IDE (rs6583817) polymorphism and type 2 diabetes differentially modify executive function in older adults

Neurobiology of Aging

Volumn 34, Issue 9, 2013, Pages 2208-2216

  McFall, G Peggy ^a   Wiebe, Sandra A ^a   Vergote, David ^b   Westaway, David ^a,b   Jhamandas, Jack ^a   Dixon, Roger A ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Aging; Executive functions; Insulin degrading enzyme; Type 2 diabetes; Victoria Longitudinal Study

Indexed keywords

INSULINASE;

ADULT; AGED; AGING; ALLELE; ALZHEIMER DISEASE; ARTICLE; CONTROLLED STUDY; ENZYME POLYMORPHISM; EXECUTIVE FUNCTION; FEMALE; FUNCTIONAL ASSESSMENT; GENETIC ASSOCIATION; GENETIC MARKER; GROWTH CURVE; HUMAN; MAJOR CLINICAL STUDY; MALE; MENTAL TASK; NON INSULIN DEPENDENT DIABETES MELLITUS; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; RISK FACTOR; RISK REDUCTION;

AGED; AGED, 80 AND OVER; AGING; ALLELES; ALZHEIMER DISEASE; COGNITION; DIABETES MELLITUS, TYPE 2; EXECUTIVE FUNCTION; FEMALE; HUMANS; INSULYSIN; MALE; MIDDLE AGED; POLYMORPHISM, GENETIC; RISK FACTORS;

EID: 84878912705     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.03.010     Document Type: Article

References (70)

