APOE mRNA and protein expression in postmortem brain are modulated by an extended haplotype structure

American Journal of Medical Genetics, Part B: Neuropsychiatric Genetics

Volumn 153, Issue 2, 2010, Pages 409-417

  Bekris, Lynn M ^a,b   Galloway, Nichole M ^a   Montine, Thomas J ^b   Schellenberg, Gerard D ^c   Yu, Chang En ^a,b  

^a VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Alzheimer's disease; APOE; Post mortem brain; TOMM40

Indexed keywords

APOLIPOPROTEIN E4; MESSENGER RNA;

AGED; ARTICLE; BRAIN REGION; CADAVER; CHROMOSOME; FEMALE; GENE STRUCTURE; GENETIC RISK; HAPLOTYPE; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; MALE; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SINGLE NUCLEOTIDE POLYMORPHISM;

AGED; AGED, 80 AND OVER; ALLELES; ALZHEIMER DISEASE; APOLIPOPROTEINS E; BRAIN; BRAIN MAPPING; FEMALE; GENE EXPRESSION REGULATION; HAPLOTYPES; HIPPOCAMPUS; HUMANS; MALE; MIDDLE AGED; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RISK;

EID: 77349123800     PISSN: 15524841     EISSN: 1552485X     Source Type: Journal    
DOI: 10.1002/ajmg.b.30993     Document Type: Article

References (48)

