Chronic diabetic states worsen Alzheimer neuropathology and cognitive deficits accompanying disruption of calcium signaling in leptin-deficient APP/PS1 mice

Oncotarget

Volumn 8, Issue 27, 2017, Pages 43617-43634

  Zhang, Shuai ^a   Chai, Rui ^a   Yang, Ying Ying ^a   Guo, Shi Qi ^a   Wang, Shan ^a   Guo, Tian ^a   Xu, Shuang Feng ^a   Zhang, Yan Hui ^a   Wang, Zhan You ^a   Guo, Chuang ^a  

^a NORTHEASTERN UNIVERSITY   (China)

Author keywords

Alzheimer's disease; Calcium; Diabetes mellitus; Tau; amyloid

Indexed keywords

AMYLOID BETA PROTEIN; CALCIUM; CALPAIN; TAU PROTEIN; LEPTIN;

ALZHEIMER DISEASE; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL DEATH; COGNITIVE DEFECT; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE ASSOCIATION; DISEASE EXACERBATION; ENZYME PHOSPHORYLATION; INFLAMMATION; MENTAL DETERIORATION; MOUSE; NERVE CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PROTEIN PHOSPHORYLATION; SYNAPTIC LOSS; SYNAPTIC TRANSMISSION; ANIMAL; BRAIN; COMPLICATION; DISEASE MODEL; GENETICS; HUMAN; MALE; MEMORY DISORDER; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION; PROTEINOSIS; PSYCHOLOGY; SIGNAL TRANSDUCTION; SYNAPSE; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BRAIN; CALCIUM SIGNALING; COGNITIVE DYSFUNCTION; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; HUMANS; INFLAMMATION; LEPTIN; MALE; MEMORY DISORDERS; MICE; MICE, TRANSGENIC; PHOSPHORYLATION; PROTEIN AGGREGATION, PATHOLOGICAL; SIGNAL TRANSDUCTION; SYNAPSES; TAU PROTEINS;

EID: 85021836187     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.17116     Document Type: Article

References (75)

