Sponarova, J., Nyström, S. N., and Westermark, G. T. (2008) AAamyloidosis can be transferred by peripheral blood monocytes. PLoS ONE 3,e3308
77. Zhang, Y., Zhou, B., Deng, B., Zhang, F., Wu, J., Wang, Y., Le, Y., and Zhai, Q. (2013) Amyloid-β induces hepatic insulin resistance in vivo via JAK2. Diabetes 62, 1159-1166
78. Zhang, S., Smailagic, N., Hyde, C., Noel-Storr, A. H., Takwoingi, Y., McShane, R., and Feng, J. (2014) (11)C-PIB-PET for the early diagnosis of Alzheimer's disease dementia and other dementias in people withmild cognitive impairment (MCI). Cochrane DatabaseSyst. Rev. 7, CD010386
79. Toledo, J. B., Arnold, S. E., Raible, K., Brettschneider, J., Xie, S. X., Grossman, M., Monsell, S. E., Kukull, W. A., and Trojanowski, J. Q. (2013) Contribution of cerebrovascular disease in autopsy confirmed neurodegenerative disease cases in the National Alzheimer's Coordinating Centre. Brain 136, 2697-2706