1. Allan CM, Walker D, Taylor JM. 1995. Evolutionary duplication of a hepatic control region in the human apolipoprotein E gene locus. Identification of a second region that confers high level and liver-specific expression of the human apolipoprotein E gene in transgenic mice. J Biol Chem 270:26278-26281.
2. Allen G, Barnard H, McColl R, Hester AL, Fields JA, Weiner MF, RingeWK, Lipton AM, Brooker M, McDonald E, Rubin CD, Cullum CM. 2007. Reduced hippocampal functional connectivity in Alzheimer disease. Arch Neurol 64:1482-1487.
3. Anandatheerthavarada HK, Biswas G, Robin MA, Avadhani NG. 2003. Mitochondrial targeting and a novel transmembrane arrest of Alzheimer's amyloid precursor protein impairs mitochondrial function in neuronal cells. J Cell Biol 161:41-54.
4. Artiga MJ, Bullido MJ, Sastre I, Recuero M, Garcia MA, Aldudo J, Vazquez J, Valdivieso F. 1998. Allelic polymorphisms in the transcriptional regulatory region of apolipoprotein E gene. FEBS Lett 421:105-108.
5. Beffert U, Cohn JS, Petit-Turcotte C, Tremblay M, Aumont N, Ramassamy C, Davignon J, Poirier J. 1999. Apolipoprotein E and beta-amyloid levels in the hippocampus and frontal cortex of Alzheimer's disease subjects are disease-related and apolipoprotein E genotype dependent. Brain Res 843:87-94.
6. BekrisLM,Millard SP, GallowayNM,Vuletic S, Albers JJ, Li G, Galasko DR, DeCarli C, Farlow MR, Clark CM, Quinn JF, Kaye JA, Schellenberg GD, Tsuang D, Peskind ER, Yu CE. 2008. Multiple SNPs within and surrounding the apolipoprotein E gene influence cerebrospinal fluid apolipoprotein E protein levels. J Alzheimers Dis 13:255-266.
7. Bertrand P, Poirier J, Oda T, Finch CE, Pasinetti GM. 1995. Association of apolipoprotein E genotype with brain levels of apolipoprotein E and apolipoprotein J (clusterin) in Alzheimer disease. Brain Res Mol Brain Res 33:174-178.
8. Bray NJ, Jehu L, Moskvina V, Buxbaum JD, Dracheva S, Haroutunian V, Williams J, Buckland PR, Owen MJ, O'Donovan MC. 2004. Allelic expression of APOE in human brain: Effects of epsilon status and promoter haplotypes. Hum Mol Genet 13:2885-2892. Epub 2004 Sep 2822.
9. Bullido MJ, Artiga MJ, Recuero M, Sastre I, Garcia MA, Aldudo J, Lendon C,Han SW, Morris JC, Frank A, Vazquez J, Goate A, Valdivieso F. 1998.A polymorphism in the regulatory region of APOE associated with risk for Alzheimer's dementia. Nat Genet 18:69-71.
10. Busciglio J, Pelsman A, Wong C, Pigino G, Yuan M, Mori H, Yankner BA. 2002. Altered metabolism of the amyloid beta precursor protein is associated with mitochondrial dysfunction in Down's syndrome. Neuron 33:677-688.
11. Cardoso SM, Santos S, Swerdlow RH, Oliveira CR. 2001. Functional mitochondria are required for amyloid beta-mediated neurotoxicity. FASEB J 15:1439-1441.
12. Casley CS, Canevari L, Land JM, Clark JB, Sharpe MA. 2002. Beta-amyloid inhibits integrated mitochondrial respiration and key enzyme activities. J Neurochem 80:91-100.
13. Cogswell JP, Ward J, Taylor IA, Waters M, Shi Y, Cannon B, Kelnar K, Kemppainen J, Brown D, Chen C, Prinjha RK, Richardson JC, Saunders AM, Roses AD, Richards CA. 2008. Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways. J Alzheimers Dis 14:27-41.
14. Coon KD, Myers AJ, Craig DW, Webster JA, Pearson JV, Lince DH, Zismann VL, Beach TG, Leung D, Bryden L, Halperin RF, Marlowe L, Kaleem M, Walker DG, Ravid R, Heward CB, Rogers J, Papassotiropoulos A, Reiman EM, Hardy J, Stephan DA. 2007.Ahigh-density wholegenome association study reveals that APOE is the major susceptibility gene for sporadic late-onset Alzheimer's disease. J Clin Psychiatry 68: 613-618.
15. Csernansky JG, Wang L, Joshi SC, Ratnanather JT, Miller MI. 2004. Computational anatomy and neuropsychiatric disease: Probabilistic assessment of variation and statistical inference of group difference, hemispheric asymmetry, and time-dependent change. Neuroimage 23:S56-S68.