1. Abraham R., Myers A., Wavrant-DeVrieze F., Hamshere M.L., Thomas H.V., Marshall H., Compton D., Spurlock G., Turic D., Hoogendoorn B., Kwon J.M., Petersen R.C., Tangalow E., Norton J., Morris J.C., Bullock R., Liolitsa D., Lovestone S., Hardy J., Goate A., O'Donovan M., Williams J., Owen M.J., Jones L. Substantial linkage disequilibrium across the insulin-degrading enzyme locus but no association with late-onset Alzheimer's disease. Hum. Genet. 2001, 109:646-652.
2. Adrover-Roig D., Sesé A., Barceló F., Palmer A. Alatent variable approach to executive control in healthy ageing. Brain Cogn. 2012, 78:284-299.
3. Andrés P., Van der Linden M. Age-related differences in supervisory attentional system functions. J.Gerontol. B Psychol. Sci. Soc. Sci. 2000, 55:P373-P380.
4. Arvanitakis Z., Wilson R.S., Bienias J.L., Evans D.A., Bennett D.A. Diabetes mellitus and risk of Alzheimer disease and decline in cognitive function. Arch. Neurol. 2004, 61:661-666.
5. Awad N., Gagnon M., Messier C. The relationship between impaired glucose tolerance, type 2 diabetes, and cognitive function. J.Clin. Exp. Neuropsychol. 2004, 26:1044-1080.
6. Bartl J., Scholz C.J., Hinterberger M., Jungwirth S., Wichart I., Rainer M.K., Kneitz S., Danielczyk W., Tragl K.H., Fischer P., Riederer P., Grunblatt E. Disorder-specific effects of polymorphisms at opposing ends of the insulin degrading enzyme gene. BMC Med. Genet. 2011, 12:151.
7. Belbin O., Crump M., Bisceglio G.D., Carrasquillo M.M., Morgan K., Younkin S.G. Multiple insulin degrading enzyme variants alter invitro reporter gene expression. PLoS One 2011, 6:e21429.
8. Bennett R.G., Duckworth W.C., Hamel F.G. Degradation of amylin by insulin-degrading enzyme. J.Biol. Chem. 2000, 275:36621-36625.
9. Berg E.A. Asimple objective technique for measuring flexibility in thinking. J.Gen. Psychol. 1948, 39:15-22.
10. Bertram L., Blacker D., Mullin K., Keeney D., Jones J., Basu S., Yhu S., McInnis M.G., Go R.C., Vekrellis K., Selkoe D.J., Saunders A.J., Tanzi R.E. Evidence for genetic linkage of Alzheimer's disease to chromosome 10q. Science 2000, 290:2302-2303.
11. Biessels G.J., Deary I.J., Ryan C.M. Cognition and diabetes: a lifespan perspective. Lancet Neurol. 2008, 7:184-190.
12. Björk B.F., Katzov H., Kehoe P., Fratiglioni L., Winblad B., Prince J.A., Graff C. Positive association between risk for late-onset Alzheimer disease and genetic variation in IDE. Neurobiol. Aging 2007, 28:1374-1380.
13. Blomqvist M.E., Chalmers K., Andreasen N., Bogdanovic N., Wilcock G.K., Cairns N.J., Feuk L., Brookes A.J., Love S., Blennow K., Kehoe P.G., Prince J.A. Sequence variants of IDE are associated with the extent of β-amyloid deposition in the Alzheimer's disease brain. Neurobiol. Aging 2005, 26:795-802.
14. Boussaha M., Hannequin D., Verpillat P., Brice A., Frebourg T., Campion D. Polymorphisms of insulin degrading enzyme gene are not associated with Alzheimer's disease. Neurosci. Lett. 2002, 329:121-123.
15. Burgess P.W., Shallice T. The Hayling and Brixton Tests 1997, Thames Valley Test Company, Bury St. Edmunds, United Kingdom.
16. Carrasquillo M.M., Belbin O., Zou F., Allen M., Ertekin-Taner N., Ansari M., Wilcox S.L., Kashino M.R., Ma L., Younkin L.H., Younkin S.G., Younkin C.S., Dincman T.A., Howard M.E., Howell C.C., Stanton C.M., Watson C.M., Crump M., Vitart V., Hayward C., Hastie N.D., Rudan I., Campbell H., Polasek O., Brown K., Passmore P., Craig D., McGuinness B., Todd S., Kehoe P.G., Mann D.M., Smith A.D., Beaumont H., Warden D., Holmes C., Heun R., Kölsch H., Kalsheker N., Pankratz V.S., Dickson D.W., Graff-Radford N.R., Petersen R.C., Wright A.F., Younkin S.G., Morgan K. Concordant association of insulin degrading enzyme gene (IDE) variants with IDE mRNA, Aβ, and Alzheimer's disease. PLoS One 2010, 5:e8764.
17. Cholerton B., Baker C.D., Craft S. Insulin resistance and pathological brain ageing. Diabet. Med. 2011, 28:1463-1475.
18. D'Elia L.A., Satz P., Uchiyama C.L., White T. Color Trails Test: Professional Manual 1996, Psychological Assessment Resources, Odessa, FL.
