APOE4 allele disrupts resting state fMRI connectivity in the absence of amyloid plaques or decreased CSF Aβ42

Journal of Neuroscience

Volumn 30, Issue 50, 2010, Pages 17035-17040

  Sheline, Yvette I ^a   Morris, John C ^a   Snyder, Abraham Z ^a   Price, Joseph L ^a   Yan, Zhizi ^a   D'Angelo, Gina ^a   Liu, Collin ^a   Dixit, Sachin ^a   Benzinger, Tammie ^a   Fagan, Anne ^a   Goate, Alison ^a   Mintun, Mark A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; APOLIPOPROTEIN E4;

ADULT; ARTICLE; CEREBROSPINAL FLUID; COGNITION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENE DISRUPTION; HUMAN; MALE; NORMAL HUMAN; PRIORITY JOURNAL;

ALLELES; AMYLOID BETA-PEPTIDES; ANILINE COMPOUNDS; APOLIPOPROTEIN E4; BRAIN MAPPING; FEMALE; GENOTYPE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEURAL PATHWAYS; PEPTIDE FRAGMENTS; PLAQUE, AMYLOID; POSITRON-EMISSION TOMOGRAPHY; THIAZOLES;

EID: 78650371044     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3987-10.2010     Document Type: Article

References (41)

