Integrated late onset Alzheimer's disease (LOAD) susceptibility genes: Cholesterol metabolism and trafficking perspectives

Gene

Volumn 597, Issue , 2017, Pages 10-16

  Dong, Hee Kim ^a,b   Gim, Jeong An ^a   Yeo, Seung Hyeon ^c   Kim, Heui Soo ^a  

^a Pusan National University   (South Korea)

^b Hyung Ju Hospital   (South Korea)

^c Pusan National University Yangsan Hospital   (South Korea)

Author keywords

Alzheimer's disease; brain; cholesterol metabolism; GWAS; LOAD

Indexed keywords

AMYLOID BETA PROTEIN; APOLIPOPROTEIN E; BIN1 PROTEIN; CHOLESTEROL; CLUSTERIN; LOW DENSITY LIPOPROTEIN RECEPTOR; PICALM PROTEIN; PROTEIN; SORL1 PROTEIN; UNCLASSIFIED DRUG; APOE PROTEIN, HUMAN; BIN1 PROTEIN, HUMAN; CARRIER PROTEIN; CLATHRIN ASSEMBLY PROTEIN; CLU PROTEIN, HUMAN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; NUCLEAR PROTEIN; PICALM PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SORL1 PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

ALZHEIMER DISEASE; CHOLESTEROL METABOLISM; EPIGENETICS; GENE EXPRESSION; GENE INTERACTION; GENETIC RISK; GENETIC SUSCEPTIBILITY; GENOME-WIDE ASSOCIATION STUDY; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; BRAIN; EPISTASIS; GENETIC PREDISPOSITION; GENETICS; METABOLISM; PROTEIN ANALYSIS; TRANSPORT AT THE CELLULAR LEVEL;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; APOLIPOPROTEINS E; BIOLOGICAL TRANSPORT; BRAIN; CHOLESTEROL; CLUSTERIN; EPISTASIS, GENETIC; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; LDL-RECEPTOR RELATED PROTEINS; MEMBRANE TRANSPORT PROTEINS; MONOMERIC CLATHRIN ASSEMBLY PROTEINS; NUCLEAR PROTEINS; PROTEIN INTERACTION MAPPING; TUMOR SUPPRESSOR PROTEINS;

EID: 85001070143     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2016.10.022     Document Type: Review

References (96)

