Insulin is differentially related to cognitive decline and atrophy in Alzheimer's disease and aging

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1822, Issue 3, 2012, Pages 333-339

  Burns, Jeffrey M ^a   Honea, Robyn A ^a   Vidoni, Eric D ^a   Hutfles, Lewis J ^a   Brooks, William M ^a,b   Swerdlow, Russell H ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

Alzheimer disease; Brain atrophy; Cognitive decline; Glucose tolerance test; Insulin

Indexed keywords

GLUCOSE; INSULIN; ORAL ANTIDIABETIC AGENT;

AGED; AGING; ALZHEIMER DISEASE; AREA UNDER THE CURVE; ARTICLE; BRAIN ATROPHY; BRAIN REGION; CINGULATE GYRUS; CLINICAL ASSESSMENT; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DIABETES MELLITUS; DIAGNOSTIC TEST; DIAGNOSTIC TEST ACCURACY STUDY; DISEASE ASSOCIATION; FEMALE; GLOBAL COGNITIVE PERFORMANCE; GLUCOSE BLOOD LEVEL; HIPPOCAMPUS; HUMAN; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INTRAVENOUS GLUCOSE TOLERANCE TEST; MAJOR CLINICAL STUDY; MALE; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RATING SCALE; RISK FACTOR; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION; TASK PERFORMANCE;

AGED; AGING; ALZHEIMER DISEASE; AREA UNDER CURVE; ATROPHY; COGNITION DISORDERS; COHORT STUDIES; DISEASE PROGRESSION; FEMALE; FOLLOW-UP STUDIES; GLUCOSE TOLERANCE TEST; GYRUS CINGULI; HIPPOCAMPUS; HUMANS; INSULIN; INSULIN RESISTANCE; MAGNETIC RESONANCE IMAGING; MALE; NEUROIMAGING;

EID: 84856046189     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2011.06.011     Document Type: Article

References (53)

