Insulin resistance as common molecular denominator linking obesity to Alzheimer’s disease

Current Alzheimer Research

Volumn 12, Issue 8, 2015, Pages 723-735

  Nuzzo, Domenico ^a   Picone, Pasquale ^a   Baldassano, Sara ^b   Caruana, Luca ^a   Messina, Elisa ^a   Gammazza, Antonella Marino ^b,c   Cappello, Francesco ^b,c   Mulè, Flavia ^b   Di Carlo, Marta ^a  

^a CNR   (Italy)

^b UNIVERSITY OF PALERMO   (Italy)

^c Euro Mediterranean Institute of Science and Technology   (Italy)

Author keywords

Adipokines; Alzheimer s disease; Gene expression; Inflammation; Insulin resistance; Mitochondrial dysfunction; Obesity

Indexed keywords

ADIPOCYTOKINE; ADIPONECTIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; BETA SECRETASE; CD3 ANTIGEN; CHAPERONIN 60; CHEMOKINE RECEPTOR CCR3; CHEMOKINE RECEPTOR CCR4; GAMMA INTERFERON; GLYCOGEN SYNTHASE KINASE 3BETA; HEME; INDUCIBLE NITRIC OXIDE SYNTHASE; INSULIN; LEPTIN; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PROTEIN KINASE B; RESISTIN; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR PDX 1; AMYLOID PROTEIN; CYTOKINE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; INSULIN RECEPTOR; SECRETASE;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; BRAIN ATROPHY; BRAIN METABOLISM; BRAIN WEIGHT; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVATION; GENE EXPRESSION; INFLAMMATION; INSULIN RESISTANCE; LIPID DIET; MOUSE; NERVE DEGENERATION; NONHUMAN; OBESITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ADVERSE EFFECTS; ANIMAL; BLOOD; BRAIN; C57BL MOUSE; CASE CONTROL STUDY; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; PATHOLOGY; PHYSIOLOGY; TIME FACTOR;

ALZHEIMER DISEASE; AMYLOID PRECURSOR PROTEIN SECRETASES; AMYLOIDOGENIC PROTEINS; ANIMALS; BRAIN; CASE-CONTROL STUDIES; CYTOKINES; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHASE KINASE 3; INSULIN; INSULIN RESISTANCE; MALE; MICE; MICE, INBRED C57BL; OBESITY; OXIDATIVE STRESS; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 84942100980     PISSN: 15672050     EISSN: 18755828     Source Type: Journal    
DOI: 10.2174/1567205012666150710115506     Document Type: Article

References (67)