16. Devi L, Prabhu BM, Galati DF, Avadhani NG, Anandatheerthavarada HK. 2006. Accumulation of amyloid precursor protein in the mitochondrial import channels of human Alzheimer's disease brain is associated with mitochondrial dysfunction. J Neurosci 26:9057-9068.
17. Filipowicz W, Bhattacharyya SN, Sonenberg N. 2008. Mechanisms of posttranscriptional regulation by microRNAs: Are the answers in sight? Nat Rev Genet 9:102-114.
18. Fukumoto H, Ingelsson M, Garevik N, Wahlund LO, Nukina N, Yaguchi Y, Shibata M, Hyman BT, Rebeck GW, Irizarry MC. 2003. APOE epsilon 3/epsilon 4 heterozygotes have an elevated proportion of apolipoprotein E4 in cerebrospinal fluid relative to plasma, independent of Alzheimer's disease diagnosis. Exp Neurol 183:249-253.
19. Glockner F, Ohm TG. 2003. Hippocampal apolipoprotein D level depends on Braak stage and APOE genotype. Neuroscience 122:103-110.
20. Hampel H, Teipel SJ, Alexander GE, Pogarell O, Rapoport SI, Moller HJ. 2002. In vivo imaging of region and cell type specific neocortical neurodegeneration in Alzheimer's disease. Perspectives of MRI derived corpus callosum measurement for mapping disease progression and effects of therapy. Evidence from studies with MRI,EEGand PET. J Neural Transm 109:837-855.
21. Hof PR, Glannakopoulos P, Bouras C. 1996. The neuropathological changes associated with normal brain aging. Histol Histopathol 11: 1075-1088.
22. Huang W, Qiu C, von Strauss E, Winblad B, Fratiglioni L. 2004. APOE genotype, family history of dementia, and Alzheimer disease risk: A 6-year follow-up study. Arch Neurol 61:1930-1934.
23. Hyman BT, Gomez-Isla T, Rebeck GW, Briggs M, Chung H, West HL, Greenberg S, Mui S, Nichols S, Wallace R, Growdon JH. 1996. Epidemiological, clinical, and neuropathological study of apolipoprotein E genotype in Alzheimer's disease. Ann NY Acad Sci 802:1-5.
24. Lambert JC, Araria-Goumidi L, Myllykangas L, Ellis C, Wang JC, Bullido MJ, Harris JM, Artiga MJ, Hernandez D, Kwon JM, Frigard B, Petersen RC, Cumming AM, Pasquier F, Sastre I, Tienari PJ, Frank A, Sulkava R, Morris JC, St Clair D, Mann DM, Wavrant-DeVrieze F, Ezquerra-TrabalonM,Amouyel P, Hardy J, HaltiaM,Valdivieso F, Goate AM,Perez-Tur J, Lendon CL, Chartier-HarlinMC.2002. Contribution of APOE promoter polymorphisms to Alzheimer's disease risk. Neurology 59:59-66.
25. Lambert JC, Berr C, Pasquier F, Delacourte A, Frigard B, Cottel D, Perez-Tur J, Mouroux V, Mohr M, Cecyre D, Galasko D, Lendon C, Poirier J, Hardy J, Mann D, Amouyel P, Chartier-Harlin MC. 1998. Pronounced impact of Th1/E47cs mutation compared with -491 AT mutation on neural APOE gene expression and risk of developing Alzheimer's disease. Hum Mol Genet 7:1511-1516.
26. Lambert JC, Perez-Tur J, Dupire MJ, Galasko D, Mann D, Amouyel P, Hardy J, Delacourte A, Chartier-Harlin MC. 1997. Distortion of allelic expression of apolipoprotein E in Alzheimer's disease. Hum Mol Genet 6:2151-2154.
27. Laws SM, Hone E, Taddei K, Harper C, Dean B, McClean C, Masters C, Lautenschlager N, Gandy SE, Martins RN. 2002. Variation at the APOE-491 promoter locus is associated with altered brain levels of apolipoprotein E. Mol Psychiatry 7:886-890.
28. Levin-Allerhand J, McEwen BS, Lominska CE, Lubahn DB, Korach KS, Smith JD. 2001. Brain region-specific up-regulation of mouse apolipoprotein E by pharmacological estrogen treatments. J Neurochem 79: 796-803.
29. Linton MF, Gish R, Hubl ST, Butler E, Esquivel C, Bry WI, Boyles JK, Wardell MR, Young SG. 1991. Phenotypes of apolipoprotein B and apolipoprotein E after liver transplantation. J Clin Invest 88: 270-281.
30. Lytle JR, Yario TA, Steitz JA. 2007. Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5′ UTR as in the 3′ UTR. Proc Natl Acad Sci USA 104:9667-9672.
