Alzheimer's disease susceptibility genes APOE and TOMM40, and hippocampal volumes in the Lothian Birth Cohort 1936

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Lyall, Donald M ^a   Royle, Natalie A ^a   Harris, Sarah E ^a   Bastin, Mark E ^a   Maniega, Susana Muñoz ^a   Murray, Catherine ^a   Lutz, Michael W ^b   Saunders, Ann M ^b   Roses, Allen D ^b,c   Del Valdés Hernández, Maria C ^a   Starr, John M ^a   Porteous, David J ^a   Wardlaw, Joanna M ^a   Deary, Ian J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c Zinfandel Pharmaceuticals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; CARRIER PROTEIN; TOMM40 PROTEIN, HUMAN;

AGED; ALZHEIMER DISEASE; FEMALE; GENE FREQUENCY; GENETIC PREDISPOSITION; GENETICS; GENOTYPE; HIPPOCAMPUS; HUMAN; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; ORGAN SIZE; PATHOLOGY;

AGED; ALZHEIMER DISEASE; APOLIPOPROTEINS E; FEMALE; GENE FREQUENCY; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MEMBRANE TRANSPORT PROTEINS; ORGAN SIZE;

EID: 84894034271     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080513     Document Type: Article

References (65)

1. Potkin SG, Guffanti G, Lakatos A, Turner JA, Kruggel F et al. (2009) Hippocampal atrophy as a quantitative trait in a genome-wide association study identifying novel susceptiblity genes for Alzheimer's disease. PLOS ONE 1. doi:10.1371/journal.pone.0006501.
2. Lind J, Larsson A, Persson J, Ingvar M, Nilsson LG et al. (2006) Reduced hippocampal volume in non-demented carriers of the apolipoprotein e4: relation to chronological age and recognition memory. Neurosci Lett 396: 23-27. doi:10.1016/j.neulet.2005.11.070. PubMed: 16406347. (Pubitemid 43233781)
3. Roses AD, Lutz MW, Amrine-Madsen H, Saunders AM, Crenshaw DG et al. (2010) A TOMM40 variable-length polymorphism predicts the age of late-onset Alzheimer's disease. Pharmacogenomics J 10: 375-384. doi:10.1038/tpj.2009.69. PubMed: 20029386.
4. NCBI APOE. information (2012). Available http://www.ncbi.nlm.nih.gov/ gene/348. Accessed 26.08.2012.
5. Ringman JM, Cummings JL (2009) The Genetic Basis for the Cognitive Deterioration of Alzheimer's Disease. In: D Goldberg te Weinberger. The Genetics of Cognitive Neuroscience. Massachusetts: MIT Press. pp. 221-244.
6. Eisenberg DTA, Kazuwa CW, Hayes MG (2010) Worldwide Allele Frequencies of the Human Apolipoprotein E Gene: Climate, Local Adaptations and Evolutionary History. Am J Phys Anthropol 143: 100-111. doi:10.1002/ajpa.21298. PubMed: 20734437.
7. Bu G (2009) Apolipoprotein E and its receptors in Alzheimer's disease: pathways, pathogenesis and therapy. Nat Neurosci 10: 333-344. doi:10.1038/ni.1713.
8. Wisdom NM, Callahan JL, Hawkins KA (2011) The effects of apolipoprotein E on non-impaired cognitive functioning: a meta-analysis. Neurobiol Aging 32: 63-74. doi:10.1016/j.neurobiolaging.2009.02.003. PubMed: 19285755.