19. de Frias C.M., Dixon R.A., Strauss E. Structure of four executive functioning tests in healthy older adults. Neuropsychology 2006, 20:206-214.
20. de Frias C.M., Dixon R.A., Strauss E. Characterizing executive functioning in older special populations: from cognitively elite to cognitively impaired. Neuropsychology 2009, 23:778-791.
21. Dixon R.A. An epidemiological approach to cognitive health in aging. Memory, Aging, and the Brain 2010, 144-166. Psychology Press, New York, NY. L. Bäckman, L. Nyberg (Eds.).
22. Dixon R.A., de Frias C.M. The Victoria Longitudinal Study: from characterizing cognitive aging to illustrating changes in memory compensation. Aging Neuropsychol. C. 2004, 11:346-376.
23. Dixon R.A., Small B.J., MacDonald S.W., McArdle J.J. Yes, memory declines with aging - but when, how, and why?. Memory and Aging 2012, 325-347. Psychology Press, New York, NY. M. Naveh-Benjamin, N. Ohta (Eds.).
24. Duggirala R., Blangero J., Almasy L., Dyer T.D., Williams K.L., Leach R.J., O'Connell P., Stern M.P. Linkage of type 2 diabetes mellitus and of age on onset to a genetic location on chromosome 10q in Mexican Americans. Am. J. Hum. Genet. 1999, 64:1127-1140.
25. Ertekin-Taner N., Aölen M., Fadale D., Scanlin L., Younkin L., Petersen R.C., Graff-Radford N., Younkin S.G. Genetic variants in a haplotype block spanning IDE are significantly associated with plasma Aβ42 levels and risk for Alzheimer Disease. Hum. Mutat. 2004, 23:334-342.
26. Farris W., Mansourian S., Chang Y., Lindsley L., Eckman E.A., Frosch M.P., Eckman C.B., Tanzi R.E., Selkoe D.J., Guénette S. Insulin-degrading enzyme regulates the levels of insulin, amyloid β-protein, and the β-amyloid precursor protein intracellular domain invivo. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:4162-4167.
27. Fischer A.L., de Frias C.M., Yeung S.E., Dixon R.A. Short-term longitudinal trends in cognitive performance in older adults with type 2 diabetes. J.Clin. Exp. Neuropsychol. 2009, 31:809-822.
28. Friedman N., Miyake A., Young S., DeFries J., Corley R., Hewitt J. Individual differences in executive functions are almost entirely genetic in origin. J.Exp. Psychol. Gen. 2008, 137:201-225.
29. Grarup N., Rose C.S., Andersson E.A., Andersen G., Nielsen A.L., Albrechtsen A., Clausen J.O., Rasmussen S.S., Jørgenen T., Sandbæk A., Lauritzen T., Schmitz O., Hansen T., Pedersen O. Studies of association of variants near the HHEX, CDKN2A/B, and IGF2BP2 genes with type 2 diabetes and impaired insulin release in 10,705 Danish subjects: validation and extension of genome-wide association studies. Diabetes 2007, 56:3105-3111.
30. Grober E., Hall C.B., Lipton R.B., Zonderman A.B., Resnick S.M., Kawas C. Memory impairment, executive dysfunction, and intellectual decline in preclinical Alzheimer's disease. J.Int. Neuropsychol. Soc. 2008, 14:266-278.
31. Karamohamed S., Demissie S., Volcjak J., Liu C., Heard-Costa N., Liu J., Shoemaker C.M., Panhuysen C.I., Meigs J.B., Wilson P., Atwood L.D., Cupples L.A., Herbert A. Polymorphisms in the insulin-degrading enzyme gene are associated with type 2 diabetes in men from the NHLBI Framingham Heart Study. Diabetes 2003, 52:1562-1567.
32. Kline R.B. Principles and Practice of Structural Equation Modeling 2011, Guilford, New York, NY. third ed.
33. Kremen W.S., Jacobson K.C., Panizzon M.S., Xian H., Eaves L.J., Eisen S.A., Tsuang M.T., Lyons M.J. Factor structure of planning and problem-solving: a behavioral genetic analysis of the Tower of London task in middle-aged twins. Behav. Genet. 2009, 39:133-144.
34. Kurochkin I.V., Goto S. Alzheimer's β-amyloid peptide specifically interacts with and is degraded by insulin degrading enzyme. FEBS Lett. 1994, 345:33-37.
35. Kwak S.H., Cho Y.M., Moon M.K., Kim J.H., Park B.L., Cheon H.S., Shin H.D., Jang H.C., Kim S.Y., Lee H.K., Park K.S. Association of polymorphisms in the insulin-degrading enzyme gene with type 2 diabetes in the Korean population. Diabetes Res. Clin. Pract. 2008, 79:284-290.
