Type 3 diabetes is sporadic Alzheimer-s disease: Mini-review

European Neuropsychopharmacology

Volumn 24, Issue 12, 2014, Pages 1954-1960

  De la Monte, Suzanne M ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Alzheimer s; Diabetes; Glucose Metabolism; Insulin resistance; Nitrosamines

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; INSULIN; NITRIC ACID DERIVATIVE; NITRITE; NITROSAMINE; SOMATOMEDIN; TAU PROTEIN; GLUCOSE;

ALZHEIMER DISEASE; ARTICLE; BRAIN METABOLISM; DIABETES MELLITUS; GLUCOSE BRAIN LEVEL; HUMAN; NERVE DEGENERATION; NEUROTOXICITY; OXIDATIVE STRESS; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TYPE 3 DIABETES; ANIMAL; BRAIN; COMPLICATION; INSULIN RESISTANCE; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOLOGY; TAUOPATHY;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BRAIN; DIABETES MELLITUS, TYPE 2; GLUCOSE; HUMANS; INSULIN; INSULIN RESISTANCE; NERVE DEGENERATION; NITROSAMINES; OXIDATIVE STRESS; SOMATOMEDINS; TAUOPATHIES;

EID: 84919380771     PISSN: 0924977X     EISSN: 18737862     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2014.06.008     Document Type: Article

References (90)

1. Arnaud L., Robakis N.K., Figueiredo-Pereira M.E. It may take inflammation, phosphorylation and ubiquitination to 'tangle' in Alzheimer-s disease. Neurodegener. Dis. 2006, 3:313-319.
2. Baker L.D., Cross D.J., Minoshima S., Belongia D., Watson G.S., 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(1):51-57.
3. Benedict C., Hallschmid M., Hatke A., Schultes B., Fehm H.L., Born J., Kern W. Intranasal insulin improves memory in humans. Psychoneuroendocrinology 2004, 29:1326-1334.
4. Bhat R., Xue Y., Berg S., Hellberg S., Ormo M., Nilsson Y., Radesater A.C., Jerning E., Markgren P.O., Borgegard T., Nylof M., Gimenez-Cassina A., Hernandez F., Lucas J.J., Diaz-Nido J., Avila J. Structural insights and biological effects of glycogen synthase kinase 3-specific inhibitor AR-A014418. J. Biol. Chem. 2003, 278:45937-45945.
5. Broughton S.K., Chen H., Riddle A., Kuhn S.E., Nagalla S., Roberts C.T., Back S.A. Large-scale generation of highly enriched neural stem-cell-derived oligodendroglial cultures: maturation-dependent differences in insulin-like growth factor-mediated signal transduction. J. Neurochem. 2007, 100:628-638.
6. Cadigan K.M., Liu Y.I. Wnt signaling: complexity at the surface. J. Cell Sci. 2006, 119:395-402.
7. Caselli R.J., Chen K., Lee W., Alexander G.E., Reiman E.M. Correlating cerebral hypometabolism with future memory decline in subsequent converters to amnestic pre-mild cognitive impairment. Arch. Neurol. 2008, 65:1231-1236.
8. Chesik D., De Keyser J., Wilczak N. Insulin-like growth factor system regulates oligodendroglial cell behavior: therapeutic potential in CNS. J. Mol. Neurosci. 2008, 35:81-90.
9. Contestabile A., Greco B., Ghezzi D., Tucci V., Benfenati F., Gasparini L. Lithium rescues synaptic plasticity and memory in Down syndrome mice. J. Clin. Investig. 2013, 123:348-361.
10. Craft S. Insulin resistance and cognitive impairment: a view through the prism of epidemiology. Arch. Neurol. 2005, 62:1043-1044.
11. Craft S. Insulin resistance syndrome and Alzheimer-s disease: age- and obesity-related effects on memory, amyloid, and inflammation. Neurobiol. Aging 2005, 26(Suppl 1):S65-S69.