1. Selkoe DJ. The genetics and molecular pathology of Alzheimer's disease: roles of amyloid and the presenilins. Neurol Clin 18: 903-922 (2000).
2. Cole SL, Vassar R. The Alzheimer's disease beta-secretase enzyme, BACE1. Mol Neurodegener 2: 1-25 (2007).
3. Alzheimer's Association. Alzheimer's disease facts and figures. Alzheimer's Dement e47-e92 (2014).
4. Gonzalez Jimenez E. Genes and obesity: A cause and effect relationship. Endocrinolog Nutr 58: 492-496 (2011).
5. Hildreth KL, Van Pelt RE, Schwartz RS. Obesity, insulin resistance and Alzheimer's disease. Obesity 20: 1549-57 (2012).
6. Beydoun MA, Beydoun HA, Wang Y. Obesity and central obesity as risk factors for incident dementia and its subtypes: a systematic review and meta-analysis. Obesity Rev 9: 204-218 (2008).
7. Fitzpatrick AL, Kuller LH, Lopez OL, Diehr P, O'Meara ES, Longstreth WJ Jr., et al. Midlife and late-life obesity and the risk of dementia: cardiovascular health study. Arch Neurol 66: 336-342 (2009).
8. Gunstad J, Paul RH, Cohen RA, Tate DF, Spitznagel MB, Grieve S, et al. Relationship between body mass index and brain volume in healthy adults. Int J Neurosci 118: 1582-1593 (2008).
9. Cohen RA. Obesity-associated cognitive decline: excess weight affects more than the waistline. Neuroepidemiology 34: 230-231 (2010).
10. Gunstad J, Lhotsky A, Wendell CR, Ferrucci L, Zonderman AB. Longitudinal examination of obesity and cognitive function: results from the Baltimore longitudinal study of aging. Neuroepidemiology 34: 222-229 (2010).
11. Ott Ott A, Stolk RP, van Harskamp F, Pols HAP, Hofman A, Breteler MMB. Diabetes mellitus and the risk of dementia: the Rotterdam Study. Neurology 53:1937-1942 (1999).
12. Lee YH, Tharp WG, Maple RL, Nair S, Permana PA, Pratley RE. Amyloid precursor protein expression is up-regulated in adipocytes in obesity. Obesity 16: 1493-1500 (2008).
13. Lee YH, Martin JM, Maple RL, Tharp WG, Pratley RE. Plasma amyloid-beta peptide levels correlate with adipocyte amyloid precursor protein gene expression in obese individuals. Neuroendocrinology 90: 383-390 (2009).
14. Kahn BB, Flier JF. Obesity and insulin resistance. J Clin Invest 106: 473-481 (2000).
15. Watson GS, Craft S. Modulation of memory by insulin and glucose: neuropsychological observations in Alzheimer's disease. Eur J Pharmacol 490: 97-113 (2004).
16. Ghasemi R, Haeri A, Dargahi L, Mohamed Z, Ahmadiani A. Insulin in the brain: sources, localization and functions. Mol Neurobiol 47: 145-171 (2013).
17. Steen E, Terry BM, Rivera EJ, Cannon JL, Neely TR, Tavares R et al. 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 (2005).
18. Watson GS, Craft S. The role of insulin resistance in the pathogenesis of Alzheimer's disease: implications for treatment. CNS Drugs 17: 27-45 (2003).
19. Marks DR, Tucker K, Cavallin MA, Mast TG, Fadool DA. Awake intranasal insulin delivery modifies protein complexes and alters memory, anxiety, and olfactory behaviors. J Neurosci 29: 6734-6751 (2009).
20. Craft S, Baker LD, Montine TJ, Minoshima S, Watson GS, Claxton A, et al. Intranasal insulin therapy for Alzheimer disease and amnestic mild cognitive impairment: a pilot clinical trial. Arch Neurol 69: 29-38 (2012).
21. Molteni R, Barnard RJ, Ying Z, Roberts CK, Gomez-Pinilla F. A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience 112: 803-814 (2002).
22. Stranahan AM, Mattson MP. Bidirectional metabolic regulation of neurocognitive function. Neurobiol Learn Mem 96: 507-516 (2011).
23. Heyward FD, Waltonb RG, Carle MS, Coleman MA, Garvey WT, Sweatt JD. Adult mice maintained on a high-fat diet exhibit object location memory deficits and reduced hippocampal SIRT1 gene expression. Neurobiol Learn Mem 98: 25-32 (2012).
24. Valladolid-Acebes I, Stucchi P, Cano V, Fernandez-Alfonso MS, Merino B, Gil-Ortega M, et al. High-fat diets impair spatial learning in the radial-arm maze in mice. Neurobiol Learn Mem 95: 80-85 (2011).
25. Moroz N, Tong M, Longato L, Xu H, de la Monte SM. Limited Alzheimer-type neurodegeneration in experimental obesity and type 2 diabetes mellitus. J Alzheimers Dis 15: 29-44 (2008).
