Aging-related magnification of genetic effects on cognitive and brain integrity

Trends in Cognitive Sciences

Volumn 19, Issue 9, 2015, Pages 506-514

  Papenberg, Goran ^a   Lindenberger, Ulman ^b,c   Bäckman, Lars ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b MAX PLANCK INSTITUTE FOR HUMAN DEVELOPMENT   (Germany)

^c MAX PLANCK UCL CENTRE FOR COMPUTATIONAL PSYCHIATRY AND AGEING RESEARCH   (United Kingdom)

Author keywords

Aging; Brain function; Brain structure; Cognition; Genetics

Indexed keywords

AGING OF MATERIALS; BIOLOGY; COGNITIVE SYSTEMS;

BRAIN FUNCTIONS; BRAIN STRUCTURE; COGNITION; COGNITIVE PERFORMANCE; EPIGENETIC MECHANISMS; GENE-ENVIRONMENT INTERACTION; GENETIC VARIATION; GENETICS;

GENES;

APOLIPOPROTEIN E; BRAIN DERIVED NEUROTROPHIC FACTOR; CATECHOL METHYLTRANSFERASE; DOPAMINE 2 RECEPTOR; KIDNEY AND BRAIN EXPRESSED PROTEIN; PROTEIN; UNCLASSIFIED DRUG; APOLIPOPROTEIN E (133-149); PEPTIDE FRAGMENT;

AGING; BEHAVIOR; BRAIN FUNCTION; COGNITION; EPIGENETICS; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; HEREDITY; HERITABILITY; HUMAN; PROTEIN POLYMORPHISM; REVIEW; SENESCENCE; AGED; ANATOMY AND HISTOLOGY; BRAIN; GENETICS; PHYSIOLOGY; VERY ELDERLY;

AGED; AGED, 80 AND OVER; AGING; APOLIPOPROTEINS E; BRAIN; COGNITION; GENE-ENVIRONMENT INTERACTION; HUMANS; PEPTIDE FRAGMENTS;

EID: 84952637125     PISSN: 13646613     EISSN: 1879307X     Source Type: Journal    
DOI: 10.1016/j.tics.2015.06.008     Document Type: Review

References (93)