1. Lorenzo A, Yankner BA. Amyloid fibril toxicity in Alzheimer's disease and diabetes. Ann N Y Acad Sci. 1996;777:89-95.
2. Biessels GJ, Staekenborg S, Brunner E, Brayne C, Scheltens P. Risk of dementia in diabetes mellitus: a systematic review. Lancet Neurol. 2006;5:64-74.
3. Haan MN. Therapy Insight: type 2 diabetes mellitus and the risk of late-onset Alzheimer's disease. Nat Clin Pract Neurol. 2006;2:159-166.
4. Biessels GJ, Reagan LP. Hippocampal insulin resistance and cognitive dysfunction. Nat Rev Neurosci. 2015;16:660-671.
5. Palleria C, Leporini C, Maida F, Succurro E, De Sarro G, Arturi F, Russo E. Potential effects of current drug therapies on cognitive impairment in patients with type 2 diabetes. Front Neuroendocrinol. 2016; 42:76-92.
6. Huang CC, Chung CM, Leu HB, Lin LY, Chiu CC, Hsu CY, Chiang CH, Huang PH, Chen TJ, Lin SJ, Chen JW, Chan WL. Diabetes mellitus and the risk of Alzheimer's disease: a nationwide population-based study. PLoS One. 2014;9:e87095.
7. Xu W, Qiu C, Winblad B, Fratiglioni L. The effect of borderline diabetes on the risk of dementia and Alzheimer's disease. Diabetes. 2007;56:211-216.
8. Steen E, Terry BM, Rivera EJ, Cannon JL, Neely TR, Tavares R, Xu XJ, Wands JR, de la Monte SM. Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease is this type 3 diabetes? J Alzheimers Dis. 2005;7:63-80.
9. Schubert M, Gautam D, Surjo D, Ueki K, Baudler S, Schubert D, Kondo T, Alber J, Galldiks N, Kustermann E, Arndt S, Jacobs AH, Krone W, et al. Role for neuronal insulin resistance in neurodegenerative diseases. Proc Natl Acad Sci U S A. 2004;101:3100-3105.
10. Baker LD, Cross DJ, Minoshima S, Belongia D, Watson GS, Craft S. Insulin resistance and Alzheimer-like reductions in regional cerebral glucose metabolism for cognitively normal adults with prediabetes or early type 2 diabetes. Arch Neurol. 2011;68:51-57.
11. Deane R, Du Yan S, Submamaryan RK, LaRue B, Jovanovic S, Hogg E, Welch D, Manness L, Lin C, Yu J, Zhu H, Ghiso J, Frangione B, et al. RAGE mediates amyloid-beta peptide transport across the blood-brain barrier and accumulation in brain. Nat Med. 2003;9:907-913.
12. Takeda S, Sato N, Uchio-Yamada K, Sawada K, Kunieda T, Takeuchi D, Kurinami H, Shinohara M, Rakugi H, Morishita R. Diabetes-accelerated memory dysfunction via cerebrovascular inflammation and Abeta deposition in an Alzheimer mouse model with diabetes. Proc Natl Acad Sci U S A. 2010;107:7036-7041.
13. Butterfield DA, Di Domenico F, Barone E. Elevated risk of type 2 diabetes for development of Alzheimer disease: a key role for oxidative stress in brain. Biochim Biophys Acta. 2014;1842:1693-1706.
14. Wei Y, Han C, Wang Y, Wu B, Su T, Liu Y, He R. Ribosylation triggering Alzheimer's disease-like Tau hyperphosphorylation via activation of CaMKII. Aging Cell. 2015;14:754-763.
15. Miklossy J, McGeer PL. Common mechanisms involved in Alzheimer's disease and type 2 diabetes: a key role of chronic bacterial infection and inflammation. Aging (Albany NY). 2016;8:575-588.
16. Calsolaro V, Edison P. Neuroinflammation in Alzheimer's disease: Current evidence and future directions. Alzheimers Dement. 2016;12:719-732.
17. De Felice FG, Ferreira ST. Inflammation, defective insulin signaling, and mitochondrial dysfunction as common molecular denominators connecting type 2 diabetes to Alzheimer disease. Diabetes. 2014;63:2262-2272.
18. Wang X, Zheng W, Xie JW, Wang T, Wang SL, Teng WP, Wang ZY. Insulin deficiency exacerbates cerebral amyloidosis and behavioral deficits in an Alzheimer transgenic mouse model. Molecular neurodegeneration. 2010;5:46.
19. Guo C, Zhang S, Li JY, Ding C, Yang ZH, Chai R, Wang X, Wang ZY. Chronic hyperglycemia induced via the heterozygous knockout of Pdx1 worsens neuropathological lesion in an Alzheimer mouse model. Scientific reports. 2016;6:29396.
