Alzheimer disease and diabetes mellitus: Do they have anything in common?

Current Alzheimer Research

Volumn 10, Issue 6, 2013, Pages 609-617

  Adeghate, Ernest ^a   Donáth, Tibor ^b   Adem, Abdu ^a  

^a UNITED ARAB EMIRATES UNIVERSITY   (United Arab Emirates)

^b SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

Alzheimer disease; Amyloidosis; Angiopathy; Brain structure; Cognitive function; Diabetes mellitus; Hyperglycaemia; Oxidative stress

Indexed keywords

ADVANCED GLYCATION END PRODUCT; GLUCAGON LIKE PEPTIDE 1; INSULIN; LIRAGLUTIDE;

ALZHEIMER DISEASE; AMYLOIDOSIS; ARTICLE; BLOOD BRAIN BARRIER; COGNITIVE DEFECT; DEMENTIA; DIABETES MELLITUS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENVIRONMENTAL FACTOR; GENE; HISTOPATHOLOGY; HUMAN; HYPERGLYCEMIA; INSULIN RESISTANCE; LIPID METABOLISM; LIPID PEROXIDATION; MOLECULAR PATHOLOGY; NON INSULIN DEPENDENT DIABETES MELLITUS; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PATHOGENESIS; PREVALENCE; PRIORITY JOURNAL; VASCULAR DISEASE;

ALZHEIMER DISEASE; DIABETES MELLITUS; HUMANS;

EID: 84882738900     PISSN: 15672050     EISSN: 18755828     Source Type: Journal    
DOI: 10.2174/15672050113109990009     Document Type: Article

References (103)