1. Rönnlund M., et al. Stability, growth, and decline in adult life span development of declarative memory: cross-sectional and longitudinal data from a population-based study. Psychol. Aging 2005, 20:3-18.
2. Lindenberger U., et al. Heterogeneity in frontal lobe aging. Principles of Frontal Lobe Functions 2013, 609-627. Oxford University Press. D.T. Stuss, R.T. Knight (Eds.).
3. Fandakova Y., et al. Maintenance of youth-like processing protects against false memory in later adulthood. Neurobiol. Aging 2014, 36:933-941.
4. Nyberg L., et al. Memory aging and brain maintenance. Trends Cogn. Sci. 2012, 16:292-305.
5. Finkel D., et al. Longitudinal and cross-sectional twin data on cognitive abilities in adulthood: the Swedish Adoption/Twin Study of Aging. Dev. Psychol. 1998, 34:1400-1413.
6. Reynolds C.A., Finkel D. A meta-analysis of heritability of cognitive aging: minding the 'missing heritability' gap. Neuropsychol. Rev. 2015, 25:97-112.
7. McClearn G.E., et al. Substantial genetic influence on cognitive abilities in twins 80 or more years old. Science 1997, 276:1560-1563.
8. Tucker-Drob E.M., et al. Shared and unique genetic and environmental influences on aging-related changes in multiple cognitive abilities. Dev. Psychol. 2014, 50:152-166.
9. Batouli S.A., et al. The heritability of volumes of brain structures and its relationship to age: a review of twin and family studies. Ageing Res. Rev. 2014, 13:1-9.
10. Kremen W.S., et al. Heritability of brain ventricle volume: converging evidence from inconsistent results. Neurobiol. Aging 2012, 33:1-8.
11. Vogler C., et al. Substantial SNP-based heritability estimates for working memory performance. Transl. Psychiatry 2014, 4:e438.
12. Davies G., et al. Genome-wide association studies establish that human intelligence is highly heritable and polygenic. Mol. Psychiatry 2011, 16:996-1005.
13. Wilson R.S., et al. Heritability of different forms of memory in the Late Onset Alzheimer's Disease Family Study. J. Alzheimers Dis. 2011, 23:249-255.
14. Lindenberger U., et al. Age-related decline in brain resources modulates genetic effects on cognitive functioning. Front. Neurosci. 2008, 2:234-244.
15. Rasch B., et al. Imaging genetics of cognitive functions: focus on episodic memory. Neuroimage 2010, 53:870-877.
16. Bu G. Apolipoprotein E and its receptors in Alzheimer's disease: pathways, pathogenesis and therapy. Nat. Rev. Neurosci. 2009, 10:333-344.
17. Okuizumi K., et al. Genetic association of the very low density lipoprotein (VLDL) receptor gene with sporadic Alzheimer's disease. Nat. Genet. 1995, 11:207-209.
18. Blacker D., et al. ApoE-4 and age at onset of Alzheimer's disease: the NIMH genetics initiative. Neurology 1997, 48:139-147.
19. Dik M.G., et al. Stroke and apolipoprotein E epsilon4 are independent risk factors for cognitive decline: a population-based study. Stroke 2000, 31:2431-2436.
20. Bretsky P., et al. The role of APOE-epsilon4 in longitudinal cognitive decline: MacArthur Studies of Successful Aging. Neurology 2003, 60:1077-1081.
21. Wisdom N.M., et al. The effects of apolipoprotein E on non-impaired cognitive functioning: a meta-analysis. Neurobiol. Aging 2011, 32:63-74.
22. Liu F., et al. The apolipoprotein E gene and its age-specific effects on cognitive function. Neurobiol. Aging 2010, 31:1831-1833.
23. Schiepers O.J., et al. APOE E4 status predicts age-related cognitive decline in the ninth decade: longitudinal follow-up of the Lothian Birth Cohort 1921. Mol. Psychiatry 2012, 17:315-324.
24. Zhang C., Pierce B.L. Genetic susceptibility to accelerated cognitive decline in the US Health and Retirement Study. Neurobiol. Aging 2014, 35:1512-1518.
25. De Jager P.L., et al. A genome-wide scan for common variants affecting the rate of age-related cognitive decline. Neurobiol. Aging 2012, 33:e1011-e1015.
26. Filippini N., et al. Differential effects of the APOE genotype on brain function across the lifespan. Neuroimage 2011, 54:602-610.
27. Nichols L.M., et al. Interactive effect of apolipoprotein e genotype and age on hippocampal activation during memory processing in healthy adults. Arch. Gen. Psychiatry 2012, 69:804-813.
28. Grady C. The cognitive neuroscience of ageing. Nat. Rev. Neurosci. 2012, 13:491-505.
29. Crivello F., et al. Effects of ApoE-epsilon4 allele load and age on the rates of grey matter and hippocampal volumes loss in a longitudinal cohort of 1186 healthy elderly persons. Neuroimage 2010, 53:1064-1069.
30. Cohen R.M., et al. Effect of apolipoprotein E genotype on hippocampal volume loss in aging healthy women. Neurology 2001, 57:2223-2228.
31. MacDonald S.W., et al. Trajectories of cognitive decline following dementia onset: what accounts for variation in progression?. Dement. Geriatr. Cogn. Disord. 2011, 31:202-209.
32. Bunce D., et al. APOE and cognitive decline in preclinical Alzheimer disease and non-demented aging. Neurology 2004, 63:816-821.
33. Tyler W.J., et al. From acquisition to consolidation: on the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning. Learn. Mem. 2002, 9:224-237.