36. Lendon C., Craddock N. Susceptibility gene(s) for Alzheimer's disease on chromosome 10. Trends Neurosci. 2001, 24:557-559.
37. Lindenberger U., Nagel I.E., Chicherio C., Li S.C., Keekeren H.R., Bäckman L. Age-related decline in brain resources modulates genetic effects on cognitive functioning. Front. Neurosci. 2008, 2:234-244.
38. Luszcz M. Executive function and cognitive aging. The Handbook of the Psychology of Aging 2011, 59-72. Academic Press, San Diego, CA. seventh ed. K.W. Schaie, S.L. Willis (Eds.).
39. McFall G.P., Geall B.P., Fischer A.L., Dolcos S., Dixon R.A. Testing covariates of type 2 diabetes-cognition associations in older adults: moderating or mediating effects?. Neuropsychology 2010, 24:547-562.
40. Miyake A., Friedman N.P., Emerson M.J., Witzkin A.H., Howerter A., Wager T.D. The unity and diversity of executive functions and their contributions to complex "frontal lobe" tasks: a latent variable analysis. Cogn. Psychol. 2000, 41:49-100.
41. Muthén L.K., Muthén B.O. Mplus User's Guide 2010, Muthén and Muthén, Los Angeles, California. sixth ed.
42. Nagel I.E., Chicherio C., Li S.C., von Oertzen T., Sander T., Villringer A., Heekeren H.R., Bäckman L., Lindenberger U. Human aging magnifies genetic effects on executive functioning and working memory. Front. Hum. Neurosci. 2008, 2:1-8.
43. Nathan J., Wilkinson D., Stammers S., Low L. The role of tests of frontal executive function in the detection of mild dementia. Int. J. Geriatr. Psychiatry 2001, 16:18-26.
44. Nilsson, E., 2006. Diabetes and cognitive functioning: the role of age and comorbidity. Unpublished doctoral dissertation, Karolinska Institutet, Stockholm.
45. Okereke O.I., Selkoe D.J., Pollak M.N., Stampfer M.J., Hu F.B., Hankinson S.E., Grodstein F. Aprofile of impaired insulin degradation in relation to late-life cognitive decline: a preliminary investigation. Int. J. Geriatr. Psychiatry 2009, 24:177-182.
46. Profenno L.A., Porsteinsson A.P., Faraone S. Meta-analysis of Alzheimer's disease risk with obesity, diabetes, and related disorders. Biol. Psychiatry 2010, 67:505-512.
47. Qiu W.Q., Folstein M.F. Insulin, insulin-degrading enzyme and amyloid-β peptide in Alzheimer's disease: review and hypothesis. Neurobiol. Aging 2006, 27:190-198.
48. Rapp M.A., Reischies F.M. Attention and executive control predict Alzheimer disease in late life: results from the Berlin Aging Study (BASE). Am. J. Geriatr. Psychiatry 2005, 13:134-141.
49. Raz N., Dahle C.L., Rodrigue K.M., Kennedy K.M., Land S. Effects of age, genes, and pulse pressure on executive functions in health adults. Neurobiol. Aging 2011, 32:1124-1137.
50. Raz N., Dahle C.L., Rodrigue K.M., Kennedy K.M., Land S., Jacobs B.S. Brain-derived neurotrophic factor Val66Met and blood glucose: a synergistic effect on memory. Front. Hum. Neurosci. 2008, 2:1-6.
51. Reitan R.M., Wolfson D. Neuropsychological Evaluation of Older Children 1992, Neuropsychology Press, Tucson, AZ.
52. Rudovich N., Pivovarova O., Fisher E., Fischer-Rosinsky A., Spranger J., Möhlig M., Schulze M.B., Boeing H., Pfeiffer A.F. Polymorphisms with insulin-degrading enzyme (IDE) gene determine insulin metabolism and risk of type 2 diabetes. J.Mol. Med. 2009, 87:1145-1151.
53. Seaquist E.R., Latteman D.F., Dixon R.A. Diabetes and the brain: American Diabetes Association Research Symposium. Diabetes 2012, 61:3056-3062.
54. Shen Y., Joachimiak A., Rosner M.R., Tang W.J. Structures of human insulin-degrading enzyme reveal a new substrate recognition mechanism. Nature 2006, 443:870-874.
55. Singer J.D., Willett J.B. Applied Longitudinal Data Analysis: Modeling Change and Event Occurrence 2003, Oxford University Press, New York, NY.
56. Small B.J., Dixon R.A., McArdle J.J. Tracking cognition-health changes from 55 to 95 years of age. J.Gerontol. B Psychol. Sci. Soc. Sci. 2011, 66B:i153-i161.
57. Strachan M.W., Reynolds R.M., Marioni R.E., Price J.F. Cognitive function, dementia, and type 2 diabetes mellitus in the elderly. Nat. Rev. Endocrinol. 2011, 7:108-114.