1. Zimmet P, Alberti KG, Shaw J. Global and societal implications of the diabetes epidemic. Nature 414(6865): 782-787(2001).
2. Musselman DL, Betan E, Larsen H, Phillips LS. Relationship of depression to diabetes types 1 and 2: epidemiology, biology, and treatment. Biol Psychiatry 54: 317-329 (2003).
3. Biessels GJ, van der Heide LP, Kamal A, Bleys RL, Gispen WH. Ageing and diabetes: implications for brain function. Eur J Pharmacol 441(1-2): 1-14 (2002).
4. Reitz C, Brayne C, Mayeux R. Epidemiology of Alzheimer disease. Nat Rev Neurol 7: 137-52 (2011).
5. Logue MW, Schu M, Vardarajan BN, Buros J, Green RC, Go RC, et al. A comprehensive genetic association study of Alzheimer disease in African Americans. Arch Neurol 68: 1569-79 (2011).
6. Nation DA, Hong S, Jak AJ, Delano-Wood L, Mills PJ, Bondi MW, et al. Stress, exercise, and Alzheimer's disease: a neurovascular pathway. Med Hypotheses 76: 847-54 (2011).
7. Coppieters N, Dragunow M. Epigenetics in Alzheimer's disease: a focus on DNA modifications. Curr Pharm Des 17: 3398-412 (2011).
8. Shen ZX. Brain cholinesterases: II. The molecular and cellular basis of Alzheimer's disease. Med Hypotheses 63: 308-321 (2004).
9. Howard R, McShane R, Lindesay J, Ritchie C, Baldwin A, Barber R, et al. Donepezil and memantine for moderate-to-severe Alzheimer's disease. N Engl J Med 366: 893-903 (2012).
10. Hardy J, Allsop D. Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol Sci 12: 383-388 (1991).
11. Mudher A, Lovestone S. Alzheimer's disease-do tauists and baptists finally shake hands? Trends Neurosci 25: 22-26(2002).
12. Nistor M, Don M, Parekh M, Sarsoza F, Goodus M, Lopez GE, et al. Alpha-and beta-secretase activity as a function of age and betaamyloid in Down syndrome and normal brain. Neurobiol Aging 28: 1493-506 (2007).
13. Lott IT, Head E. Alzheimer disease and Down syndrome: factors in pathogenesis. Neurobiol Aging 26: 383-389 (2005).
14. Polvikoski T, Sulkava R, Haltia M, Kainulainen K, Vuorio A, Verkkoniemi A, et al. Apolipoprotein E, dementia, and cortical deposition of beta-amyloid protein. N Engl J Med 333: 1242-1247 (1995).
15. Lacor PN, Buniel MC, Furlow PW, Clemente AS, Velasco PT, Wood M, Viola KL, et al. Abeta oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J Neurosci 27: 796-807 (2007).
16. Nikolaev A, McLaughlin T, O'Leary DD, Tessier-Lavigne M. APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 457: 981-989 (2009).
17. Schmitz C, Rutten BP, Pielen A, Schafer S, Wirths O, Tremp G, et al. Hippocampal neuron loss exceeds amyloid plaque load in a transgenic mouse model of Alzheimer's disease. Am J Pathol 164: 1495-1502 (2004).
18. Iqbal K, Alonso Adel C, Chen S, Chohan MO, El-Akkad E, et al. Tau pathology in Alzheimer disease and other tauopathies. Biochim Biophys Acta 1739: 198-210 (2005).
19. Chun W, Johnson GV. The role of tau phosphorylation and cleavage in neuronal cell death. Front Biosci 12: 733-756 (2007).
20. Clodfelder-Miller BJ, Zmijewska AA, Johnson GV, Jope RS. Tau is hyperphosphorylated at multiple sites in mouse brain in vivo after streptozotocin-induced insulin deficiency. Diabetes 55(12): 3320-3325 (2006).
21. Bartzokis G. Alzheimer's disease as homeostatic responses to agerelated myelin breakdown. Neurobiol Aging 32: 1341-1371 (2009).
22. Heneka MT, Nadrigny F, Regen T, Martinez-Hernandez A, Dumitrescu-Ozimek L, Terwel D, et al. Locus ceruleus controls Alzheimer's disease pathology by modulating microglial functions through norepinephrine. Proc Natl Acad Sci USA 107: 6058-63(2010).
23. Adeghate E, Ponery AS, Sheen R. Streptozotocin-Induced diabetes mellitus is associated with increased pancreatic tissue levels of noradrenaline and adrenaline in the rat. Pancreas 22: 311-316 (2001).