20. Vassar R, Kovacs DM, Yan R, Wong PC. The betasecretase enzyme BACE in health and Alzheimer's disease: regulation, cell biology, function, and therapeutic potential. J Neurosci. 2009;29:12787-12794.
21. Iqbal K, Liu F, Gong CX, Alonso Adel C, Grundke-Iqbal I. Mechanisms of tau-induced neurodegeneration. Acta Neuropathol. 2009;118:53-69.
22. Bezprozvanny I, Mattson MP. Neuronal calcium mishandling and the pathogenesis of Alzheimer's disease. Trends in neurosciences. 2008;31:454-463.
23. Fonseca AC, Moreira PI, Oliveira CR, Cardoso SM, Pinton P, Pereira CF. Amyloid-beta disrupts calcium and redox homeostasis in brain endothelial cells. Mol Neurobiol. 2015;51:610-622.
24. Oseki KT, Monteforte PT, Pereira GJ, Hirata H, Ureshino RP, Bincoletto C, Hsu YT, Smaili SS. Apoptosis induced by Abeta25-35 peptide is Ca(2+)-IP3 signaling-dependent in murine astrocytes. Eur J Neurosci. 2014;40:2471-2478.
25. Mattson MP. Pathways towards and away from Alzheimer's disease. Nature. 2004;430:631-639.
26. Demuro A, Parker I, Stutzmann GE. Calcium signaling and amyloid toxicity in Alzheimer disease. J Biol Chem. 2010;285:12463-12468.
27. Mattson MP, Engle MG, Rychlik B. Effects of elevated intracellular calcium levels on the cytoskeleton and tau in cultured human cortical neurons. Mol Chem Neuropathol. 1991;15:117-142.
28. Hopp SC, D'Angelo HM, Royer SE, Kaercher RM, Crockett AM, Adzovic L, Wenk GL. Calcium dysregulation via L-type voltage-dependent calcium channels and ryanodine receptors underlies memory deficits and synaptic dysfunction during chronic neuroinflammation. J Neuroinflammation. 2015;12:56.
29. Trinchese F, Fa M, Liu S, Zhang H, Hidalgo A, Schmidt SD, Yamaguchi H, Yoshii N, Mathews PM, Nixon RA, Arancio O. Inhibition of calpains improves memory and synaptic transmission in a mouse model of Alzheimer disease. J Clin Invest. 2008;118:2796-2807.
30. Thibault O, Anderson KL, DeMoll C, Brewer LD, Landfield PW, Porter NM. Hippocampal calcium dysregulation at the nexus of diabetes and brain aging. Eur J Pharmacol. 2013;719:34-43.
31. Biessels GJ, ter Laak MP, Hamers FP, Gispen WH. Neuronal Ca2+ disregulation in diabetes mellitus. Eur J Pharmacol. 2002;447:201-209.
32. O'Day DH, Eshak K, Myre MA. Calmodulin Binding Proteins and Alzheimer's Disease. J Alzheimers Dis. 2015;46:553-569.
33. O'Day DH, Myre MA. Calmodulin-binding domains in Alzheimer's disease proteins: extending the calcium hypothesis. Biochem Biophys Res Commun. 2004;320:1051-1054.
34. Thibault O, Gant JC, Landfield PW. Expansion of the calcium hypothesis of brain aging and Alzheimer's disease: minding the store. Aging Cell. 2007;6:307-317.
35. Popugaeva E, Bezprozvanny I. Can the calcium hypothesis explain synaptic loss in Alzheimer's disease? Neurodegener Dis. 2014;13:139-141.
36. Lee MS, Kwon YT, Li M, Peng J, Friedlander RM, Tsai LH. Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature. 2000;405:360-364.
37. Ghosh A, Giese KP. Calcium/calmodulin-dependent kinase II and Alzheimer's disease. Mol Brain. 2015;8:78.
38. Caccamo A, De Pinto V, Messina A, Branca C, Oddo S. Genetic reduction of mammalian target of rapamycin ameliorates Alzheimer's disease-like cognitive and pathological deficits by restoring hippocampal gene expression signature. J Neurosci. 2014;34:7988-7998.
39. Lee SJ, Escobedo-Lozoya Y, Szatmari EM, Yasuda R. Activation of CaMKII in single dendritic spines during long-term potentiation. Nature. 2009;458:299-304.
40. Markova B, Albers C, Breitenbuecher F, Melo JV, Brummendorf TH, Heidel F, Lipka D, Duyster J, Huber C, Fischer T. Novel pathway in Bcr-Abl signal transduction involves Akt-independent, PLC-gamma1-driven activation of mTOR/p70S6-kinase pathway. Oncogene. 2010;29:739-751.
41. Ma QL, Harris-White ME, Ubeda OJ, Simmons M, Beech W, Lim GP, Teter B, Frautschy SA, Cole GM. Evidence of Abeta-and transgene-dependent defects in ERKCREB signaling in Alzheimer's models. J Neurochem. 2007;103:1594-1607.