26. Arvanitidis AP, Corbett D, Colbourne F. A high fat diet does not exacerbate CA1 injury and cognitive deficits following global ischemia in rats. Brain Res 1252: 192-200 (2009).
27. Camargo N, Brouwers JF, Loos M, Gutmann DH, Smit AB, Verhijen MH. High-fat diet ameliorates neurological deficits caused by defective astrocyte lipid metabolism. FASEB J 10: 4302-15 (2012).
28. Heyward FD, Walton RG, Carle MS, Coleman MA, Garvey WT, Sweatt JD. Adult mice maintained on a high-fat diet exhibit object location memory deficits and reduced hippocampal SIRT1 gene expression. Neurobiol Learn Mem 98: 25-32 (2012).
29. Ramos-Rodriguez JJ, Molina-Gil S, Ortiz-Barajas O, Jimenez-Palomares M, Perdomo G, Cozar-Castellano I, et al. Central proliferation and neurogenesis is impaired in type 2 diabetes and prediabetes animal models. PLoS One 9(2): e89229 (2014).
30. Baldassano S, Amato A, Cappello F, Rappa F, Mule F. Glucagonlike peptide-2 and mouse intestinal adaptation to a high-fat diet. J Endocrinol 217: 11-20 (2013).
31. Marino Gammazza A, Colangeli R, Orban G, Pierucci M, Di Gennaro G, Bello ML, et al. Hsp60 response in experimental and human temporal lobe epilepsy. Sci Rep 5: 9434 (2015).
32. Eskelinen MH, Ngandu T, Helkala EL, Tuomilehto J, Nissinen A, Soininen H, et al. Fat intake at midlife and cognitive impairment later in life: a population-based CAIDE study. Int J Geriatr Psychiatry 23: 741-747 (2008).
33. Kalmijn S, Launer LJ, Ott A, Witteman JC, Hofman A, Breteler MM. Dietary fat intake and the risk of incident dementia in the Rotterdam Study. Ann Neurol 42: 776-782 (1997).
34. Nickl-Jockschat T, Kleiman A, Schulz JB, Schneider F, Laird AR, Fox PT, et al. Neuroanatomic changes and their association with cognitive decline in mild cognitive impairment: a metaanalysis. Brain Struct Funct 217: 115-25 (2012).
35. Pedrini S, Thomas C, Brautigam H, Schmeidler J, Ho L, Fraser P, et al. Dietary composition modulates brain mass and solubilizable Abeta levels in a mouse model of aggressive Alzheimer's amyloid pathology. Mol Neurodegener 21: 4: 40 (2009).
36. de la Monte SM, Tong M. Brain metabolic dysfunction at the core of Alzheimer's disease. Biochem Pharmacol 88: 548-59 (2014).
37. Ho L, Qin W, Pompl PN, Xiang Z, Wang J, Zhao Z, et al. Dietinduced insulin resistance promotes amyloidosis in a transgenic mouse model of Alzheimer's disease. FASEB J 18: 902-904 (2004).
38. Letra L, Santana I, Seica R. Obesity as a risk factor for Alzheimer's disease: the role of adipocytokines. Metab Brain Dis 29: 563-568 (2014).
39. Puig KL, Floden AM, Adhikari R, Golovko MY, Combs CK. Amyloid precursor protein and proinflammatory changes are regulated in brain and adipose tissue in a murine model of high fat dietinduced obesity. PLoS One 7: e30378 (2012).
40. Baldassano S, Rappa F, Amato A, Cappello F, Mule F. GLP-2 as beneficial factor in the glucose homeostasis in mice fed a high fat diet. J Cell Physiol 230(12): 3029-36 (2015).
41. Zhao WQ, De Felice FG, Fernandez S, Chen H, Lambert H, Quon MJ, et al. Amyloid beta oligomers induce impairment of neuronal insulin receptors. FASEB J 22: 246-260 (2008).
42. De Felice FG, Vieira MNN, Bomfim TR, Decker H, Velasco PT, Lambert MP, et al. Protection of synapses against Alzheimer'slinked toxins: insulin signaling prevents the pathogenic binding of Abeta oligomers. Proc Natl Acad Sci USA 106: 1971-1976 (2009).
43. Picone P, Giacomazza D, Vetri V, Carrotta R, Militello V, San Biagio PL, et al. Insulin-activated Akt rescues Aβ oxidative stressinduced cell death by orchestrating molecular trafficking. Aging Cell 10: 832-43 (2011).
44. Qin W, Zhao W, Ho L, Wang J, Walsh K, Gandy S, et al. Regulation of forkhead transcription factor FoxO3a contributes to calorie restriction-induced prevention of Alzheimer's disease-type amyloid neuropathology and spatial memory deterioration. Ann NY Acad Sci 1147: 335-47 (2008).
45. Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annu Rev Immunol 29: 415-445 (2011).