9. Deary IJ, Whiteman MC, Pattie A, Starr JM, Hayward C et al. (2004) Apolipoprotein E Gene Variability and Cognitive Functions at Age 79: A Follow-Up of the Scottish Mental Survey of 1932. Psychol Aging 19: 367-371. doi:10.1037/0882-7974.19.2.367. PubMed: 15222832. (Pubitemid 38720884)
10. Corder EH, Saunders AM, Risch NJ, Strittmatter WJ, Schmechel DE et al. (1994) Protective effect of apolipoprotein-E type 2 allele for late onset Alzheimer disease. Nat Genet 7: 180-184. doi:10.1038/ng0694-180. PubMed: 7920638. (Pubitemid 24174658)
11. Martins IJ, Hone E, Foster JK, Sünram-Lea SI, Gnjec A et al. (2006) Apolipoprotein E, cholesterol metabolism, diabetes, and the convergence of risk factors for Alzheimer's disease and cardiovascular disease. Mol Psychiatry 11: 721-736. doi:10.1038/sj.mp.4001854. PubMed: 16786033. (Pubitemid 44141805)
12. Hardy JA, Higgins GA (1992) Alzheimer's disease: The amyloid cascade hypothesis. Science 256: 184-185. doi:10.1126/science.1566067. PubMed: 1566067.
13. Erkinjuntti T (2007) Acute Stroke Management: Brain Protection, Vascular Cognitive Deterioration and Stroke. Brain 24: 189-194.
14. De La Torre JCD (2010) Vascular risk factor detection and control may prevent Alzheimer's disease. Ageing Res Rev 9: 218-225. doi:10.1016/j.arr.2010. 04.002. PubMed: 20385255.
15. NCBI. TOMM40 information (2012). Available http://www.ncbi.nlm.nih.gov/ gene/10452. Accessed 26.08.2012.
16. Takei N, Miyashita A, Tsukie T, Arai H, Asada T et al. (2009) Genetic association study on in and around the APOE in late-onset Alzheimer disease in Japanese. Genomics 93: 441-448. doi:10.1016/j.ygeno.2009.01.003. PubMed: 19442637.
17. Humphries AD, Streimann IC, Stojanovski D, Johnston AJ, Yano M et al. (2005) Dissection of the Mitochondrial Import and Assembly Pathway for Human Tom40. J Biol Chem 280: 11535: 11535-43-11543. PubMed: 15644312
18. Koehler CM, Merchant S, Schatz G (1999) How membrane proteins travel across the mitochondrial intermembrane space. Trends Biochem Sci 24: 428-432. doi:10.1016/S0968-0004(99)01462-0. PubMed: 10542408. (Pubitemid 29528202)
19. Swerdlow RH, Khan SM (2004) A "mitochondrial cascade hypothesis" for sporadic Alzheimer's disease. Med Hypotheses 63: 8-20. doi:10.1016/j.mehy.2003.12.045. PubMed: 15193340. (Pubitemid 38887104)
20. Bekris LM, Lutz F, Yu CE (2012) Functional analysis of APOE locus genetic vairation implicates regional enhancers in the regulation of both TOMM40 and APOE. J Hum Genet 57: 18-25. doi:10.1038/jhg.2011.123. PubMed: 22089642.
21. Lutz MW, Crenshaw DG, Saunders AM, Roses AD (2010) Genetic variation at a single locus and age of onset for Alzheimer's Disease. Alzheimers Dement 6: 125-131. doi:10.1016/j.jalz.2010.01.011. PubMed: 20298972.
22. Cruchaga C, Nowotny P, Kauwe JSK, Ridge PG, Mayo K et al. (2011) Association and expression analyses with single-nucleotide polymorphisms in TOMM40 in Alzheimer disease. Arch Neurol 68: 1013-1019. doi:10.1001/archneurol. 2011.155. PubMed: 21825236.
23. Bruno D, Nierenberg JJ, Ritchie JC, Lutz MW, Pomara N et al. (2011) Cerebrospinal fluid cortisol concentrations in healthy elderly are affected by both APOE and TOMM40 variants. Psychoneuroendocrino 37: 366-371. PubMed: 21803501.
24. Schiepers OJG, Harris SE, Gow AJ, Pattie A, Brett CE et al. (2012) APOE ε4 status predicts age-related cognitive decline in the ninth decade: longitudinal follow-up of the Lothian Birth Cohort 1921. Mol Psychiatry 17: 315-324. doi:10.1038/mp.2010.137. PubMed: 21263443.