24. Su B, Wang X, Nunomura A, Moreira PI, Lee HG, Perry G, et al. Oxidative stress signaling in Alzheimer's disease. Curr Alzheimer Res 5: 525-532 (2008).
25. Geula C, Wu CK, Saroff D, Lorenzo A, Yuan M, Yankner BA. Aging renders the brain vulnerable to amyloid beta-protein neurotoxicity. Nat Med 4: 827-831 (1998).
26. Ferrer I. Defining Alzheimer as a common age-related neurodegenerative process not inevitably leading to dementia. Prog Neurobiol 97(1): 38-51 (2012).
27. Reid PC, Urano Y, Kodama T, Hamakubo T. Alzheimer's disease: cholesterol, membrane rafts, isoprenoids and statins. J Cell Mol Med 11(3): 383-392 (2007).
28. De Felice FG, Vieira MN, 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: 1971-6 (2009).
29. 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(1): 63-80 (2005).
30. Trevisan R, Vedovato M, Tiengo A. The epidemiology of diabetes mellitus. Nephrol. Dial Transplant 13: 2-5 (1998).
31. Kumar PJ, ML Clark. Diabetes mellitus and other disorders of metabolism. In Clinical Medicine, 4th ed. PJ Kumar & ML Clark, Eds.: 959-1005. Sunders, London. 1999.
32. Virtanen SM, Räsänen L, Aro A, Lindström J, Sippola H, Lounamaa R, Toivanen L, et al. Childhood diabetes in Finland Study Group. Infant feeding in children <7 years of age with newly diagnosed IDDM. Diabetes Care 14: 415-417 (1991).
33. Virtanen SM, Aro A. Dietary factors in the aetiology of diabetes. Ann Med 26: 469-478 (1994).
34. Horwitz MS, Bradley LM, Harbertson J, Krahl T, Lee J, Sarvetnick N. Diabetes induced by Coxsackie virus: initiation by bystander damage and not molecular mimicry. Nat Med 4: 781-785 (1998).
35. Roivainen M, Knip M, Hyöty H, Kulmala P, Hiltunen M, Vähäsalo P, et al. Several different enterovirus serotypes can be associated with prediabetic autoimmune episodes and onset of overt IDDM. Childhood Diabetes in Finland (DiMe) Study Group. J Med Virol 56: 74-78 (1998).
36. Syllaba J. New findings in type I diabetes. Cas Lek Cesk 133: 37-40 (1994).
37. Trabucchi A, Guerra LL, Faccinetti NI, Iacono RF, Poskus E, Valdez SN. Surface plasmon resonance reveals a different pattern of proinsulin autoantibodies concentration and affinity in diabetic patients. PLoS One 7: e33574 (2012).
38. Alves LI, Davini E, Correia MR, Fukui RT, Santos RF, Cunha MR, et al. Autoantibodies and High-Risk HLA Susceptibility Markers in First-Degree Relatives of Brazilian Patients with Type 1 Diabetes Mellitus: A Progression to Disease Based Study. J Clin Immunol 32(4): 778-85 (2012).
39. Hemminki K, Li X, Sundquist J, Sundquist K. Familial association between type 1 diabetes and other autoimmune and related diseases. Diabetologia 52: 1820-1828 (2009).
40. Kinoshita J, Hata S, Yamazaki H, Tajima N. Slowly progressive insulin-dependent diabetes mellitus associated with pernicious anemia. Intern Med 49: 155-9 (2010).
41. Wenzlau JM, Gardner TJ, Frisch LM, Davidson HW, Hutton JC. Development of a novel autoantibody assay for autoimmune gastritis in type 1 diabetic individuals. Diabetes Metab Res Rev 27: 887-890 (2011).
42. Franco LJ. Diabetes in Japanese-Brazilians: influence of the cultural process. Diabetes Res Clin Pract 34: S51-S57 (1996).
43. Garduno-Diaz SD, Khokhar S. Prevalence, risk factors and complications associated with type 2 diabetes in migrant South Asians. Diabetes Metab Res Rev 28: 6-24 (2012).
44. Huang Z, Cabanela V, Howell T. Stress, bottle feeding, and diabetes. Lancet 350: 889 (1997).
45. Zaccardi F, Pitocco D, Martini F, Caputo S, Miele L, Grieco A, et al. A case of esomeprazole-induced transient diabetes and hepatitis: the role of liver inflammation in the pathogenesis of insulin resistance. Acta Diabetol (2012).
46. Lee CC, Sun Y, Huang HW. How Type II Diabetes-Related Islet Amyloid Polypeptide Damages Lipid Bilayers. Biophys J 102: 1059-68 (2012).