42. Palomer E, Martin-Segura A, Baliyan S, Ahmed T, Balschun D, Venero C, Martin MG, Dotti CG. Aging Triggers a Repressive Chromatin State at Bdnf Promoters in Hippocampal Neurons. Cell Rep. 2016;16:2889-2900.
43. Leissring MA, Akbari Y, Fanger CM, Cahalan MD, Mattson MP, LaFerla FM. Capacitative calcium entry deficits and elevated luminal calcium content in mutant presenilin-1 knockin mice. J Cell Biol. 2000;149:793-798.
44. Bordji K, Becerril-Ortega J, Nicole O, Buisson A. Activation of extrasynaptic, but not synaptic, NMDA receptors modifies amyloid precursor protein expression pattern and increases amyloid-ss production. J Neurosci. 2010;30:15927-15942.
45. Magi S, Castaldo P, Macri ML, Maiolino M, Matteucci A, Bastioli G, Gratteri S, Amoroso S, Lariccia V. Intracellular Calcium Dysregulation: Implications for Alzheimer's Disease. Biomed Res Int. 2016;2016:6701324.
46. Alberdi E, Sanchez-Gomez MV, Cavaliere F, Perez-Samartin A, Zugaza JL, Trullas R, Domercq M, Matute C. Amyloid beta oligomers induce Ca2+ dysregulation and neuronal death through activation of ionotropic glutamate receptors. Cell Calcium. 2010;47:264-272.
47. Verkhratsky A, Fernyhough P. Mitochondrial malfunction and Ca2+ dyshomeostasis drive neuronal pathology in diabetes. Cell Calcium. 2008;44:112-122.
48. Gispen WH, Biessels GJ. Cognition and synaptic plasticity in diabetes mellitus. Trends Neurosci. 2000;23:542-549.
49. Ramos-Rodriguez JJ, Ortiz-Barajas O, Gamero-Carrasco C, de la Rosa PR. Prediabetes-induced vascular alterations exacerbate central pathology in APPswe/PS1dE9 mice. Psychoneuroendocrinology. 2014;48:123-135.
50. Papon MA, El Khoury NB, Marcouiller F, Julien C, Morin F, Bretteville A, Petry FR, Gaudreau S, Amrani A, Mathews PM, Hebert SS, Planel E. Deregulation of protein phosphatase 2A and hyperphosphorylation of tau protein following onset of diabetes in NOD mice. Diabetes. 2013;62:609-617.
51. El Khoury NB, Gratuze M, Papon MA, Bretteville A, Planel E. Insulin dysfunction and Tau pathology. Front Cell Neurosci. 2014;8:22.
52. Shah K, Lahiri DK. Cdk5 activity in the brain-multiple paths of regulation. Journal of cell science. 2014;127:2391-2400.
53. Zhou M, Huang T, Collins N, Zhang J, Shen H, Dai X, Xiao N, Wu X, Wei Z, York J, Lin L, Zhu Y, LaDu MJ, Chen X. APOE4 Induces Site-Specific Tau Phosphorylation Through Calpain-CDK5 Signaling Pathway in EFAD-Tg Mice. Current Alzheimer research. 2016;13:1048-1055.
54. Masliah E, Mallory M, Alford M, DeTeresa R, Hansen LA, McKeel DW, Jr, Morris JC. Altered expression of synaptic proteins occurs early during progression of Alzheimer's disease. Neurology. 2001;56:127-129.
55. Pham E, Crews L, Ubhi K, Hansen L, Adame A, Cartier A, Salmon D, Galasko D, Michael S, Savas JN, Yates JR, Glabe C, Masliah E. Progressive accumulation of amyloidbeta oligomers in Alzheimer's disease and in amyloid precursor protein transgenic mice is accompanied by selective alterations in synaptic scaffold proteins. The FEBS journal. 2010;277:3051-3067.
56. Proctor DT, Coulson EJ, Dodd PR. Reduction in postsynaptic scaffolding PSD-95 and SAP-102 protein levels in the Alzheimer inferior temporal cortex is correlated with disease pathology. Journal of Alzheimer's disease: JAD. 2010;21:795-811.
57. Wang CY, Xie JW, Xu Y, Wang T, Cai JH, Wang X, Zhao BL, An L, Wang ZY. Trientine reduces BACE1 activity and mitigates amyloidosis via the AGE/RAGE/NF-kappaB pathway in a transgenic mouse model of Alzheimer's disease. Antioxid Redox Signal. 2013;19:2024-2039.
58. Gong Y, Lippa CF. Review: disruption of the postsynaptic density in Alzheimer's disease and other neurodegenerative dementias. American journal of Alzheimer's disease and other dementias. 2010;25:547-555.
59. De Felice FG, Velasco PT, Lambert MP, Viola K, Fernandez SJ, Ferreira ST, Klein WL. Abeta oligomers induce neuronal oxidative stress through an N-methyl-Daspartate receptor-dependent mechanism that is blocked by the Alzheimer drug memantine. The Journal of biological chemistry. 2007;282:11590-11601.