1. Allen, M., et al. Novel late-onset Alzheimer disease loci variants associate with brain gene expression. Neurology 79 (2012), 221–228.
2. Bai, F., Yuan, Y., Shi, Y., Zhang, Z., Multiple genetic imaging study of the association between cholesterol metabolism and brain functional alterations in individuals with risk factors for Alzheimer's disease. Oncotarget 7 (2016), 15315–15328.
3. Baig, S., et al. Distribution and expression of picalm in Alzheimer disease. J. Neuropathol. Exp. Neurol. 69 (2010), 1071–1077.
4. Barral, S., et al. Genotype patterns at PICALM, CR1, BIN1, CLU, and APOE genes are associated with episodic memory. Neurology 78 (2012), 1464–1471.
5. Bartl, M.M., et al. Multiple receptors mediate apoJ-dependent clearance of cellular debris into nonprofessional phagocytes. Exp. Cell Res. 271 (2001), 130–141.
6. Belbin, O., et al. Regulatory region single nucleotide polymorphisms of the apolipoprotein E gene and the rate of cognitive decline in Alzheimer's disease. Hum. Mol. Genet. 16 (2007), 2199–2208.
7. Bell, R.D., et al. Transport pathways for clearance of human Alzheimer's amyloid β-peptide and apolipoproteins E and J in the mouse central nervous system. J. Cereb. Blood Flow Metab. 27 (2007), 909–918.
8. Bertram, L., Tanzi, R., The genetics of Alzheimer's disease. Prog. Mol. Biol. Transl. Sci. 107 (2012), 79–100.
9. Bertram, L., et al. Systematic meta-analyses of Alzheimer disease genetic association studies: the AlzGene database. Nat. Genet. 39 (2007), 17–23.
10. Bertram, L., et al. Genome-wide association analysis reveals putative Alzheimer's disease susceptibility loci in addition to APOE. Am. J. Hum. Genet. 83 (2008), 623–632.
11. Biffi, A., et al. Genetic variation and neuroimaging measures in Alzheimer disease. Arch. Neurol. 67 (2010), 677–685.
12. Bruni, A.C., Conidi, M.E., Bernardi, L., Genetics in degenerative dementia: current status and applicability. Alzheimer Dis. Assoc. Disord. 28 (2014), 199–205.
13. Bu, G., Apolipoprotein E and its receptors in Alzheimer's disease: pathways, pathogenesis and therapy. Nat. Rev. Neurosci. 10 (2009), 333–344.
14. Buckner, R.L., et al. Molecular, structural, and functional characterization of Alzheimer's disease: evidence for a relationship between default activity, amyloid, and memory. J. Neurosci. 25 (2005), 7709–7717.
15. Buckner, R.L., Andrews-Hanna, J.R., Schacter, D.L., The brain's default network. Ann. N. Y. Acad. Sci. 1124 (2008), 1–38.
16. Calero, M., et al. Functional and structural properties of lipid-associated apolipoprotein J (clusterin). Biochem. J. 344 (1999), 375–383.
17. Chao, L.L., et al. Deficits in cognitive flexibility are associated with APOE-E4 allele and precuneus volume and thickness in nondemented older adults. Alzheimers Dement. 6 (2010), S441–S442.
18. Chapuis, J., et al. Increased expression of BIN1 mediates Alzheimer genetic risk by modulating tau pathology. Mol. Psychiatry 18 (2013), 1225–1234.
19. Chibnik, L.B., et al. Alzheimer's loci: epigenetic associations and interaction with genetic factors. Ann. Clin. Transl. Neurol. 2 (2015), 636–647.
20. de Lange, E.C., Potential role of ABC transporters as a detoxification system at the blood–CSF barrier. Adv. Drug Deliv. Rev. 56 (2004), 1793–1809.
21. Deane, R., et al. LRP/amyloid β-peptide interaction mediates differential brain efflux of Aβ isoforms. Neuron 43 (2004), 333–344.
22. Deane, R., et al. ApoE isoform–specific disruption of amyloid β peptide clearance from mouse brain. J. Clin. Invest. 118 (2008), 4002–4013.
23. Di Paolo, G., Kim, T.-W., Linking lipids to Alzheimer's disease: cholesterol and beyond. Nat. Rev. Neurosci. 12 (2011), 284–296.
24. Dodson, S.E., et al. Loss of LR11/SORLA enhances early pathology in a mouse model of amyloidosis: evidence for a proximal role in Alzheimer's disease. J. Neurosci. 28 (2008), 12877–12886.
25. Donahue, J.E., et al. RAGE, LRP-1, and amyloid-beta protein in Alzheimer's disease. Acta Neuropathol. 112 (2006), 405–415.
26. Eisenstein, M., Genetics: finding risk factors. Nature 475 (2011), S20–S22.
27. Fennema-Notestine, C., et al. Presence of ApoE ε4 allele associated with thinner frontal cortex in middle age. J. Alzheimers Dis. 26 (2011), 49–60.
28. Furuya, T.K., SORL1 and SIRT1 mRNA expression and promoter methylation levels in aging and Alzheimer's Disease. Neurochem. Int. 61 (2012), 973–975.