47. Musaiger AO, Al-Hazzaa HM. Prevalence and risk factors associated with nutrition-related noncommunicable diseases in the Eastern Mediterranean region. Int J Gen Med 5: 199-217 (2012).
48. Adeghate E, Hameed RS, Ponery AS, Tariq S, Sheen RS, Shaffiullah M, et al. Streptozotocin causes pancreatic beta cell failure via early and sustained biochemical and cellular alterations. Exp Clin Endocrinol Diabetes 118: 699-707 (2010).
49. Al-Salam S, Rashed H, Adeghate E. Diabetes mellitus is associated with an increased expression of resistin in human pancreatic islet cells. Islets 3: 246-249 (2011).
50. de Haan W, van der Flier WM, Koene T, Smits LL, Scheltens P, Stam CJ. Disrupted modular brain dynamics reflect cognitive dysfunction in Alzheimer's disease. Neuroimage 59: 3085-93 (2012).
51. Emerick AJ, Richards MP, Kartje GL, Neafsey EJ, Stubbs EB, Jr. Experimental diabetes attenuates cerebral cortical-evoked forelimb motor responses. Diabetes 54: 2764-2771 (2005).
52. Brands AM, Biessels GJ, de Haan EH, Kappelle LJ, Kessels RP. The effects of type 1 diabetes on cognitive performance: a metaanalysis. Diabetes Care 28: 726-35(2005).
53. Cukierman T, Gerstein HC, Williamson JD. Cognitive decline and dementia in diabetes-systematic overview of prospective observational studies. Diabetologia 48: 2460-2469 (2005).
54. Gold SM, Dziobek I, Sweat V, Tirsi A, Rogers K, Bruehl H, et al. Hippocampal damage and memory impairments as possible early brain complications of type 2 diabetes. Diabetologia 50: 711-719 (2007).
55. Stewart R, Liolitsa D. Type 2 diabetes mellitus, cognitive impairment and dementia. Diabet Med 16: 93-112 (1999).
56. Weinstock M, Shoham S. Rat models of dementia based on reductions in regional glucose metabolism, cerebral blood flow and cytochrome oxidase activity. J Neural Transm 111(3): 347-66 (2004).
57. Planel E, Tatebayashi Y, Miyasaka T, Liu L, Wang L, Herman M, Yu WH, et al. Insulin dysfunction induces in vivo tau hyperphosphorylation through distinct mechanisms. J Neurosci 27(50): 13635-13648 (2007).
58. Schechter R, Beju D, Miller KE. The effect of insulin deficiency on tau and neurofilament in the insulin knockout mouse. Biochem Biophys Res Commun 334(4): 979-986 (2005).
59. S-Roriz-Filho J, Sá-Roriz TM, Rosset I, Camozzato AL, Santos AC, Chaves ML, Moriguti JC, et al. (Pre)diabetes, brain aging, and cognition. Biochim Biophys Acta 1792: 432-443 (2009).
60. Holscher C. Diabetes as a risk factor for Alzheimer's disease: insulin signalling impairment in the brain as an alternative model of Alzheimer's disease. Biochem Soc Trans 39: 891-897 (2011).
61. Ferguson SC, Blane A, Wardlaw J, Frier BM, Perros P, McCrimmon RJ, et al. Influence of an early-onset age of type 1 diabetes on cerebral structure and cognitive function, Diabetes Care 28: 1431-1437 (2005).
62. Revsin Y, Saravia F, Roig P, Lima A, de Kloet ER, Homo-Delarche F, et al. Neuronal and astroglial alterations in the hippocampus of a mouse model for type 1 diabetes. Brain Res 1038(1): 22-31 (2005).
63. Ho MS, Weller NJ, Ives FJ, Carne CL, Murray K, Vanden Driesen RI, et al. Prevalence of Structural Central Nervous System Abnormalities in Early-Onset Type 1 Diabetes Mellitus. J Pediatrics 153: 385-390 (2008).
64. Li L, Holscher C. Common pathological processes in Alzheimer disease and type 2 diabetes: a review. Brain Res Rev 56: 384-402 (2007).
65. Liu Y, Liu F, Iqbal K, Grundke-Iqbal I, Gong CX. Decreased glucose transporters correlate to abnormal hyperphosphorylation of tau in Alzheimer disease. FEBS Lett 582: 359-364 (2008).
66. Adeghate E. Molecular and cellular basis of the aetiology and management of diabetic cardiomyopathy: a short review. Mol Cell Biochem 261: 187-191 (2004).