1. Blennow K, de Leon MJ, Zetterberg H (2006) Alzheimer's disease. Lancet 368:387-403.
2. Buckner RL, Snyder AZ, Shannon BJ, LaRossa G, Sachs R, Fotenos AF, Sheline YI, Klunk WE, Mathis CA, Morris JC, Mintun MA (2005) Molecular, structural, and functional characterization of Alzheimer's disease: evidence for a relationship between default activity, amyloid, and memory. J Neurosci 25:7709-7717.
3. Cairns NJ, Ikonomovic MD, Benzinger T, Storandt M, Fagan AM, Shah A, Reinwald LT, Carter D, Felton A, Holtzman DM, Mintun MA, Klunk WE, Morris JC (2009) Absence of Pittsburgh Compound B detection of cerebral amyloid beta in a patient with clinical, cognitive, and cerebrospinal fluid markers of Alzheimer disease. Arch Neurol 66:1557-1562.
4. Carmichael ST, Price JL (1996) Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol 371:179-207.
5. Cirrito JR, Deane R, Fagan AM, Spinner ML, Parsadanian M, Finn MB, Jiang H, Prior JL, Sagare A, Bales KR, Paul SM, Zlokovic BV, Piwnica-Worms D, Holtzman DM (2005) P-glycoprotein deficiency at the blood - brain barrier increases amyloid-beta deposition in an Alzheimer disease mouse model. J Clin Invest 115:3285-3290.
6. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, Roses AD, Haines JL, Pericak-Vance MA (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261:921-923.
7. Corder EH, Saunders AM, Risch NJ, Strittmatter WJ, Schmechel DE, Gaskell PC Jr, Rimmler JB, Locke PA, Conneally PM, Schmader KE (1994) Protective effect of apolipoprotein E type 2 allele for late onset Alzheimer disease. Nat Genet 7:180-184.
8. Daselaar SM, Prince SE, Cabeza R (2004) When less means more: deactivations during encoding that predict subsequent memory. Neuroimage 23:921-927.
9. Deane R, Sagare A, Hamm K, Parisi M, Lane S, Finn MB, Holtzman DM, Zlokovic BV (2008) apoE isoform-specific disruption of amyloid beta peptide clearance from mouse brain. J Clin Invest 118:4002-4013.
10. Dong LM, Wilson C, Wardell MR, Simmons T, Mahley RW, Weisgraber KH, Agard DA (1994) (1994) Human apolipoprotein E: role of arginine 61 in mediating the lipoprotein preferences of the E3 and E4 isoforms. J Biol Chem 269:22358-22365.
11. Drzezga A, Grimmer T, Henriksen G, Mühlau M, Perneczky R, Miederer I, Praus C, Sorg C, Wohlschläger A, Riemenschneider M, Wester HJ, Foerstl H, Schwaiger M, Kurz A (2009) Effect of APOE genotype on amyloid plaque load and gray matter volume in Alzheimer disease. Neurology 72:1487-1494.
12. Filippini N, MacIntosh BJ, Hough MG, Goodwin GM, Frisoni GB, Smith SM, Matthews PM, Beckmann CF, Mackay CE (2009) Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele. Proc Natl Acad Sci U S A 106:7209-7214.
13. Fleisher AS, Sherzai A, Taylor C, Langbaum JB, Chen K, Buxton RB (2009) Resting-state BOLD networks versus task-associated functional MRI for distinguishing Alzheimer's disease risk groups. Neuroimage 47:1678-1690.
14. Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700-711.
15. Fox MD, Zhang D, Snyder AZ, Raichle ME (2009) The global signal and observed anticorrelated resting state brain networks. J Neurophysiol 101:3270-3283.
16. Greicius MD, Menon V (2004) Default-mode activity during a passive sensory task: uncoupled from deactivation but impacting activation. J Cogn Neurosci 16:1484-1492.
17. Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, Sporns O (2008) Mapping the structural core of human cerebral cortex. PLoS Biol 6:e159.
18. Harris FM, Brecht WJ, Xu Q, Tesseur I, Kekonius L, Wyss-Coray T, Fish JD, Masliah E, Hopkins PC, Scearce-Levie K, Weisgraber KH, Mucke L, Mahley RW, Huang Y (2003) Carboxyl-terminal-truncated apolipoprotein E4 causes Alzheimer's disease-like neurodegeneration and behavioral deficits in transgenic mice. Proc Natl Acad Sci U S A 100:10966-10971.
19. Hatters DM, Zhong N, Rutenber E, Weisgraber KH (2006) Amino-terminal domain stability mediates apolipoprotein E aggregation into neurotoxic fibrils. J Mol Biol 361:932-944.
20. Hedden T, Van Dijk KR, Becker JA, Mehta A, Sperling RA, Johnson KA, Buckner RL (2009) Disruption of functional connectivity in clinically normal older adults harboring amyloid burden. J Neurosci 29:12686-12694.
21. Kim J, Basak JM, Holtzman DM (2009) The role of apolipoprotein E in Alzheimer's disease. Neuron 63:287-303.
22. Lustig C, Snyder AZ, Bhakta M, O'Brien KC, McAvoy M, Raichle ME, Morris JC, Buckner RL (2003) Functional deactivations: change with age and dementia of the Alzheimer type. Proc Natl Acad Sci U S A 100:14504-14509.
23. Mintun MA, Larossa GN, Sheline YI, Dence CS, Lee SY, Mach RH, Klunk WE, Mathis CA, DeKosky ST, Morris JC (2006) [11C]PIB in a nondemented population: potential antecedent marker of Alzheimer disease. Neurology 67:446-452.
24. Morris JC (1993) The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology 43:2412-2414.
25. Morris JC, Roe CM, Xiong C, Fagan AM, Goate AM, Holtzman DM, Mintun MA (2010) APOE predicts amyloid-beta but not tau Alzheimer pathology in cognitively normal aging. Ann Neurol 67:122-131.
26. Petrella JR, Wang L, Krishnan S, Slavin MJ, Prince SE, Tran TT, Doraiswamy PM (2007) Cortical deactivation in mild cognitive impairment: high-field-strength functional MR imaging. Radiology 245:224-235. (Pubitemid 47417806)
27. Price JL, Morris JC (1999) Tangles and plaques in nondemented aging and "preclinical" Alzheimer's disease. Ann Neurol 45:358-368.
28. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci U S A 98:676-682.
29. Rebeck GW, Reiter JS, Strickland DK, Hyman BT (1993) Apolipoprotein E in sporadic Alzheimer's disease: allelic variation and receptor interactions. Neuron 11:575-580.
30. Reiman EM, Chen K, Liu X, Bandy D, Yu M, Lee W, Ayutyanont N, Keppler J, Reeder SA, Langbaum JB, Alexander GE, Klunk WE, Mathis CA, Price JC, Aizenstein HJ, DeKosky ST, Caselli RJ (2009) Fibrillar amyloid-beta burden in cognitively normal people at 3 levels of genetic risk for Alzheimer's disease. Proc Natl Acad Sci U S A 106:6820-6825.
31. Sheline YI, Raichle ME, Snyder AZ, Morris JC, Head D, Wang S, Mintun MA (2010) Amyloid plaques disrupt resting state default mode network connectivity in cognitively normal elderly. Biol Psychiatry 67:584-587.
32. Shulman GL, Fiez JA, Corbetta M, Buckner RL, Miezin FM, Riachle ME, Petersen SE (1997) Common blood flow changes across visual tasks. II. Decreases in cerebral cortex. J Cogn Neurosci 9:648-663.
33. Small GW, Siddarth P, Burggren AC, Kepe V, Ercoli LM, Miller KJ, Lavretsky H, Thompson PM, Cole GM, Huang SC, Phelps ME, Bookheimer SY, Barrio JR (2009) Influence of cognitive status, age, and APOE-4 genetic risk on brain FDDNP positron-emission tomography imaging in persons without dementia. Arch Gen Psychiatry 66:81-87.
34. Sperling RA, Laviolette PS, O'Keefe K, O'Brien J, Rentz DM, Pihlajamaki M, Marshall G, Hyman BT, Selkoe DJ, Hedden T, Buckner RL, Becker JA, Johnson KA (2009) Amyloid deposition is associated with impaired default network function in older persons without dementia. Neuron 63:178-188.
35. Strittmatter WJ, Roses AD (1996) Apolipoprotein E and Alzheimer's disease. Annu Rev Neurosci 19:53-77.
36. Tiraboschi P, Hansen LA, Masliah E, Alford M, Thal LJ, Corey-Bloom J (2004) Impact of APOE genotype on neuropathologic and neurochemical markers of Alzheimer disease. Neurology 62:1977-1983.
37. Vincent JL, Snyder AZ, Fox MD, Shannon BJ, Andrews JR, Raichle ME, Buckner RL (2006) Coherent spontaneous activity identifies a hippocampal-parietal memory network. J Neurophysiol 96:3517-3531.
38. Wisniewski T, Castaño EM, Golabek A, Vogel T, Frangione B (1994) Acceleration of Alzheimer's fibril formation by apolipoprotein E in vitro. Am J Pathol 145:1030-1035.
39. Wolk DA, Dickerson BC, the Alzheimer's Disease Neuroimaging Initiative (2010) Apolipoprotein E (APOE) genotype has dissociable effects on memory and attentional-executive network function in Alzheimer's disease. Proc Natl Acad Sci U S A 107:10256-10261.
40. Xu Q, Bernardo A, Walker D, Kanegawa T, Mahley RW, Huang Y (2006) Profile and regulation of apolipoprotein E (ApoE) expression in the CNS in mice with targeting of green fluorescent protein gene to the ApoE locus. J Neurosci 26:4985-4994.
41. Zhong N, Weisgraber KH (2009) Understanding the basis for the association of apoE4 with Alzheimer's disease: opening the door for therapeutic approaches. Curr Alzheimer Res 6:415-418.