12. Craft S. Insulin resistance syndrome and Alzheimer disease: pathophysiologic mechanisms and therapeutic implications. Alzheimer Dis. Assoc. Disord. 2006, 20:298-301.
13. Craft S. Insulin resistance and Alzheimer-s disease pathogenesis: potential mechanisms and implications for treatment. Curr. Alzheimer Res. 2007, 4:147-152.
14. Craft S., Asthana S., Cook D.G., Baker L.D., Cherrier M., Purganan K., Wait C., Petrova A., Latendresse S., Watson G.S., Newcomer J.W., Schellenberg G.D., Krohn A.J. Insulin dose-response effects on memory and plasma amyloid precursor protein in Alzheimer-s disease: interactions with apolipoprotein E genotype. Psychoneuroendocrinology 2003, 28:809-822.
15. Cummings J.L. Definitions and Diagnostic Criteria 2007, Informa UK Limited, London. Third ed.
16. De Ferrari G.V., Inestrosa N.C. Wnt signaling function in Alzheimer-s disease. Brain Res. Brain Res. Rev. 2000, 33:1-12.
17. de la Monte S.M. Contributions of brain insulin resistance and deficiency in amyloid-related neurodegeneration in Alzheimer-s disease. Drugs 2011, 72:1-18.
18. de la Monte S.M. Triangulated mal-signaling in Alzheimer-s disease: roles of neurotoxic ceramides, ER stress, and insulin resistance reviewed. J. Alzheimers Dis. 2012, 30(Suppl. 2):S231-S249.
19. de la Monte S.M., Chen G.J., Rivera E., Wands J.R. Neuronal thread protein regulation and interaction with microtubule-associated proteins in SH-Sy5y neuronal cells. Cell. Mol. Life Sci. 2003, 60:2679-2691.
20. de la Monte S.M., Ganju N., Banerjee K., Brown N.V., Luong T., Wands J.R. Partial rescue of ethanol-induced neuronal apoptosis by growth factor activation of phosphoinositol-3-kinase. Alcohol. Clin. Exp. Res. 2000, 24:716-726.
21. de la Monte S.M., Longato L., Tong M., Wands J.R. Insulin resistance and neurodegeneration: roles of obesity, type 2 diabetes mellitus and non-alcoholic steatohepatitis. Curr. Opin. Investig. Drugs 2009, 10:1049-1060.
22. de la Monte S.M., Neely T.R., Cannon J., Wands J.R. Ethanol impairs insulin-stimulated mitochondrial function in cerebellar granule neurons. Cell. Mol. Life Sci. 2001, 58:1950-1960.
23. de la Monte S.M., Neusner A., Chu J., Lawton M. Epidemiological trends strongly suggest exposures as etiologic agents in the pathogenesis of sporadic Alzheimer-s disease, diabetes mellitus, and non-alcoholic steatohepatitis. J. Alzheimers Dis. 2009, 17:519-529.
24. de la Monte S.M., Re E., Longato L., Tong M. Dysfunctional pro-ceramide, ER stress, and insulin/IGF signaling networks with progression of Alzheimer-s disease. J. Alzheimers Dis. 2012, 30(Suppl. 2):S217-S229.
25. de la Monte S.M., Tong M. Mechanisms of nitrosamine-mediated neurodegeneration: potential relevance to sporadic Alzheimer-s disease. J. Alzheimers Dis. 2009, 17(4):817-825.
26. de la Monte S.M., Tong M., Bowling N., Moskal P. si-RNA inhibition of brain insulin or insulin-like growth factor receptors causes developmental cerebellar abnormalities: relevance to fetal alcohol spectrum disorder. Mol. Brain 2011, 4:13.
27. de la Monte S.M., Tong M., Lawton M., Longato L. Nitrosamine exposure exacerbates high fat diet-mediated type 2 diabetes mellitus, non-alcoholic steatohepatitis, and neurodegeneration with cognitive impairment. Mol. Neurodegener. 2009, 4:54.