1. Unger J.W., Livingston J.N., Moss A.M. Insulin receptors in the central nervous system: localization, signalling mechanisms and functional aspects. Prog. Neurobiol. 1991, 36:343-362.
2. Adamo M., Raizada M.K., LeRoith D. Insulin and insulin-like growth factor receptors in the nervous system. Mol. Neurobiol. 1989, 3:71-100.
3. van der Heide L.P., Ramakers G.M.J., Smidt M.P. Insulin signaling in the central nervous system: learning to survive. Prog. Neurobiol. 2006, 79:205-221.
4. Chiu S.L., Chen C.M., Cline H.T. Insulin receptor signaling regulates synapse number, dendritic plasticity, and circuit function in vivo. Neuron 2008, 58:708-719.
5. Zhao W.Q., Townsend M. Insulin resistance and amyloidogenesis as common molecular foundation for type 2 diabetes and Alzheimer's disease. Biochim. Biophys. Acta 2009, 1792:482-496.
6. Matsuzaki H T.M., Mitsuda N., Namikawa K., Kiyama H., Miyake S., Tohyama M. Activation of Akt kinase inhibits apoptosis and changes in Bcl-2 and Bax expression induced by nitric oxide in primary hippocampal neurons. J. Neurochem. 1999, 73:2037-2046.
7. Yamaguchi A., Tamatani M., Matsuzaki H., Namikawa K., Kiyama H., Vitek M.P., Mitsuda N., Tohyama M. Akt Activation Protects Hippocampal Neurons from Apoptosis by Inhibiting Transcriptional Activity of p53 2001, vol. 276:5256-5264.
8. Philpott K.L., McCarthy M.J., Klippel A., Rubin L.L. Activated Phosphatidylinositol 3-Kinase and Akt Kinase Promote Survival of Superior Cervical Neurons 1997, vol. 139:809-815.
9. Ott A., Stolk R.P., van Harskamp F., Pols H.A.P., Hofman A., Breteler M.M.B. Diabetes mellitus and the risk of dementia: the Rotterdam study. Neurology 1999, 53:1937.
10. Leibson C.L., Rocca W.A., Hanson V.A., Cha R., Kokmen E., O'Brien P.C., Palumbo P.J. Risk of dementia among persons with diabetes mellitus: a population-based cohort study. Am. J. Epidemiol. 1997, 145:301-308.
11. 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.
12. Yaffe K., Kanaya A., Lindquist K., Simonsick E.M., Harris T., Shorr R.I., Tylavsky F.A., Newman A.B. The metabolic syndrome, inflammation, and risk of cognitive decline. JAMA 2004, 292:2237-2242.
13. Peila R., Rodriguez B.L., White L.R., Launer L.J. Fasting insulin and incident dementia in an elderly population of Japanese-American men. Neurology 2004, 63:228-233.
14. Luchsinger J.A., Tang M.-X., Shea S., Mayeux R. Hyperinsulinemia and risk of Alzheimer disease. Neurology 2004, 63:1187-1192.
15. Araki Y., Nomura M., Tanaka H., Yamamoto H., Yamamoto T., Tsukaguchi I., Nakamura H. MRI of the brain in diabetes mellitus. Neuroradiology 1994, 36:101-103.
16. den Heijer T., Vermeer S.E., van Dijk E.J., Prins N.D., Koudstaal P.J., Hofman A., Breteler M.M. Type 2 diabetes and atrophy of medial temporal lobe structures on brain MRI. Diabetologia 2003, 46:1604-1610.
17. Craft S., Peskind E., Schwartz M.W., Schellenberg G.D., Raskind M., Porte D. Cerebrospinal fluid and plasma insulin levels in Alzheimer's disease: relationship to severity of dementia and apolipoprotein E genotype. Neurology 1998, 50:164-168.
18. 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.
19. Phiel C.J., Wilson C.A., Lee V.M.Y., Klein P.S. GSK-3[alpha] regulates production of Alzheimer's disease amyloid-[beta] peptides. Nature 2003, 423:435-439.
20. 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.
21. 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. 2004, 101:3100-3105.
22. Gasparini L., Gouras G.K., Wang R., Gross R.S., Flint Beal M., 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.
23. Carro E., Trejo J.L., Gomez-Isla T., LeRoith D., Torres-Aleman I. Serum insulin-like growth factor I regulates brain amyloid-[Beta;] levels. Nat. Med. 2002, 8:1390-1397.
24. Watson G.S., Peskind E.R., Asthana S., Purganan K., Wait C., Chapman D., Schwartz M.W., Plymate S., Craft S. Insulin increases CSF A{beta}42 levels in normal older adults. Neurology 2003, 60:1899-1903.
25. De Felice F.G., Vieira M.N., Bomfim T.R., Decker H., Velasco P.T., Lambert M.P., Viola K.L., Zhao W.Q., Ferreira S.T., Klein W.L. Protection of synapses against Alzheimer's-linked toxins: insulin signaling prevents the pathogenic binding of Abeta oligomers. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:1971-1976.
26. 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.
27. Craft S., Asthana S., Schellenberg G., Baker L., Cherrier M., Boyt A.A., Martins R.N., Raskind M., Peskind E., Plymate S. Insulin effects on glucose metabolism, memory, and plasma amyloid precursor protein in Alzheimer's disease differ according to apolipoprotein-E genotype. Ann. N. Y. Acad. Sci. 2000, 903:222-228.
28. Craft S. Insulin resistance syndrome and Alzheimer disease: pathophysiologic mechanisms and therapeutic implications. Alzheimer Dis. Assoc. Disord. 2006, 20:298-301.