58. Taylor S.F., Kornblum S., Lauber E.J., Minoshima S., Koeppe R.A. Isolation of specific interference processing in the Stroop task: PET activation studies. Neuroimage 1997, 6:81-92.
59. Turner G.R., Spreng R.N. Executive functions and neurocognitive aging: dissociable patterns of brain activity. Neurobiol. Aging 2012, 33. 826.e1-826.e13.
60. Umegaki H. Neurodegeneration in diabetes mellitus. Neurodegenerative Diseases 2012, 258-265. Landes Bioscience and Springer Science and Business Media, New York, NY. H.I. Ahmad (Ed.).
61. Vardy E.R.L.C., Brown K., Stopford C.L., Thompson J.C., Richardson A.M., Neary D., Kalsheker N., Morgan K., Mann D.M., Snowden J.S. Cognitive phenotypes in Alzheimer's disease and genetic variants in ACE and IDE. Neurobiol. Aging 2012, 33:1486.e1-1486.e2.
62. Vasilopoulos T., Franz C.E., Panisson M.S., Xian H., Grant M.D., Lyons M.J., Toomey R., Jacobson K.C., Kremen W.S. Genetic architecture of the Delis-Kaplan executive function system trail making test: evidence for distinct genetic influences on executive function. Neuropsychology 2012, 26:238-250.
63. Vionnet N., Hani E.H., Dupont S., Gallena S., Francke S., Dotte S., De Matos F., Durand E., Leprêtre F., Lecoeur C., Gallina P., Zekiri L., Dina C., Froguel P. Genomewide search for type 2 diabetes-susceptibility genes in French whites: a novel susceptibility locus for early-onset diabetes on chromosome 3q27-qter and independent replication of a type 2-diabetes locus on chromosome 1q21-q24. Am. J. Hum. Genet. 2000, 67:1470-1480.
64. Wang F., Shu C., Jia L., Zuo X., Zhang Y., Zhou A., Qin W., Song H., Wei C., Zhang F., Hong Z., Tang M., Wang D.M., Jia J. Exploration of 16 candidate genes identifies the association of IDE with Alzheimer's disease in Han Chinese. Neurobiol. Aging 2012, 33:1014.e1-1014.e9.
65. West R.L. An application of prefrontal cortex function theory to cognitive aging. Psychol. Bull. 1996, 120:272-292.
66. Wiebe S.A., Espy K.A., Charak D. Using confirmatory factor analysis to understand executive control in preschool children: I. Latent structure. Dev. Psychol. 2008, 44:575-587.
67. Wiebe S.A., Sheffield T., Nelson J.M., Clark C.A., Chevalier N., Espy K.A. The structure of executive function in 3-year-olds. J.Exp. Child Psychol. 2010, 108:436-452.
68. Wishart H.A., Roth R.M., Saykin A.J., Rhodes C.H., Tsongalis G.J., Pattin K.A., Moore J.H., McAllister T.W. COMT Val158Met genotype and individual differences in executive function in healthy adults. J.Int. Neuropsychol. Soc. 2011, 17:174-180.
69. Yeung S.E., Fischer A.L., Dixon R.A. Exploring effects of type 2 diabetes on cognitive functioning in older adults. Neuropsychology 2009, 23:1-9.
70. Zeggini E., Scott L.J., Saxena R., Voight B.F., Marchini J.L., Hu T., de Bakker P.I., Abecasis G.R., Almgren P., Andersen G., Ardlie K., Boström K.B., Bergman R.N., Bonnycastle L.L., Borch-Johnsen K., Burtt N.P., Chen H., Chines P.S., Daly M.J., Deodhar P., Ding C., Doney A.S., Duren W.L., Elliott K.S., Erdos M.R., Frayling T.M., Freathy R.M., Gianniny L., Grallert H., Grarup N., Groves C.J., Guiducci C., Hansen T., Herder C., Hitman G.A., Hughes T.E., Isomaa B., Jackson A.U., Jørgensen T., Kong A., Kubalanza K., Kuruvilla F.G., Kuusisto J., Langenberg C., Lango H., Lauritzen T., Li Y., Lindgren C.M., Lyssenko V., Marvelle A.F., Meisinger C., Midthjell K., Mohlke K.L., Morken M.A., Morris A.D., Narisu N., Nilsson P., Owen K.R., Palmer C.N., Payne F., Perry J.R., Pettersen E., Platou C., Prokopenko I., Qi L., Qin L., Rayner N.W., Rees M., Roix J.J., Sandbæk A., Shields B., Sjögren M., Steinthorsdottir V., Stringham H.M., Swift A.J., Thorleifsson G., Thorsteinsdottir U., Timpson N.J., Tuomi T., Tuomilehto J., Walker M., Watanabe R.M., Weedon M.N., Willer C.J., Illig T., Hveem K., Hu F.B., Laakso M., Stefansson K., Pedersen O., Wareham N.J., Barroso I., Hattersley A.T., Collins F.S., Groop L., McCarthy M.I., Boehnke M., Altshuler D. Meta-analysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes. Nat. Genet. 2008, 40:638-645. Wellcome Trust Case Control Consortium.