28. de la Monte S.M., Tong M., Lester-Coll N., Plater M., Wands J.R. Therapeutic rescue of neurodegeneration in experimental type 3 diabetes: relevance to Alzheimer-s disease. J. Alzheimers Dis. 2006, 10:89-109.
29. de la Monte S.M., Wands J.R. Chronic gestational exposure to ethanol impairs insulin-stimulated survival and mitochondrial function in cerebellar neurons. Cell. Mol. Life Sci. 2002, 59:882-893.
30. de la Monte S.M., Wands J.R. Review of insulin and insulin-like growth factor expression, signaling, and malfunction in the central nervous system: relevance to Alzheimer-s disease. J. Alzheimers Dis. 2005, 7:45-61.
31. de la Monte S.M., Wands J.R. Molecular indices of oxidative stress and mitochondrial dysfunction occur early and often progress with severity of Alzheimer-s disease. J. Alzheimers Dis. 2006, 9:167-181.
32. Doble B.W., Woodgett J.R. GSK-3: tricks of the trade for a multi-tasking kinase. J. Cell Sci. 2003, 116:1175-1186.
33. Duyckaerts C., Delatour B., Potier M.C. Classification and basic pathology of Alzheimer disease. Acta Neuropathol. 2009, 118:5-36.
34. Foltz D.R., Santiago M.C., Berechid B.E., Nye J.S. Glycogen synthase kinase-3beta modulates notch signaling and stability. Curr. Biol. 2002, 12:1006-1011.
35. Fraser P.E., Yu G., Levesque L., Nishimura M., Yang D.S., Mount H.T., Westaway D., George-Hyslop P.H. Presenilin function: connections to Alzheimer-s disease and signal transduction. Biochem. Soc. Symp. 2001, 67:89-100.
36. Freude S., Schilbach K., Schubert M. The role of IGF-1 receptor and insulin receptor signaling for the pathogenesis of Alzheimer-s disease: from model organisms to human disease. Curr. Alzheimer Res. 2009, 6:213-223.
37. Frolich L., Blum-Degen D., Bernstein H.G., Engelsberger S., Humrich J., Laufer S., Muschner D., Thalheimer A., Turk A., Hoyer S., Zochling R., Boissl K.W., Jellinger K., Riederer P. Brain insulin and insulin receptors in aging and sporadic Alzheimer-s disease. J. Neural Transm. 1998, 105:423-438.
38. Gasparini L., Gouras G.K., Wang R., Gross R.S., Beal M.F., Greengard P., Xu H. Stimulation of beta-amyloid precursor protein trafficking by insulin reduces intraneuronal beta-amyloid and requires mitogen-activated protein kinase signaling. J. Neurosci. 2001, 21:2561-2570.
39. Gasparini L., Netzer W.J., Greengard P., Xu H. Does insulin dysfunction play a role in Alzheimer-s disease?. Trends Pharmacol. Sci. 2002, 23:288-293.
40. Gong X., Xie Z., Zuo H. Invivo insulin deficiency as a potential etiology for demyelinating disease. Med. Hypotheses 2008, 71:399-403.
41. Gonzalez-Sanchez J.L., Serrano-Rios M. Molecular basis of insulin action. Drug News Perspect. 2007, 20:527-531.
42. Grilli M., Ferrari Toninelli G., Uberti D., Spano P., Memo M. Alzheimer-s disease linking neurodegeneration with neurodevelopment. Funct. Neurol. 2003, 18:145-148.
43. Grunblatt E., Salkovic-Petrisic M., Osmanovic J., Riederer P., Hoyer S. Brain insulin system dysfunction in streptozotocin intracerebroventricularly treated rats generates hyperphosphorylated tau protein. J. Neurochem. 2007, 101:757-770.
44. Gustaw-Rothenberg K., Lerner A., Bonda D.J., Lee H.G., Zhu X., Perry G., Smith M.A. Biomarkers in Alzheimer-s disease: past, present and future. Biomark. Med. 2010, 4:15-26.