25. Braak H, Braak E (1991) Neuropathological staging of Alzheimer-related changes. Acta Neuropathol 82: 239-259. doi:10.1007/BF00308809. PubMed: 1759558.
26. Amaral DL, Lavenex P (2006) Hippocampal Neuroanatomy. In: P AndersenR MorrisD AmaralT BlissJ O'Keefe. The Hippocampus Book. Oxford: Oxford University Press. pp. 37-110.
27. Duvernoy HM (2006) The Human Hippocampus: An Atlas of Applied Anatomy. Berlin: Springer-Verlag. pp.39-73.
28. Braak H, Braak E (1995) Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiol Aging 16: 271-278. doi:10.1016/0197-4580(95) 00021-6. PubMed: 7566337.
29. Ohm TG, Muller H, Braak H (1995) Apolipoprotein e polymorphism influences not only cerebral senile plaque load but also Alzheimer-type neurofibrillary tangle formation. Neuroscience 66: 583-587. doi:10.1016/0306-4522(94)00596-W. PubMed: 7644022.
30. Simic G, Kostovic I, Winblad BB (1997) Volume and number of neurons in the human hippocampal formation in Alzheimers disease. J Comp Neurol 379: 428-494. doi:10.1002/(SICI)1096-9861(19970317)379:3. PubMed: 9067834.
31. Price JL, Morris JC (1999) Tangles and plaques in nondemented aging and 'preclinical' Alzheimer's disease. Ann Neurol 45: 358-368. doi:10.1002/1531- 8249(199903)45:3. PubMed: 10072051. (Pubitemid 29120041)
32. Plassman BL, Welsh-Bohmer KA, Bigler ED, Johnson SC, Anderson CV et al. (1997) Apolipoprotein E ε4 allele and hippocampal volume in twins with normal cognition. Neurology 48: 985-992. doi:10.1212/WNL.48.4.985. PubMed: 9109888.
33. Richter-Schmidinger T, Alexopoulos P, Horn M, Maus S, Reichel M et al. (2011) Influence of brain-derived neurotrophic-factor and apolipoprotein E genetic variants on hippocampal volume and memory performance in healthy young adults. J Neural Transm 118: 249-257. doi:10.1007/s00702-010-0539-8. PubMed: 21190051.
34. Jak AJ, Houston WS, Nagel BJ, Corey-Bloom J, Bondi WM (2007) Differential cross-sectional and longutdinal impact of APOE genotype on hippocampal volmes in nondemented older adults. Dement Geriatr Cogn 23: 382-389. doi:10.1159/000101340. (Pubitemid 46897174)
35. Tupler LA, Krishnan KRR, Greenberg DL, Marcovina SM, Payne ME et al. (2007) Predicting memory decline in normal elderly: Genetics, MRI and cognitive reserve. Neurobiol Aging 28: 1644-1656. doi:10.1016/j.neurobiolaging.2006.07. 001. PubMed: 16916565. (Pubitemid 47384943)
36. Chiang GC, Insel PS, Tosun D, Schuff N, Truran-Sacrey D et al. (2011) Hippocampal atrophy rates and CSF biomarkers in elderly APOE e2 normal subjects. Neurology 75: 1976-1984.
37. Lemaître H, Crivello F, Dufouil CG, Grassiot B, Tzourio C et al. (2005) No ε4 gene dose effect on hippocampal atrophy in large MRI database of healthy elderly subjects. NeuroImage 24: 1205-1213. doi:10.1016/j.neuroimage. 2004.10.016. PubMed: 15670698. (Pubitemid 40164522)
38. Den Heijer T, Oudkerk M, Launer LJ, van Duijn CM, Hofman A et al. (2002) Hippocampal, amygdalar, and global brain atrophy in different apiloprotein e genotypes. Neurology 59: 746-748. doi:10.1212/WNL.59.5.746. PubMed: 12221169.