34. Egan M.F., et al. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 2003, 112:257-269.
35. Kambeitz J.P., et al. Effect of BDNF val(66)met polymorphism on declarative memory and its neural substrate: a meta-analysis. Neurosci. Biobehav. Rev. 2012, 36:2165-2177.
36. Li S-C., et al. Ebbinghaus revisited: influences of the BDNF Val66Met polymorphism on backward serial recall are modulated by human aging. J. Cogn. Neurosci. 2010, 22:2164-2173.
37. Ghisletta P., et al. The Val/Met polymorphism of the brain-derived neurotrophic factor (BDNF) gene predicts decline in perceptual speed in older adults. Psychol. Aging 2014, 29:384-392.
38. Sanchez M.M., et al. BDNF polymorphism predicts the rate of decline in skilled task performance and hippocampal volume in healthy individuals. Transl. Psychiatry 2011, 1:e51.
39. Sambataro F., et al. BDNF modulates normal human hippocampal ageing. Mol. Psychiatry 2010, 15:116-118.
40. Ikeda O., et al. Effects of brain-derived neurotrophic factor (BDNF) on compression-induced spinal cord injury: BDNF attenuates down-regulation of superoxide dismutase expression and promotes up-regulation of myelin basic protein expression. J. Neuropathol. Exp. Neurol. 2002, 61:142-153.
41. Morse J.K., et al. Brain-derived neurotrophic factor (BDNF) prevents the degeneration of medial septal cholinergic neurons following fimbria transection. J. Neurosci. 1993, 13:4146-4156.
42. Lim Y.Y., et al. Effect of BDNF Val66Met on memory decline and hippocampal atrophy in prodromal Alzheimer's disease: a preliminary study. PLoS ONE 2014, 9:e86498.
43. Kennedy K.M., et al. BDNF Val66Met polymorphism influences age differences in microstructure of the corpus callosum. Front. Hum. Neurosci. 2009, 3:19.
44. Matsumoto M., et al. Catechol O-methyltransferase mRNA expression in human and rat brain: evidence for a role in cortical neuronal function. Neuroscience 2003, 116:127-137.
45. Tunbridge E.M., et al. Catechol-O-methyltransferase, cognition, and psychosis: Val158Met and beyond. Biol. Psychiatry 2006, 60:141-151.
46. Egan M.F., et al. Effect of COMT Val108/158 Met genotype on frontal lobe function and risk for schizophrenia. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:6917-6922.
47. Lotta T., et al. Kinetics of human soluble and membrane-bound catechol O-methyltransferase: a revised mechanism and description of the thermolabile variant of the enzyme. Biochemistry 1995, 34:4202-4210.
48. Nagel I.E., et al. Human aging magnifies genetic effects on executive functioning and working memory. Front. Hum. Neurosci. 2008, 2:1.
49. Störmer V.S., et al. Dopaminergic and cholinergic modulations of visual-spatial attention and working memory: insights from molecular genetic research and implications for adult cognitive development. Dev. Psychol. 2011, 48:875-889.
50. Papenberg G., et al. COMT polymorphism and memory dedifferentiation in old age. Psychol. Aging 2013, 29:347-383.
51. de Frias C.M., et al. Catechol O-methyltransferase Val158Met polymorphism is associated with cognitive performance in nondemented adults. J. Cogn. Neurosci. 2005, 17:1018-1025.
52. Josefsson M., et al. Genetic and lifestyle predictors of 15-year longitudinal change in episodic memory. J. Am. Geriatr. Soc. 2012, 60:2308-2312.
53. Sambataro F., et al. Catechol-O-methyltransferase valine(158)methionine polymorphism modulates brain networks underlying working memory across adulthood. Biol. Psychiatry 2009, 66:540-548.
54. Papenberg G., et al. Magnified effects of the COMT gene on white-matter microstructure in very old age. Brain Struct. Funct. 2014.
55. Papassotiropoulos A., et al. Common Kibra alleles are associated with human memory performance. Science 2006, 314:475-478.
56. Schneider A., et al. KIBRA: a new gateway to learning and memory?. Front. Aging Neurosci. 2010, 2:4.
57. Schuck N.W., et al. Aging and KIBRA/WWC1 genotype affect spatial memory processes in a virtual navigation task. Hippocampus 2013, 23:919-930.
58. Almeida O.P., et al. KIBRA genetic polymorphism influences episodic memory in later life, but does not increase the risk of mild cognitive impairment. J. Cell. Mol. Med. 2008, 12:1672-1676.
59. Kauppi K., et al. KIBRA polymorphism is related to enhanced memory and elevated hippocampal processing. J. Neurosci. 2011, 31:14218-14222.
60. Muse J., et al. WWC1 genotype modulates age-related decline in episodic memory function across the adult life span. Biol. Psychiatry 2014, 75:693-700.
61. Colzato L.S., et al. The genetic impact (C957T-DRD2) on inhibitory control is magnified by aging. Neuropsychologia 2013, 51:1377-1381.
62. Persson J., et al. Influences of a DRD2 polymorphism on updating of long-term memory representations and caudate BOLD activity: magnification in aging. Hum. Brain Mapp. 2014, 36:1325-1334.
63. Bäckman L., et al. Effects of working-memory training on striatal dopamine release. Science 2011, 333:718.
64. Laukka E.J., et al. Genetic effects on old-age cognitive functioning: a population-based study. Psychol. Aging 2013, 28:262-274.