67. Aragno M, Mastrocola R, Brignardello E, Catalano M, Robino G, Manti R, et al. Dehydroepiandrosterone modulates nuclear factorkappaB activation in hippocampus of diabetic rats. Endocrinology 143: 3250-3258 (2002).
68. Sasaki N, Fukatsu R, Tsuzuki K, Hayashi Y, Yoshida T, Fujii N, et al. Advanced glycation end products in Alzheimer's disease and other neurodegenerative diseases. Am J Pathol 153: 1149-1155 (1998).
69. Moreira PI, Rolo AP, Sena C, Seiça R, Oliveira CR, Santos MS. Insulin attenuates diabetes-related mitochondrial alterations: a comparative study. Med Chem 2(3): 299-308 (2006).
70. Moreira PI, Santos MS, Sena C, Seiça R, Oliveira CR. Insulin protects against amyloid beta-peptide toxicity in brain mitochondria of diabetic rats. Neurobiol Dis 18(3): 628-637 (2005).
71. Cassano T, Serviddio G, Gaetani S, Romano A, Dipasquale P, Cianci S, et al. Glutamatergic alterations and mitochondrial impairment in a murine model of Alzheimer disease. Neurobiol Aging 33(6): 1121.e1-12 (2012).
72. Sheng B, Wang X, Su B, Lee HG, Casadesus G, Perry G, et al. Impaired mitochondrial biogenesis contributes to mitochondrial dysfunction in Alzheimer's disease. J Neurochem 120: 419-429 (2012).
73. Lester-Coll N, Rivera EJ, Soscia SJ, Doiron K, Wands JR, de la Monte SM. Intracerebral streptozotocin model of type 3 diabetes: relevance to sporadic Alzheimer's disease. J Alzheimers Dis 9: 13-33 (2006).
74. Summers WK. Alzheimer's disease, oxidative injury, and cytokines. J Alzheimers Dis (6): 651-657 (2004).
75. Baydas G, Reiter RJ, Yasar A, Tuzcu M, Akdemir I, Nedzvetskii VS. Melatonin reduces glial reactivity in the hippocampus, cortex, and cerebellum of streptozotocin-induced diabetic rats. Free Radic Biol Med 35(7): 797-804 (2003).
76. Hong JH, Kim MJ, Park MR, Kwag OG, Lee IS, Byun BH, et al. Effects of vitamin E on oxidative stress and membrane fluidity in brain of streptozotocin-induced diabetic rats. Clin Chim Acta 340(1-2): 107-115 (2004).
77. van Campenhout A, van Campenhout CM, Lagrou AR, Manuel-y-Keenoy B. Transferrin modifications and lipid peroxidation: implications in diabetes mellitus. Free Radic Res 37(10):1069-1077 (2003).
78. Raza H, Prabu SK, Robin MA, Avadhani NG. Elevated mitochondrial cytochrome P450 2E1 and glutathione S-transferase A4-4 in streptozotocin-induced diabetic rats: tissue-specific variations and roles in oxidative stress. Diabetes 53(1): 185-194 (2004).
79. Aliciguzel Y, Ozen I, Aslan M, Karayalcin U. Activities of xanthine oxidoreductase and antioxidant enzymes in different tissues of diabetic rats. J Lab Clin Med 142(3): 172-177 (2003).
80. Tsakanova GV, Ayvazyan VA, Boyajyan AS, Arakelova EA, Grigoryan GS, Guevorkyan AA, et al. A comparative study of antioxidant system and intensity of lipid peroxidation in type 2 diabetes mellitus and ischemic stroke aggravated and not aggravated by type 2 diabetes mellitus. Bull Exp Biol Med 151: 564-6 (2011).
81. Reagan LP, Magariños AM, Yee DK, Swzeda LI, Van Bueren A, McCall AL, et al. Oxidative stress and HNE conjugation of GLUT3 are increased in the hippocampus of diabetic rats subjected to stress. Brain Res 862(1-2): 292-300 (2000).
82. Tapsell LC, Gillen LJ, Patch CS. Walnuts and dietary approaches to the prevention and management of abnormal lipid profiles in Type 2 diabetes mellitus. Future Cardiol 1: 809-814 (2005).
83. Marcovecchio ML, Dalton RN, Prevost AT, Acerini CL, Barrett TG, Cooper JD, et al. Prevalence of abnormal lipid profiles and the relationship with the development of microalbuminuria in adolescents with type 1 diabetes. Diabetes Care 32: 658-63 (2009).