46. Ferreira ST, Clarke JR, Bomfim TR, De Felice FG. Inflammation, defective insulin signaling, and neuronal dysfunction in Alzheimer's disease. Alzheimers Dement 10: S76-S83 (2014).
47. Takeda S, Sato N, Ikimura K, Nishino H, Rakugi H, Morishita R. Increased blood-brain barrier vulnerability to systemic inflammation in an Alzheimer disease mouse model. Neurobiol Aging 34: 2064-2070 (2013).
48. Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH. Mechanisms underlying inflammation in neurodegeneration. Cell 140: 918-934 (2010).
49. Mastrangelo MA, Sudol KL, Narrow WC, Bowers WJ. Interferon-γ differentially affects Alzheimer's disease pathologies and induces neurogenesis in triple transgenic-AD mice. J Am Pathol 175: 2076-2088 (2009).
50. Kershaw EE, Flier JS. Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 89: 2548-2556 (2004).
51. Wayner MJ, Armstrong DL, Phelix CF, Oomura Y. Orexin-A (Hypocretin-1) and leptin enhance LTP in the dentate gyrus of rats in vivo. Peptides 25: 991-996 (2004).
52. Fewlass DC, Noboa K, Pi-Sunyer FX, Johnston JM, Yan SD, Tezapsidis N. Obesity-related leptin regulates Alzheimer's Abeta. FASEB J 18: 1870-1878 (2004).
53. Greco SJ, Sarkar S, Casadesus G, Zhu X, Smith MA, Ashford JW, et al. Leptin inhibits glycogen synthase kinase-3beta to prevent tau phosphorylation in neuronal cells. Neurosci Lett 455:19-194 (2009).
54. Lieb W, Beiser AS, Vasan RS, Tan ZS, Au R, Harris TB, et al. Association of plasma leptin levels with incident Alzheimer disease and MRI measures of brain aging. JAMA 302: 2565-2572 (2009).
55. Gustafson DR. Adiposity hormones and dementia. J Neurol Sci 299: 30-34 (2010).
56. Erol A. An integrated and unifying hypotesis for the metabolic basis of sporadic Alzheimer's disease. J Alzhemers Dis 13: 241-253 (2008).
57. Teixeira AL, Diniz BS, Campos AC, Miranda AS, Rocha NP, Talib LL, et al. Decreased levels of circulating adiponectin in mild cognitive impairment and Alzheimer's disease. Neuromol Med 15: 115-121 (2013).
58. Liu J, Chi N, Chen H, Zhang J, Bian Y, Cui G, et al. Resistin protection against endogenous Aβ neuronal cytotoxicity from mitochondrial pathway. Brain Res 1523: 77-84 (2013).
59. Brown GC. Nitric oxide and neuronal death. Nitric Oxide 23: 153-165 (2010).
60. Reddy PH. Amyloid beta-induced glycogen synthase kinase 3β phosphorylated VDAC1 in Alzheimer's disease: implications for synaptic dysfunction and neuronal damage. Biochim Biophys Acta 1832: 1913-1921 (2013).
61. Manczak M, Reddy PH. Abnormal interaction of VDAC1 with amyloid beta and phosphorylated tau causes mitochondrial dysfunction in Alzheimer's disease. Hum Mol Genet 21: 5131-5146 (2012).
62. Marino Gammazza A, Rizzo M, Citarrella R, Rappa F, Campanella C, Bucchieri F, et al. Elevated blood Hsp60, its structural similarities and cross-reactivity with thyroid molecules, and its presence on the plasma membrane of oncocytes point to the chaperonin as an immunopathogenic factor in Hashimoto's thyroiditis. Cell Stress Chaperones. 19(3): 343-53 (2014).
63. Cappello F, Marino Gammazza A, Palumbo Piccionello A, Campanella C, Pace A, Conway de Macario E, et al. Hsp60 chaperonopathies and chaperonotherapy: targets and agents. Expert Opin Ther Targets 18(2): 185-208 (2014).
64. Kleinridders A, Lauritzen HPMM, Ussar S, Christensen JH, Mori MA, Bross P, et al. Leptin regulation of Hsp60 impacts hypothalamic insulin signaling. J Clin Invest 123: 4667-4680 (2013).
65. Wang X, Su B, Siedlak SL, Moreira PI, Fujioka H, Wang Y, et al. Amyloid-βoverproduction causes abnormal mitochondrial dynamics via differential modulation of mitochondrial fission/fusion proteins. Proc Natl Acad Sci USA 49: 19318-23 (2008).
66. Wang X, Su B, Lee HG, Li X, Perry G, Smith MA, et al. Impaired balance of mitochondrial fission and fusion in Alzheimer's disease. J Neurosci 29: 9090-9103 (2009).
67. Jheng HF, Tsai PJ, Guo SM, Kuo LH, Chang CS, Su IJ, et al. Mitochondrial fission contributes to mitochondrial dysfunction and insulin resistance in skeletal muscle. Mol Cell Biol 32: 309-19 (2012).