65. Das D., et al. Cognitive ability, intraindividual variability, and common genetic variants of catechol-O-methyltransferase and brain-derived neurotrophic factor: a longitudinal study in a population-based sample of older adults. Psychol. Aging 2014, 29:393-403.
66. Papenberg G., et al. Dopaminergic gene polymorphisms affect long-term forgetting in old age: further support for the magnification hypothesis. J. Cogn. Neurosci. 2013, 25:571-579.
67. Greenwood P.M., et al. Healthy aging increases the cognitive effects of two genes that influence extracellular dopamine. Psychol. Aging 2014, 29:363-373.
68. Li S-C., et al. Aging magnifies the effects of dopamine transporter and D2 receptor genes on backward serial memory. Neurobiol. Aging 2012, 34:e1-e10.
69. Papenberg G., et al. Dopamine and glutamate receptor genes interactively influence episodic memory in old age. Neurobiol. Aging 2014, 35:e1213-e1218.
70. Sapkota S., et al. Synergistic associations of catechol-O-methyltransferase and brain-derived neurotrophic factor with executive function in aging are selective and modified by apolipoprotein E. Neurobiol. Aging 2015, 36:249-256.
71. Kauppi K., et al. Additive genetic effect of APOE and BDNF on hippocampus activity. Neuroimage 2014, 89:306-313.
72. Thorvaldsson V., et al. Onset and rate of cognitive change before dementia diagnosis: findings from two Swedish population-based longitudinal studies. J. Int. Neuropsychol. Soc. 2011, 17:154-162.
73. Pantzar A., et al. Interactive effects of KIBRA and CLSTN2 polymorphisms on episodic memory in old-age unipolar depression. Neuropsychologia 2014, 62:137-142.
74. Ceaser A., et al. COMT influences on prefrontal and striatal blood oxygenation level-dependent responses during working memory among individuals with schizophrenia, their siblings, and healthy controls. Cogn. Neuropsychiatry 2013, 18:257-283.
75. Kim B., et al. The effects of the catechol-O-methyltransferase val158met polymorphism on white matter connectivity in patients with panic disorder. J. Affect. Disord. 2013, 147:64-71.
76. Seok J.H., et al. Effect of the COMT val158met polymorphism on white matter connectivity in patients with major depressive disorder. Neurosci. Lett. 2013, 545:35-39.
77. Ferencz B., et al. The benefits of staying active in old age: physical activity counteracts the negative influence of PICALM, BIN1, and CLU risk alleles on episodic memory functioning. Psychol. Aging 2014, 29:440-449.
78. Erickson K.I., et al. The brain-derived neurotrophic factor Val66Met polymorphism moderates an effect of physical activity on working memory performance. Psychol. Sci. 2013, 24:1770-1779.
79. Wang H.X., et al. Education halves the risk of dementia due to apolipoprotein epsilon4 allele: a collaborative study from the Swedish brain power initiative. Neurobiol. Aging 2012, 33:e1001-e1007.
80. Vemuri P., et al. Association of lifetime intellectual enrichment with cognitive decline in the older population. JAMA Neurol. 2014, 71:1017-1024.
81. de Frias C.M., et al. Hypertension moderates the effect of APOE on 21-year cognitive trajectories. Psychol. Aging 2014, 29:431-439.
82. McFall G.P., et al. ApoE and pulse pressure interactively influence level and change in the aging of episodic memory: protective effects among epsilon2 carriers. Neuropsychology 2014, 29:388-401.
83. Raz N., et al. Genetic and vascular modifiers of age-sensitive cognitive skills: Effects of COMT, BDNF, ApoE, and hypertension. Neuropsychology 2009, 23:105-116.
84. Wersching H., et al. Impact of common KIBRA allele on human cognitive functions. Neuropsychopharmacology 2011, 36:1296-1304.
85. Whalley L.J., et al. n-3 Fatty acid erythrocyte membrane content, APOE varepsilon4, and cognitive variation: an observational follow-up study in late adulthood. Am. J. Clin. Nutr. 2008, 87:449-454.
86. Smith J.C., et al. Physical activity reduces hippocampal atrophy in elders at genetic risk for Alzheimer's disease. Front. Aging Neurosci. 2014, 6:61.
87. Wirth M., et al. Gene-environment interactions: lifetime cognitive activity, APOE genotype, and beta-amyloid burden. J. Neurosci. 2014, 34:8612-8617.
88. Sweatt J.D. The emerging field of neuroepigenetics. Neuron 2013, 80:624-632.
89. Talens R.P., et al. Epigenetic variation during the adult lifespan: cross-sectional and longitudinal data on monozygotic twin pairs. Aging Cell 2012, 11:694-703.
90. Bell J.T., Spector T.D. DNA methylation studies using twins: what are they telling us?. Genome Biol. 2012, 13:172.
91. Spiegel A.M., et al. Epigenetic contributions to cognitive aging: disentangling mindspan and lifespan. Learn. Mem. 2014, 21:569-574.
92. Deater-Deckard K., Mayr U. Cognitive change in aging: identifying gene-environment correlation and nonshared environment mechanisms. J. Gerontol. B: Psychol. Sci. Soc. Sci. 2005, 60:24-31.
93. Beam C.R., Turkheimer E. Phenotype-environment correlations in longitudinal twin models. Dev. Psychopathol. 2013, 25:7-16.