Cognitively impaired elderly exhibit insulin resistance and no memory improvement with infused insulin

Neurobiology of Aging

Volumn 39, Issue , 2016, Pages 19-24

  Morris, Jill K ^a,b   Vidoni, Eric D ^a,b   Mahnken, Jonathan D ^a,b   Montgomery, Robert N ^b   Johnson, David K ^a,c   Thyfault, John P ^b   Burns, Jeffrey M ^a,b  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

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

^c UNIVERSITY OF KANSAS   (United States)

Author keywords

Aging; Alzheimer's disease; Cognitive impairment; Hyperinsulinemia; Insulin; Insulin resistance

Indexed keywords

AMYLIN; INSULIN; GLUCOSE;

ADULT; AGED; ARTICLE; BLOOD BRAIN BARRIER; BODY MASS; COGNITIVE DEFECT; EPISODIC MEMORY; FAT MASS; FEMALE; HUMAN; INSULIN RESISTANCE; LEAN BODY WEIGHT; MAJOR CLINICAL STUDY; MALE; METABOLIC DISORDER; PRIORITY JOURNAL; STEADY STATE; VERBAL MEMORY; ALZHEIMER DISEASE; COGNITION DISORDERS; COHORT ANALYSIS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; RISK FACTOR;

AGED; ALZHEIMER DISEASE; BLOOD-BRAIN BARRIER; COGNITION DISORDERS; COHORT STUDIES; FEMALE; GLUCOSE; HUMANS; INSULIN; INSULIN RESISTANCE; MALE; MEMORY, EPISODIC; RISK FACTORS;

EID: 84959572889     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2015.11.005     Document Type: Article

References (55)