45. Hoyer S. The brain insulin signal transduction system and sporadic (type II) Alzheimer disease: an update. J. Neural Transm. 2002, 109:341-360.
46. Hoyer S. Causes and consequences of disturbances of cerebral glucose metabolism in sporadic Alzheimer disease: therapeutic implications. Adv. Exp. Med. Biol. 2004, 541:135-152.
47. Hoyer S. Glucose metabolism and insulin receptor signal transduction in Alzheimer disease. Eur. J. Pharmacol. 2004, 490:115-125.
48. Hoyer S., Lannert H. Inhibition of the neuronal insulin receptor causes Alzheimer-like disturbances in oxidative/energy brain metabolism and in behavior in adult rats. Ann. N. Y. Acad. Sci. 1999, 893:301-303.
49. Hoyer S., Lannert H., Noldner M., Chatterjee S.S. Damaged neuronal energy metabolism and behavior are improved by Ginkgo biloba extract (EGb 761). J. Neural Transm. 1999, 106:1171-1188.
50. Hoyer S., Lee S.K., Loffler T., Schliebs R. Inhibition of the neuronal insulin receptor. An in vivo model for sporadic Alzheimer disease?. Ann. N. Y. Acad. Sci. 2000, 920:256-258.
51. Hoyer S., Nitsch R., Oesterreich K. Predominant abnormality in cerebral glucose utilization in late-onset dementia of the Alzheimer type: a cross-sectional comparison against advanced late-onset and incipient early-onset cases. J. Neural. Transm. Park. Dis. Dement. Sect. 1991, 3:1-14.
52. Iqbal K., Liu F., Gong C.X., Alonso Adel C., Grundke-Iqbal I. Mechanisms of tau-induced neurodegeneration. Acta Neuropathol. 2009, 118:53-69.
53. Iwangoff P., Armbruster R., Enz A., Meier-Ruge W. Glycolytic enzymes from human autoptic brain cortex: normal aged and demented cases. Mech. Ageing Dev. 1980, 14:203-209.
54. Krikorian R., Eliassen J.C., Boespflug E.L., Nash T.A., Shidler M.D. Improved cognitive-cerebral function in older adults with chromium supplementation. Nutr. Neurosci. 2010, 13:116-122.
55. Labak M., Foniok T., Kirk D., Rushforth D., Tomanek B., Jasinski A., Grieb P. Metabolic changes in rat brain following intracerebroventricular injections of streptozotocin: a model of sporadic Alzheimer-s disease. Acta Neurochir. Suppl. 2010, 106:177-181.
56. Langbaum J.B., Chen K., Caselli R.J., Lee W., Reschke C., Bandy D., Alexander G.E., Burns C.M., Kaszniak A.W., Reeder S.A., Corneveaux J.J., Allen A.N., Pruzin J., Huentelman M.J., Fleisher A.S., Reiman E.M. Hypometabolism in Alzheimer-affected brain regions in cognitively healthy Latino individuals carrying the apolipoprotein E epsilon4 allele. Arch. Neurol. 2010, 67:462-468.
57. Lannert H., Hoyer S. Intracerebroventricular administration of streptozotocin causes long-term diminutions in learning and memory abilities and in cerebral energy metabolism in adult rats. Behav. Neurosci. 1998, 112:1199-1208.
58. Lester-Coll N., Rivera E.J., Soscia S.J., Doiron K., Wands J.R., de la Monte S.M. Intracerebral streptozotocin model of type 3 diabetes: relevance to sporadic Alzheimer-s disease. J. Alzheimers Dis. 2006, 9:13-33.
59. Liang G., Cline G.W., Macica C.M. IGF-1 stimulates de novo fatty acid biosynthesis by Schwann cells during myelination. Glia 2007, 55:632-641.
60. Ling X., Martins R.N., Racchi M., Craft S., Helmerhorst E. Amyloid beta antagonizes insulin promoted secretion of the amyloid beta protein precursor. J. Alzheimers Dis. 2002, 4:369-374.