39. Cherbuin N, Anstey KJ, Sachdev PS, Maller JJ, Mack HA et al. (2008) Total and Regional Gray Matter Volume is Not Related to APOE e4 Status in a Community Sample of Middle-Aged Individuals. J Gerontol 63A: 501-504.
40. Panizzon MS, Hauger R, Dale AM, Eaves LJ, Eyler LT et al. (2010) Testosterone modifies the effect of APOE genotype on hippocampal volume in middle-aged men. Neurology 75: 874-880. doi:10.1212/WNL.0b013e3181f11deb. PubMed: 20819998.
41. Ferencz B, Laukka EJ, Lovdén M, Kalpouzos G, Keller L et al. (2013) The influence of APOE and TOMM40 polymorphisms on hippocampal volume and episodic memory in old age. FNHUM 7. doi:10.3389/fnhum.2013.00198.
42. Hostage C, Choudhurt KR, Doraiswamy PM, Petrella J, for the Alzheimers Disease Neuroimaging Initiative (2013) Dissecting the Gene Dose-Effects of the APOE ε4 and ε2 Alleles on Hippocampal Volumes in Aging and Alzheimer's Disease. PLOS ONE 8 : doi:10.1371/journal.pone.0054483.
43. Johnson SC, Rue A, Hermann BP, Xu G, Koscik RL et al. (2011) The effect of TOMM40 poly-T length on gray matter volume and cognition in middle-aged persons with APOE ε3/ε3 genotype. Alzheimers Dement 7: 456-465. doi:10.1016/j.jalz.2011.05.1319. PubMed: 21784354.
44. Stein JL, Medland SE, Vasquez AA, Hibar DP, Senstad RE et al. (2012) Identification of common variants associated with human hippocampal and intracranial volumes. Nat Genet 44: 552-561. doi:10.1038/ng.2250. PubMed: 22504417.
45. Deary ID, Gow AJ, Taylor MD, Corley J, Brett C et al. (2007) The Lothian Birth Cohort 1936: a study to examine influences on cognitive ageing from age 11 to age 70 and beyond. BMC Geriatr 7: 1-12. doi:10.1186/1471-2318-7-1. PubMed: 17222340.
46. Council Scottishfor Research in Education (1949) The trend of Scottish intelligence: A comparison of the 1947 and 1932 surveys of the intelligence of eleven-year-old pupils. London, UK: University of London Press.
47. Deary IJ, Gow AJ, Pattie A, Starr JM (2012) Cohort Profile: The Lothian Birth Cohorts of 1921 and 1936. Int J Epidemiol 41: 1576-84. doi:10.1093/ije/dyr19. PubMed: 22253310.
48. Wardlaw JM, Bastin ME, Hernandez MV, Munoz-Maniega S, Royle NA et al. (2011) Brain Ageing, Cognition in Youth and Old Age, and Vascular Disease in the Lothian Birth Cohort 1936: Rationale, Design and Methodology of the Imaging Protocol. Int J Stroke 6: 547-559. doi:10.1111/j.1747-4949.2011.00683.x. PubMed: 22111801.
49. Folstein MF, Folstein SE, McHugh PR (1975) "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12: 189-198. doi:10.1016/0022-3956(75)90026-6. PubMed: 1202204.
50. Linnertz C, Saunders AM, Lutz MW, Crenshaw DM, Grossman I et al. (2012) Characterization of the Poly-T Variant in the TOMM40 Gene in Diverse Populations. PLOS-ONE 7: e30994. doi:10.1371/journal.pone.0030994. PubMed: 22359560.
51. Hardy-weinberg calculator website (2012). Available http://www.had2know. com/academics/hardy-weinberg-equilibrium-calculator-3-alleles.html. Accessed 26.08.2012.
52. Free SL, Bergin PS, Fish DR, Cook MJ, Shorvon SD et al. (1995) Methods for Normalization of Hippocampal Volumes Measured with MR. AJNR Am J Neuroradiol 16: 637-643. PubMed: 7611015.