60. Decker H, Jurgensen S, Adrover MF, Brito-Moreira J, Bomfim TR, Klein WL, Epstein AL, De Felice FG, Jerusalinsky D, Ferreira ST. N-methyl-D-aspartate receptors are required for synaptic targeting of Alzheimer's toxic amyloid-beta peptide oligomers. Journal of neurochemistry. 2010;115:1520-1529.
61. Kim JH, Roberts DS, Hu Y, Lau GC, Brooks-Kayal AR, Farb DH, Russek SJ. Brain-derived neurotrophic factor uses CREB and Egr3 to regulate NMDA receptor levels in cortical neurons. Journal of neurochemistry. 2012;120:210-219.
62. Ferreira IL, Ferreiro E, Schmidt J, Cardoso JM, Pereira CM, Carvalho AL, Oliveira CR, Rego AC. Abeta and NMDAR activation cause mitochondrial dysfunction involving ER calcium release. Neurobiol Aging. 2015;36:680-692.
63. Rosales-Corral S, Tan DX, Manchester L, Reiter RJ. Diabetes and Alzheimer disease, two overlapping pathologies with the same background: oxidative stress. Oxid Med Cell Longev. 2015;2015:985845.
64. Vitek MP, Bhattacharya K, Glendening JM, Stopa E, Vlassara H, Bucala R, Manogue K, Cerami A. Advanced glycation end products contribute to amyloidosis in Alzheimer disease. Proceedings of the National Academy of Sciences of the United States of America. 1994;91:4766-4770.
65. Wells-Knecht KJ, Zyzak DV, Litchfield JE, Thorpe SR, Baynes JW. Mechanism of autoxidative glycosylation: identification of glyoxal and arabinose as intermediates in the autoxidative modification of proteins by glucose. Biochemistry. 1995;34:3702-3709.
66. Yamagishi S, Maeda S, Matsui T, Ueda S, Fukami K, Okuda S. Role of advanced glycation end products (AGEs) and oxidative stress in vascular complications in diabetes. Biochim Biophys Acta. 2012;1820:663-671.
67. Guglielmotto M, Aragno M, Tamagno E, Vercellinatto I, Visentin S, Medana C, Catalano MG, Smith MA, Perry G, Danni O, Boccuzzi G, Tabaton M. AGEs/RAGE complex upregulates BACE1 via NF-kappaB pathway activation. Neurobiology of aging. 2012;33:196 e13-27.
68. Chen Z, Zhong C. Decoding Alzheimer's disease from perturbed cerebral glucose metabolism: implications for diagnostic and therapeutic strategies. Prog Neurobiol. 2013;108:21-43.
69. Verma N, Manna SK. Advanced Glycation End Products (AGE) Potently Induce Autophagy through Activation of RAF Protein Kinase and Nuclear Factor kappaB (NFkappaB). J Biol Chem. 2016;291:1481-1491.
70. Yeh CH, Sturgis L, Haidacher J, Zhang XN, Sherwood SJ, Bjercke RJ, Juhasz O, Crow MT, Tilton RG, Denner L. Requirement for p38 and p44/p42 mitogen-activated protein kinases in RAGE-mediated nuclear factor-kappaB transcriptional activation and cytokine secretion. Diabetes. 2001;50:1495-1504.
71. Apelt J, Schliebs R. Beta-amyloid-induced glial expression of both pro-and anti-inflammatory cytokines in cerebral cortex of aged transgenic Tg2576 mice with Alzheimer plaque pathology. Brain research. 2001;894:21-30.
72. LaFerla FM. Calcium dyshomeostasis and intracellular signalling in Alzheimer's disease. Nature reviews. Neuroscience. 2002;3:862-872.
73. Kahya MC, Naziroglu M, Ovey IS. Modulation of Diabetes-Induced Oxidative Stress, Apoptosis, and Ca2+ Entry Through TRPM2 and TRPV1 Channels in Dorsal Root Ganglion and Hippocampus of Diabetic Rats by Melatonin and Selenium. Molecular neurobiology. 2017; 54: 2345-2360.
74. Guo C, Wang T, Zheng W, Shan ZY, Teng WP, Wang ZY. Intranasal deferoxamine reverses iron-induced memory deficits and inhibits amyloidogenic APP processing in a transgenic mouse model of Alzheimer's disease. Neurobiol Aging. 2013;34:562-575.
75. Yu X, Guan PP, Guo JW, Wang Y, Cao LL, Xu GB, Konstantopoulos K, Wang ZY, Wang P. By suppressing the expression of anterior pharynx-defective-1alpha and-1beta and inhibiting the aggregation of beta-amyloid protein, magnesium ions inhibit the cognitive decline of amyloid precursor protein/presenilin 1 transgenic mice. FASEB J. 2015;29:5044-5058.