61. Luchsinger J.A. Type 2 diabetes, related conditions, in relation and dementia: an opportunity for prevention?. J. Alzheimers Dis. 2010, 20:723-736.
62. Mandelkow E.M., Stamer K., Vogel R., Thies E., Mandelkow E. Clogging of axons by tau, inhibition of axonal traffic and starvation of synapses. Neurobiol. Aging 2003, 24:1079-1085.
63. Messier C., Teutenberg K. The role of insulin, insulin growth factor, and insulin-degrading enzyme in brain aging and Alzheimer-s disease. Neural Plast. 2005, 12:311-328.
64. Mosconi L., Mistur R., Switalski R., Tsui W.H., Glodzik L., Li Y., Pirraglia E., De Santi S., Reisberg B., Wisniewski T., de Leon M.J. FDG-PET changes in brain glucose metabolism from normal cognition to pathologically verified Alzheimer-s disease. Eur. J. Nucl. Med. Mol. Imaging 2009, 36:811-822.
65. Mosconi L., Pupi A., De Leon M.J. Brain glucose hypometabolism and oxidative stress in preclinical Alzheimer-s disease. Ann. N. Y. Acad. Sci. 2008, 1147:180-195.
66. Mudher A., Chapman S., Richardson J., Asuni A., Gibb G., Pollard C., Killick R., Iqbal T., Raymond L., Varndell I., Sheppard P., Makoff A., Gower E., Soden P.E., Lewis P., Murphy M., Golde T.E., Rupniak H.T., Anderton B.H., Lovestone S. Dishevelled regulates the metabolism of amyloid precursor protein via protein kinase C/mitogen-activated protein kinase and c-Jun terminal kinase. J. Neurosci. 2001, 21:4987-4995.
67. Neumann K.F., Rojo L., Navarrete L.P., Farias G., Reyes P., Maccioni R.B. Insulin resistance and Alzheimer-s disease: molecular links & clinical implications. Curr. Alzheimer Res. 2008, 5:438-447.
68. Nishimura M., Yu G., Levesque G., Zhang D.M., Ruel L., Chen F., Milman P., Holmes E., Liang Y., Kawarai T., Jo E., Supala A., Rogaeva E., Xu D.M., Janus C., Levesque L., Bi Q., Duthie M., Rozmahel R., Mattila K., Lannfelt L., Westaway D., Mount H.T., Woodgett J., George-Hyslop P., et al. Presenilin mutations associated with Alzheimer disease cause defective intracellular trafficking of beta-catenin, a component of the presenilin protein complex. Nat. Med. 1999, 5:164-169.
69. Oddo S. The ubiquitin-proteasome system in Alzheimer-s disease. J. Cell. Mol. Med. 2008, 12:363-373.
70. Reger M.A., Watson G.S., Frey W.H., Baker L.D., Cholerton B., Keeling M.L., Belongia D.A., Fishel M.A., Plymate S.R., Schellenberg G.D., Cherrier M.M., Craft S. Effects of intranasal insulin on cognition in memory-impaired older adults: modulation by APOE genotype. Neurobiol. Aging 2006, 27:451-458.
71. Reger M.A., Watson G.S., Green P.S., Wilkinson C.W., Baker L.D., Cholerton B., Fishel M.A., Plymate S.R., Breitner J.C., Degroodt W., Mehta P., Craft S. Intranasal insulin improves cognition and modulates {beta}-amyloid in early AD. Neurology 2008, 70:440-448.
72. Rivera E.J., Goldin A., Fulmer N., Tavares R., Wands J.R., de la Monte S.M. Insulin and insulin-like growth factor expression and function deteriorate with progression of Alzheimer-s disease: link to brain reductions in acetylcholine. J. Alzheimers Dis. 2005, 8:247-268.