53. Van Petten C (2004) Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: review and meta-analysis. Neuropsychologia 42: 1394-1413. doi:10.1016/j.neuropsychologia.2004.04.006. PubMed: 15193947.
54. Arndt S, Cohen G, Alliger RJ, Swayze VW, Andreasen NC (1991) Problems with Ratio and Proportion Measures of Imaged Cerebral Structures. Psychiat ResNeuroim 40: 79-89. doi:10.1016/0925-4927(91)90031-K. PubMed: 1946842.
55. Garcia-Berthou E (2001) On the Misuse of Residuals in Ecology: Testing Regression Residuals vs. the Analysis of Covariance. J Anim Ecol 70: 708-711. doi:10.1046/j.1365-2656.2001.00524.x.
56. Luciano M, Gow AJ, Taylor MD, Hayward C, Harris SE et al. (2009) Apolipoprotein E is not Related to Memory Abilities at 70 Years of Age. Behav Genet 39: 6-14. doi:10.1007/s10519-008-9236-x. PubMed: 18946731.
57. Devi L, Prabhu BM, Galati DF, Avadhani NG, Anandatheerthavarada HK (2006) Accumulation of Amlyoid Precursor Protein in the Mitochondrial Import Channels of Human Alzheimer's Disease Brain is Associated with Mitochondrial Dysfunction. J Neurosci 26: 9057-9068. doi:10.1523/JNEUROSCI.1469-06.2006. PubMed: 16943564. (Pubitemid 44319397)
58. Caselli RJ, Dueck AC, Huentelman MJ, Lutz WM, Saunders AM et al. (2012) Longitudinal modeling of cognitive aging and the TOMM40 effect. Alzheimers Dement 8: 490-495. doi:10.1016/j.jalz.2012.05.1328. PubMed: 23102119.
59. deToledo-Morrell L, Stoub TR, Bulgakova M, Wilson RS, Bennett DA et al. (2004) MRI-derived entorhinal volume is a good predictor of conversion from MCI to AD. Neurobiol Aging 25: 1197-1203. doi:10.1016/j.neurobiolaging.2003.12.007. PubMed: 15312965. (Pubitemid 39094022)
60. MacLullich AMJ, Ferguson KJ, Deary IJ, Seckl JR, Starr JM et al. (2002) Intracranial capacity and brain volumes are associated with cognition in healthy elderly men. Neurology 59: 169-174. doi:10.1212/WNL.59.2.169. PubMed: 12136052. (Pubitemid 34779172)
61. Rushton JP, Ankney C (1996) Brain size and cognitive ability: correlations with age, sex, social class and race. Psychon B Rev 3: 21-36. doi:10.3758/BF03210739. (Pubitemid 126421494)
62. Shenkin SD, Rivers CS, Deary IJ, Starr JM, Wardlaw JM (2009) Maximum (prior) brain size, not atrophy, correlates with cognition in community-dwelling old people: a cross-sectional neuroimaging study. BMC Geriatr 9; Retrieved onpublished at whilst December year 1111 from . doi:10.1186/1471-2318-9-12
63. Raji CA, Lopez OL, Kuller LH, Carmichael OT, Longstreth WT Jnr et al. (2012) White matter lesions and brain gray matter volume in cognitively normal elders. Neurobiol Aging 33: 834: e7-16. PubMed: 21943959.
64. Hedskog L, Brohede J, Wiehager B, Pinho CM, Revathikumar P et al. (2012) Biochemical Studies of Poly-T Variants in the Alzheimer's Disease Associated TOMM40 Gene. J Alzheimers Dis 31: 527-536. PubMed: 22596268.
65. Devanand DP, Bansal R, Liu J, Hao X, Pradhaban G et al. (2012) MRI hippocampal and entorhinal cortex mapping in predicting conversion to Alzheimer's disease. NeuroImage 60: 1622-1629. doi:10.1016/j.neuroimage.2012.01. 075. PubMed: 22289801.