29. Strachan M.W. Insulin and cognitive function in humans: experimental data and therapeutic considerations. Biochem. Soc. Trans. 2005, 33:1037-1040.
30. Landreth G. PPARgamma agonists as new therapeutic agents for the treatment of Alzheimer's disease.[comment]. Exp. Neurol. 2006, 199:245-248.
31. 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.
32. Burns J.M., Donnelly J.E., Anderson H.S., Mayo M.S., Spencer-Gardner L., Thomas G., Cronk B.B., Haddad Z., Klima D., Hansen D., Brooks W.M. Peripheral insulin and brain structure in early Alzheimer disease. Neurology 2007, 69:1094-1104.
33. Mielke M.M., Zandi P.P., Sjogren M., Gustafson D., Ostling S., Steen B., Skoog I. High total cholesterol levels in late life associated with a reduced risk of dementia. Neurology 2005, 64:1689-1695.
34. Sanz C., Andrieu S., Sinclair A., Hanaire H., Vellas B. Diabetes is associated with a slower rate of cognitive decline in Alzheimer disease. Neurology 2009, 73:1359-1366.
35. Beeri M.S., Silverman J.M., Davis K.L., Marin D., Grossman H.Z., Schmeidler J., Purohit D.P., Perl D.P., Davidson M., Mohs R.C., Haroutunian V. Type 2 diabetes is negatively associated with Alzheimer's disease neuropathology. J. Gerontol. A Biol. Sci. Med. Sci. 2005, 60:471-475.
36. Sonnen J.A., Larson E.B., Brickell K., Crane P.K., Woltjer R., Montine T.J., Craft S. Different patterns of cerebral injury in dementia with or without diabetes. Arch. Neurol. 2009, 66:315-322.
37. McKhann G., Drachman D., Folstein M., Katzman R., Price D., Stadlan E.M. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's disease. Neurology 1984, 34:939-944.
38. Morris J.C. The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology 1993, 43:2412b-2414b.
39. Smith S.M., Zhang Y., Jenkinson M., Chen J., Matthews P.M., Federico A., De Stefano N. Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. NeuroImage 2002, 17:479-489.
40. Ashburner J. A fast diffeomorphic image registration algorithm. NeuroImage 2007, 38:95-113.
41. Yaffe K., Blackwell T., Kanaya A.M., Davidowitz N., Barrett-Connor E., Krueger K. Diabetes, impaired fasting glucose, and development of cognitive impairment in older women. Neurology 2004, 63:658-663.
42. Geroldi C., Frisoni G.B., Paolisso G., Bandinelli S., Lamponi M., Abbatecola A.M., Zanetti O., Guralnik J.M., Ferrucci L. Insulin resistance in cognitive impairment: the InCHIANTI study. Arch. Neurol. 2005, 62:1067-1072.
43. Tanaka M., Sawada M., Yoshida S., Hanaoka F., Marunouchi T. Insulin prevents apoptosis of external granular layer neurons in rat cerebellar slice cultures. Neurosci. Lett. 1995, 199:37-40.
44. Ahtiluoto S., Polvikoski T., Peltonen M., Solomon A., Tuomilehto J., Winblad B., Sulkava R., Kivipelto M. Diabetes, Alzheimer disease, and vascular dementia. Neurology 2010, 75:1195-1202.
45. Bruandet A., Richard F., Bombois S., Maurage C.A., Deramecourt V., Lebert F., Amouyel P., Pasquier F. Alzheimer disease with cerebrovascular disease and vascular dementia: clinical features and course compared with Alzheimer disease. J. Neurol. Neurosurg. Psychiatry 2009, 80:133-139.
46. Snowdon D.A., Greiner L.H., Mortimer J.A., Riley K.P., Greiner P.A., Markesbery W.R. Brain infarction and the clinical expression of Alzheimer disease. J. Am. Med. Assoc. 1997, 277:813-817.
47. Burns J.M., Church J.A., Johnson D.K., Xiong C., Marcus D., Fotenos A.F., Snyder A.Z., Morris J.C., Buckner R.L. White matter lesions are prevalent but differentially related with cognition in aging and early Alzheimer disease. Arch. Neurol. 2005, 62:1870-1876.
48. Janson J., Laedtke T., Parisi J.E., O'Brien P., Petersen R.C., Butler P.C. Increased risk of type 2 diabetes in Alzheimer disease. Diabetes 2004, 53:474-481.
49. Ronnemaa E., Zethelius B., Sundelof J., Sundstrom J., Degerman-Gunnarsson M., Berne C., Lannfelt L., Kilander L. Impaired insulin secretion increases the risk of Alzheimer disease. Neurology 2008, 71:1065-1071.
50. Loskutova N., Honea R.A., Brooks W.M., Burns J.M. Reduced limbic and hypothalamic volumes correlate with bone density in early Alzheimer's disease. J. Alzheimers Dis. 2010, 20:313-322.
51. Johnson D.K., Wilkins C.H., Morris J.C. Accelerated weight loss may precede diagnosis in Alzheimer disease. Arch. Neurol. 2006, 63:1312-1317.
52. Peila R., Rodriguez B.L., Launer L.J. Type 2 diabetes, APOE gene, and the risk for dementia and related pathologies: the Honolulu-Asia aging study. Diabetes 2002, 51:1256-1262.
53. Morris J.C., Storandt M., Miller J.P., McKeel D.W., Price J.L., Rubin E.H., Berg L. Mild cognitive impairment represents early-stage Alzheimer disease. Arch. Neurol. 2001, 58:397-405.