31. Mahley RW, Weisgraber KH, Huang Y. 2006. Apolipoprotein E4: A causative factor and therapeutic target in neuropathology, including Alzheimer's disease. Proc Natl Acad Sci USA 103:5644-5651. Epub 2006 Mar 5627.
32. MakPA, Laffitte BA, Desrumaux C, Joseph SB, Curtiss LK, Mangelsdorf DJ, Tontonoz P, Edwards PA. 2002. Regulated expression of the apolipoprotein E/C-I/C-IV/C-II gene cluster in murine and human macrophages. A critical role for nuclear liver X receptors alpha and beta. J Biol Chem 277:31900-31908. Epub 32002 May 3 1924.
33. Manczak M, Anekonda TS, Henson E, Park BS, Quinn J, Reddy PH. 2006. Mitochondria are a direct site of A beta accumulation in Alzheimer's disease neurons: Implications for free radical generation and oxidative damage in disease progression. Hum Mol Genet 15:1437-1449. Epub 2006 Mar 1421.
34. Matsui T, Ingelsson M, Fukumoto H, Ramasamy K, Kowa H, Frosch MP, Irizarry MC, Hyman BT. 2007. Expression of APP pathway mRNAs and proteins in Alzheimer's disease. Brain Res 1161:116-123. Epub 2007 Jun 2005.
35. Mehler MF, Mattick JS. 2006. Non-coding RNAs in the nervous system. J Physiol 575:333-341.
36. Parker GR, Cathcart HM, Huang R, Lanham IS, Corder EH, Poduslo SE. 2005. Apolipoprotein gene E4 allele promoter polymorphisms as risk factors for Alzheimer's disease. Psychiatr Genet 15:271-275.
37. Pitas RE, Boyles JK, Lee SH, Foss D, Mahley RW. 1987. Astrocytes synthesize apolipoprotein Eand metabolize apolipoprotein E-containing lipoproteins. Biochim Biophys Acta 917:148-161.
38. Ramos MC, Matias S, Artiga MJ, Pozueta J, Sastre I, Valdivieso F, Bullido MJ. 2005. Neuronal specific regulatory elements in apolipoprotein E gene proximal promoter. Neuroreport 16:1027-1030.
39. Shih SJ, Allan C, Grehan S, Tse E, Moran C, Taylor JM. 2000. Duplicated downstream enhancers control expression of the human apolipoprotein Egene in macrophages and adipose tissue. J BiolChem275:31567-31572.
40. Simonet WS, Bucay N, Lauer SJ, Taylor JM. 1993. A far-downstream hepatocyte-specific control region directs expression of the linkedhuman apolipoprotein E and C-I genes in transgenic mice. J Biol Chem 268: 8221-8229.
41. Sluimer JD, Vrenken H, Blankenstein MA, Fox NC, Scheltens P, Barkhof F, van der Flier WM. 2008. Whole-brain atrophy rate in Alzheimer disease: Identifying fast progressors. Neurology 70:1836-1841.
42. Town T, Paris D, Fallin D, Duara R, BarkerW, Gold M, Crawford F, Mullan M. 1998. The -491A/T apolipoprotein E promoter polymorphism association with Alzheimer's disease: Independent risk and linkage disequilibrium with the known APOE polymorphism. Neurosci Lett 252:95-98.
43. Xu PT, Gilbert JR, Qiu HL, Ervin J, Rothrock-Christian TR, Hulette C, Schmechel DE. 1999. Specific regional transcription of apolipoprotein E in human brain neurons. Am J Pathol 154:601-611.
44. Xu PT, Gilbert JR, Qiu HL, Rothrock-Christian T, Settles DL, Roses AD, Schmechel DE. 1998. Regionally specific neuronal expression of human APOE gene in transgenic mice. Neurosci Lett 246:65-68.
45. Yamagata K, Urakami K, Ikeda K, Ji Y, Adachi Y, Arai H, Sasaki H, Sato K, Nakashima K. 2001. High expression of apolipoprotein E mRNA in the brains with sporadic Alzheimer's disease. Dement Geriatr Cogn Disord 12:57-62.
46. Yu CE, Devlin B, Galloway N, Loomis E, Schellenberg GD. 2004. ADLAPH: A molecular haplotyping method based on allele-discriminating longrange PCR. Genomics 84:600-612.
47. Yu CE, Seltman H, Peskind ER, Galloway N, Zhou PX, Rosenthal E, Wijsman EM, Tsuang DW, Devlin B, Schellenberg GD. 2007. Comprehensive analysis of APOE and selected proximate markers for late-onset Alzheimer's disease: Patterns of linkage disequilibrium and disease/marker association. Genomics 89:655-665. Epub 2007 Apr 2016.
48. Zheng P, Pennacchio LA, Le Goff W, Rubin EM, Smith JD. 2004. Identification of a novel enhancer of brain expression near the apoE gene cluster by comparative genomics. Biochim Biophys Acta 1676:41-50.