84. Matsuzaki T, Sasaki K, Hata J, Hirakawa Y, Fujimi K, Ninomiya T, et al. Association of Alzheimer disease pathology with abnormal lipid metabolism: the Hisayama Study. Neurology 77: 1068-1075 (2011).
85. Luchsinger JA, Mayeux R. Cardiovascular risk factors and Alzheimer's disease. Curr Atheroscler Rep 6: 261-266 (2004).
86. Cade WT. Diabetes-related microvascular and macrovascular diseases in the physical therapy setting. Phys Ther 88(11): 1322-1335 (2008).
87. Last D, Alsop DC, Abduljalil AM, Marquis RP, de Bazelaire C, Hu K, et al. Global and regional effects of type 2 diabetes on brain tissue volumes and cerebral vasoreactivity. Diabetes Care 30: 1193-1199 (2007).
88. Ryan CM, Geckle MO, Orchard TJ. Cognitive efficiency declines over time in adults with Type 1 diabetes: effects of micro-and macrovascular complications. Diabetologia 46(7): 940-948 (2003)
89. Westermark GT, Davalli AM, Secchi A, Folli F, Kin T, Toso C, et al. Further evidence for amyloid deposition in clinical pancreatic islet grafts. Transplantation 93: 219-23 (2012).
90. Gotz J, Ittner LM, Lim YA. Common features between diabetes mellitus and Alzheimer's disease. Cell Mol Life Sci 66: 1321-1325 (2009).
91. Grossman H. Does diabetes protect or provoke Alzheimer's disease? Insights into the pathobiology and future treatment of Alzheimer's disease. CNS Spectr 8: 815-23 (2003).
92. Poungvarin N, Lee JK, Yechoor VK, Li MV, Assavapokee T, Suksaranjit P, et al. Carbohydrate response element-binding protein (ChREBP) plays a pivotal role in beta cell glucotoxicity. Diabetologia 55(6): 1783-96 (2012).
93. Li ZG, Zhang W, Sima AA. The role of impaired insulin/IGF action in primary diabetic encephalopathy. Brain Res 1037(1-2): 12-24 (2005).
94. Piotrowski P, Wierzbicka K, Smiałek M. Neuronal death in the rat hippocampus in experimental diabetes and cerebral ischaemia treated with antioxidants. Folia Neuropathol 39(3): 147-54 (2001).
95. Okouchi M, Okayama N, Alexander JS, Aw TY. NRF2-dependent glutamate-L-cysteine ligase catalytic subunit expression mediates insulin protection against hyperglycemia-induced brain endothelial cell apoptosis. Curr Neurovasc Res 3(4): 249-261 (2006).
96. Hawkins BT, Lundeen TF, Norwood KM, Brooks HL, Egleton RD. Increased blood-brain barrier permeability and altered tight junctions in experimental diabetes in the rat: contribution of hyperglycaemia and matrix metalloproteinases. Diabetologia 50(1): 202-211 (2007).
97. Adeghate E, Schattner P, Dunn E. An Update on the Etiology and Epidemiology of Diabetes Mellitus. Ann NY Acad Sci 1084: 1-29 (2006).
98. Muller D, Jones PM, Persaud SJ. Autocrine anti-apoptotic and proliferative effects of insulin in pancreatic beta-cells. FEBS Lett 580: 6977-80 (2006).
99. Duarte AI, Santos MS, Seica R, Oliveira CR. Oxidative stress affects synaptosomal gamma-aminobutyric acid and glutamate transport in diabetic rats: the role of insulin. Diabetes 53: 2110-6 (2004).
100. Lotfy M, Singh J, Kalász H, Tekes K, Adeghate E. Medicinal Chemistry and Applications of Incretins and DPP-4 Inhibitors in the Treatment of Type 2 Diabetes Mellitus. Open Med Chem J 5: 82-92 (2011).
101. Perry T, Lahiri DK, Sambamurti K, Chen D, Mattson MP, Egan JM, et al. Glucagon-like peptide-1 decreases endogenous amyloidbeta peptide (Abeta) levels and protects hippocampal neurons from death induced by Abeta and iron. J Neurosci Res 72(5): 603-612 (2003).
102. McClean PL, Parthsarathy V, Faivre E, Holscher C. The diabetes drug liraglutide prevents degenerative processes in a mouse model of Alzheimer's disease. J Neurosci 31: 6587-94 (2011).
103. Saadi H, Carruthers SG, Nagelkerke N, Al-Maskari F, Afandi B, Reed R, et al. Prevalence of diabetes mellitus and its complications in a population-based sample in Al Ain, United Arab Emirates. Diabetes Res Clin Pract 78: 369-77 (2007).