1. Adler B.L, Yarchoan M., Hwang H.M., Louneva N., Blair J.A., Palm R., Smith M.A., Lee H.G., Arnold S.E., Casadesus G. Neuroprotective effects of the amylin analogue pramlintide on Alzheimer's disease pathogenesis and cognition. Neurobiol. Aging 2014, 35:793-801.
2. Banks W.A. The source of cerebral insulin. Eur. J. Pharmacol. 2004, 490:5-12.
3. Baura G.D, Foster D.M., Porte D., Kahn S.E., Bergman R.N., Cobelli C., Schwartz M.W. Saturable transport of insulin from plasma into the central nervous system of dogs in vivo. A mechanism for regulated insulin delivery to the brain. J. Clin. Invest. 1993, 92:1824-1830.
4. 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.
5. Burns J.M, Honea R.A., Vidoni E.D., Hutfles L.J., Brooks W.M., Swerdlow R.H. Insulin is differentially related to cognitive decline and atrophy in Alzheimer's disease and aging. Biochim. Biophys. Acta 2012, 1822:333-339.
6. Carantoni M, Zuliani G., Munari M.R., D'Elia K., Palmieri E., Fellin R. Alzheimer disease and vascular dementia: relationships with fasting glucose and insulin levels. Dement. Geriatr. Cogn. Disord. 2000, 11:176-180.
7. Charge S.B, de Koning E.J., Clark A. Effect of pH and insulin on fibrillogenesis of islet amyloid polypeptide in vitro. Biochemistry 1995, 34:14588-14593.
8. Cheng D, Noble J., Tang M.X., Schupf N., Mayeux R., Luchsinger J.A. Type 2 diabetes and late-onset Alzheimer's disease. Dement Geriatr. Cogn. Disord. 2011, 31:424-430.
9. Clark A, Saad M.F., Nezzer T., Uren C., Knowler W.C., Bennett P.H., Turner R.C. Islet amyloid polypeptide in diabetic and non-diabetic Pima Indians. Diabetologia 1990, 33:285-289.
10. Claxton A, Baker L.D., Wilkinson W., Trittschuh E.H., Chapman D., Watson G.S., Cholerton B., Plymate S.R., Arbuckle M., Craft S. Sex and ApoE genotype differences in treatment response to two doses of intranasal insulin in adults with mild cognitive impairment or Alzheimer's disease. J. Alzheimers Dis. 2013, 35:789-797.
11. Claxton A, Baker L.D., Hanson A., Trittschuh E.H., Cholerton B., Morgan A., Callaghan M., Arbuckle M., Behl C., Craft S. Long-acting intranasal insulin detemir improves cognition for adults with mild cognitive impairment or early-stage Alzheimer's disease dementia. J. Alzheimers Dis. 2015, 44:897-906.
12. Craft S, Dagogo-Jack S.E., Wiethop B.V., Murphy C., Nevins R.T., Fleischman S., Rice V., Newcomer J.W., Cryer P.E. Effects of hyperglycemia on memory and hormone levels in dementia of the Alzheimer type: a longitudinal study. Behav. Neurosci. 1993, 107:926-940.
13. Craft S, Newcomer J., Kanne S., Dagogo-Jack S., Cryer P., Sheline Y., Luby J., Dagogo-Jack A., Alderson A. Memory improvement following induced hyperinsulinemia in Alzheimer's disease. Neurobiol. Aging 1996, 17:123-130.
14. 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.
15. Craft S, Asthana S., Newcomer J.W., Wilkinson C.W., Matos I.T., Baker L.D., Cherrier M., Lofgreen C., Latendresse S., Petrova A., Plymate S., Raskind M., Grimwood K., Veith R.C. Enhancement of memory in Alzheimer disease with insulin and somatostatin, but not glucose. Arch. Gen. Psychiatry 1999, 56:1135-1140.
16. Craft S, Asthana S., Schellenberg G., Cherrier M., Baker L.D., Newcomer J., Plymate S., Latendresse S., Petrova A., Raskind M., Peskind E., Lofgreen C., Grimwood K. Insulin metabolism in Alzheimer's disease differs according to apolipoprotein E genotype and gender. Neuroendocrinology 1999, 70:146-152.
17. Craft S, Baker L.D., Montine T.J., Minoshima S., Watson G.S., Claxton A., Arbuckle M., Callaghan M., Tsai E., Plymate S.R., Green P.S., Leverenz J., Cross D., Gerton B. Intranasal insulin therapy for Alzheimer disease and amnestic mild cognitive impairment: a pilot clinical trial. Arch. Neurol. 2012, 69:29-38.
18. Emoto M, Nishizawa Y., Maekawa K., Hiura Y., Kanda H., Kawagishi T., Shoji T., Okuno Y., Morii H. Homeostasis model assessment as a clinical index of insulin resistance in type 2 diabetic patients treated with sulfonylureas. Diabetes Care 1999, 22:818-822.
19. Fruehwald-Schultes B, Kern W., Born J., Fehm H.L., Peters A. Hyperinsulinemia causes activation of the hypothalamus-pituitary-adrenal axis in humans. Int. J. Obes. Relat. Metab. Disord. 2001, 25(Suppl 1):S38-S40.
20. Garcia-Lara J.M, Aguilar-Navarro S., Gutierrez-Robledo L.M., Avila-Funes J.A. The metabolic syndrome, diabetes, and Alzheimer's disease. Rev. Invest. Clin. 2010, 62:343-349.
21. Het S, Ramlow G., Wolf O.T. A meta-analytic review of the effects of acute cortisol administration on human memory. Psychoneuroendocrinology 2005, 30:771-784.
22. Hishikawa N, Yamashita T., Deguchi K., Wada J., Shikata K., Makino H., Abe K. Cognitive and affective functions in diabetic patients associated with diabetes-related factors, white matter abnormality and aging. Eur. J. Neurol. 2015, 22:313-321.
23. Jackson K, Barisone G.A., Diaz E., Jin L.W., DeCarli C., Despa F. Amylin deposition in the brain: a second amyloid in Alzheimer disease?. Ann. Neurol. 2013, 74:517-526.
24. Katsuki A, Sumida Y., Gabazza E.C., Murashima S., Furuta M., Araki-Sasaki R., Hori Y., Yano Y., Adachi Y. Homeostasis model assessment is a reliable indicator of insulin resistance during follow-up of patients with type 2 diabetes. Diabetes Care 2001, 24:362-365.