73. Schubert M., Brazil D.P., Burks D.J., Kushner J.A., Ye J., Flint C.L., Farhang-Fallah J., Dikkes P., Warot X.M., Rio C., Corfas G., White M.F. Insulin receptor substrate-2 deficiency impairs brain growth and promotes tau phosphorylation. J. Neurosci. 2003, 23:7084-7092.
74. Schubert M., Gautam D., Surjo D., Ueki K., Baudler S., Schubert D., Kondo T., Alber J., Galldiks N., Kustermann E., Arndt S., Jacobs A.H., Krone W., Kahn C.R., Bruning J.C. Role for neuronal insulin resistance in neurodegenerative diseases. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:3100-3105.
75. Steen E., Terry B.M., Rivera E.J., Cannon J.L., Neely T.R., Tavares R., Xu X.J., Wands J.R., de la Monte S.M. 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.
76. Tabatadze N., Tomas C., McGonigal R., Lin B., Schook A., Routtenberg A. Wnt transmembrane signaling and long-term spatial memory. Hippocampus 2012, 22:1228-1241.
77. Takashima A. Amyloid-beta, tau, and dementia. J. Alzheimers Dis. 2009, 17:729-736.
78. Takashima A. Drug development for tauopathy and Alzheimer-s disease. Nihon Shinkei Seishin Yakurigaku Zasshi 2010, 30:177-180.
79. 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., Arnold S.E. Demonstrated brain insulin resistance in Alzheimer-s disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J. Clin. Investig. 2012, 122:1316-1338.
80. Tong M., Longato L., de la Monte S.M. Early limited nitrosamine exposures exacerbate high fat diet-mediated type 2 diabetes and neurodegeneration. BMC Endocr. Disord. 2010, 10:4.
81. Tong M., Neusner A., Longato L., Lawton M., Wands J.R., de la Monte S.M. Nitrosamine exposure causes insulin resistance diseases: relevance to type 2 diabetes mellitus, non-alcoholic steatohepatitis, and Alzheimer-s disease. J. Alzheimers Dis. 2009, 17(4):827-844.
82. Varela-Nallar L., Inestrosa N.C. Wnt signaling in the regulation of adult hippocampal neurogenesis. Front. Cell. Neurosci. 2013, 7:100.
83. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., Selkoe D.J. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002, 416:535-539.
84. Watson G.S., Craft S. Insulin resistance, inflammation, and cognition in Alzheimer-s Disease: lessons for multiple sclerosis. J. Neurol. Sci. 2006, 245:21-33.
85. Watson G.S., Peskind E.R., Asthana S., Purganan K., Wait C., Chapman D., Schwartz M.W., Plymate S., Craft S. Insulin increases CSF Abeta42 levels in normal older adults. Neurology 2003, 60:1899-1903.
86. 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. 2004, 111:347-366.
87. Winocur G., Greenwood C.E., Piroli G.G., Grillo C.A., Reznikov L.R., Reagan L.P., McEwen B.S. Memory impairment in obese Zucker rats: an investigation of cognitive function in an animal model of insulin resistance and obesity. Behav. Neurosci. 2005, 119:1389-1395.
88. Xie L., Helmerhorst E., Taddei K., Plewright B., Van Bronswijk W., Martins R. Alzheimer-s beta-amyloid peptides compete for insulin binding to the insulin receptor. J. Neurosci. 2002, 22:RC221.
89. Xu J., Eun Yeon J., Chang H., Tison G., Jun Chen G., Wands J.R., De La Monte S.M. Ethanol impairs insulin-stimulated neuronal survival in the developing brain: role of PTEN phosphatase. J. Biol. Chem. 2003, 278:26929-26937.
90. Zeger M., Popken G., Zhang J., Xuan S., Lu Q.R., Schwab M.H., Nave K.A., Rowitch D., D'Ercole A.J., Ye P. Insulin-like growth factor type 1 receptor signaling in the cells of oligodendrocyte lineage is required for normal in vivo oligodendrocyte development and myelination. Glia 2007, 55:400-411.