25. Lebowitz M.R., Blumenthal S.A. The molar ratio of insulin to C-peptide. An aid to the diagnosis of hypoglycemia due to surreptitious (or inadvertent) insulin administration. Arch. Intern. Med. 1993, 153:650-655.
26. Lee H.K, Kumar P., Fu Q., Rosen K.M., Querfurth H.W. The insulin/Akt signaling pathway is targeted by intracellular beta-amyloid. Mol. Biol. Cell 2009, 20:1533-1544.
27. 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.
28. Liu Y, Liu F., Grundke-Iqbal I., Iqbal K., Gong C.X. Deficient brain insulin signalling pathway in Alzheimer's disease and diabetes. J. Pathol. 2011, 225:54-62.
29. Liu Z, Zhu H., Fang G.G., Walsh K., Mwamburi M., Wolozin B., Abdul-Hay S.O., Ikezu T., Leissring M.A., Qiu W.Q. Characterization of insulin degrading enzyme and other amyloid-beta degrading proteases in human serum: a role in Alzheimer's disease?. J. Alzheimers Dis. 2012, 29:329-340.
30. Lorenzo A, Razzaboni B., Weir G.C., Yankner B.A. Pancreatic islet cell toxicity of amylin associated with type-2 diabetes mellitus. Nature 1994, 368:756-760.
31. Lukinius A, Wilander E., Westermark G.T., Engstrom U., Westermark P. Co-localization of islet amyloid polypeptide and insulin in the B cell secretory granules of the human pancreatic islets. Diabetologia 1989, 32:240-244.
32. Man H.Y, Wang Q., Lu W.Y., Ju W., Ahmadian G., Liu L., D'Souza S., Wong T.P., Taghibiglou C., Lu J., Becker L.E., Pei L., Liu F., Wymann M.P., MacDonald J.F., Wang Y.T. Activation of PI3-kinase is required for AMPA receptor insertion during LTP of mEPSCs in cultured hippocampal neurons. Neuron 2003, 38:611-624.
33. Moloney A.M, Griffin R.J., Timmons S., O'Connor R., Ravid R., O'Neill C. Defects in IGF-1 receptor, insulin receptor and IRS-1/2 in Alzheimer's disease indicate possible resistance to IGF-1 and insulin signalling. Neurobiol. Aging 2010, 31:224-243.
34. Morris J.C. The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology 1993, 43:2412-2414. [see comment].
35. Morris J.C. Clinical dementia rating: a reliable and valid diagnostic and staging measure for dementia of the Alzheimer type. Int. Psychogeriatr. 1997, 9:173-176.
36. Morris J.K., Burns J.M. Insulin: an emerging treatment for Alzheimer's disease dementia?. Curr. Neurol. Neurosci. Rep. 2012, 12:520-527.
37. Morris J.K., Vidoni E.D., Perea R.D., Rada R., Johnson D.K., Lyons K., Pahwa R., Burns J.M., Honea R.A. Insulin resistance and gray matter volume in neurodegenerative disease. Neuroscience 2014, 270:139-147.
38. Ohara T, Doi Y., Ninomiya T., Hirakawa Y., Hata J., Iwaki T., Kanba S., Kiyohara Y. Glucose tolerance status and risk of dementia in the community: the Hisayama study. Neurology 2011, 77:1126-1134.
39. 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.
40. Perez A, Morelli L., Cresto J.C., Castano E.M. Degradation of soluble amyloid beta-peptides 1-40, 1-42, and the Dutch variant 1-40Q by insulin degrading enzyme from Alzheimer disease and control brains. Neurochem. Res. 2000, 25:247-255.
41. Polonsky K.S., Rubenstein A.H. Current approaches to measurement of insulin secretion. Diabetes Metab. Rev. 1986, 2:315-329.
42. 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.
43. 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 administration dose-dependently modulates verbal memory and plasma amyloid-beta in memory-impaired older adults. J. Alzheimers Dis. 2008, 13:323-331.
44. 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.
45. Rockwood K, Strang D., MacKnight C., Downer R., Morris J.C. Interrater reliability of the Clinical Dementia Rating in a multicenter trial. J. Am. Geriatr. Soc. 2000, 48:558-559.
46. Rojas J.M., Schwartz M.W. Control of hepatic glucose metabolism by islet and brain. Diabetes Obes. Metab. 2014, 16(Suppl 1):33-40.
47. Rosenbloom M.H, Barclay T.R., Pyle M., Owens B.L., Cagan A.B., Anderson C.P., Frey W.H., Hanson L.R. A single-dose pilot trial of intranasal rapid-acting insulin in apolipoprotein E4 carriers with mild-moderate Alzheimer's disease. CNS Drugs 2014, 28:1185-1189.
48. Rushing P.A, Hagan M.M., Seeley R.J., Lutz T.A., D'Alessio D.A., Air E.L., Woods S.C. Inhibition of central amylin signaling increases food intake and body adiposity in rats. Endocrinology 2001, 142:5035.
49. Skeberdis V.A, Lan J., Zheng X., Zukin R.S., Bennett M.V. Insulin promotes rapid delivery of N-methyl-D- aspartate receptors to the cell surface by exocytosis. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:3561-3566.
50. 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.
51. 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. Invest. 2012, 122:1316-1338.
52. 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.
53. Xu W, Qiu C., Gatz M., Pedersen N.L., Johansson B., Fratiglioni L. Mid- and late-life diabetes in relation to the risk of dementia: a population-based twin study. Diabetes 2009, 58:71-77.
54. Yokoyama H, Emoto M., Fujiwara S., Motoyama K., Morioka T., Komatsu M., Tahara H., Shoji T., Okuno Y., Nishizawa Y. Quantitative insulin sensitivity check index and the reciprocal index of homeostasis model assessment in normal range weight and moderately obese type 2 diabetic patients. Diabetes Care 2003, 26:2426-2432.
55. Young S.E, Mainous A.G., Carnemolla M. Hyperinsulinemia and cognitive decline in a middle-aged cohort. Diabetes Care 2006, 29:2688-2693.