29. Gaiteri, C., et al. Genetic variants in Alzheimer disease - molecular and brain network approaches. Nat. Rev. Neurol. 12 (2016), 413–427.
30. Gatz, M., et al. Role of genes and environments for explaining Alzheimer disease. Arch. Gen. Psychiatry 63 (2006), 168–174.
31. Gong, J.-S., et al. Apolipoprotein E (ApoE) isoform-dependent lipid release from astrocytes prepared from human ApoE3 and ApoE4 knock-in mice. J. Biol. Chem. 277 (2002), 29919–29926.
32. Guerreiro, R., Hardy, J., Genetics of Alzheimer's Disease. Neurotherapeutics 11 (2014), 732–737.
33. Guerreiro, R., Brás, J., Hardy, J., SnapShot: genetics of Alzheimer's disease. Cell, 155, 2013, 968, e1.
34. Guye, M., Bettus, G., Bartolomei, F., Cozzone, P.J., Graph theoretical analysis of structural and functional connectivity MRI in normal and pathological brain networks. Magn. Reson. Mat. Phys. Biol. Med. 23 (2010), 409–421.
35. Hardy, J., Selkoe, D.J., The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297 (2002), 353–356.
36. Harold, D., et al. Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease. Nat. Genet. 41 (2009), 1088–1093.
37. Herz, J., Bock, H.H., Lipoprotein receptors in the nervous system. Annu. Rev. Biochem. 71 (2002), 405–434.
38. Herz, J., Strickland, D.K., LRP: a multifunctional scavenger and signaling receptor. J. Clin. Invest. 108 (2001), 779–784.
39. Hohman, T.J., et al. Discovery of gene-gene interactions across multiple independent data sets of late onset Alzheimer disease from the Alzheimer Disease Genetics Consortium. Neurobiol. Aging 38 (2016), 141–150.
40. Hollingworth, P., et al. Common variants at ABCA7, MS4A6A/MS4A4E, EPHA1, CD33 and CD2AP are associated with Alzheimer's disease. Nat. Genet. 43 (2011), 429–435.
41. Holtzman, D.M., Herz, J., Bu, G., Apolipoprotein E and apolipoprotein E receptors: normal biology and roles in Alzheimer disease. Cold Spring Harb. Perspect. Med., 2, 2012, a006312.
42. Jarrett, J.T., Berger, E.P., Lansbury, P.T. Jr., The carboxy terminus of the. beta. amyloid protein is critical for the seeding of amyloid formation: Implications for the pathogenesis of Alzheimer's disease. Biochemistry 32 (1993), 4693–4697.
43. Jones, R., et al. Collaborative research between academia and industry using a large clinical trial database: a case study in Alzheimer's disease. Trials, 12, 2011, 1.
44. Jun, G., et al. Meta-analysis confirms CR1, CLU, and PICALM as Alzheimer disease risk loci and reveals interactions with APOE genotypes. Arch. Neurol. 67 (2010), 1473–1484.
45. Kanekiyo, T., et al. LRP1 in brain vascular smooth muscle cells mediates local clearance of Alzheimer's amyloid-β. J. Neurosci. 32 (2012), 16458–16465.
46. Kanekiyo, T., Xu, H., Bu, G., ApoE and Aβ in Alzheimer's disease: Accidental encounters or partners?. Neuron 81 (2014), 740–754.
47. Karch, C.M., Cruchaga, C., Goate, A.M., Alzheimer's disease genetics: from the bench to the clinic. Neuron 83 (2014), 11–26.
48. Kiddle, S.J., et al. Candidate blood proteome markers of Alzheimer's disease onset and progression: a systematic review and replication study. J. Alzheimers Dis. 38 (2014), 515–531.
49. Kim, J., Basak, J.M., Holtzman, D.M., The role of apolipoprotein E in Alzheimer's disease. Neuron 63 (2009), 287–303.
50. Kim, D.H., et al. Genetic markers for diagnosis and pathogenesis of Alzheimer's disease. Gene 545 (2014), 185–193.
51. Koch, W., et al. Diagnostic power of default mode network resting state fMRI in the detection of Alzheimer's disease. Neurobiol. Aging 33 (2012), 466–478.
52. Lambert, J.-C., et al. Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease. Nat. Genet. 41 (2009), 1094–1099.
53. Lambert, J.-C., et al. Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer's disease. Nat. Genet. 45 (2013), 1452–1458.
54. Li, J., et al. Differential regulation of amyloid-β endocytic trafficking and lysosomal degradation by apolipoprotein E isoforms. J. Biol. Chem. 287 (2012), 44593–44601.
55. Ling, I.-F., et al. Genetics of clusterin isoform expression and Alzheimer's disease risk. PLoS One, 7, 2012, e33923.
56. Liu, G., et al. BIN1 gene rs744373 polymorphism contributes to Alzheimer's disease in East Asian population. Neurosci. Lett. 544 (2013), 47–51.
57. Liu, G., et al. PICALM Gene rs3851179 Polymorphism Contributes to Alzheimer's Disease in an Asian Population. Neruomol. Med. 15 (2013), 384–388.
58. Loison, F., et al. Up-regulation of the clusterin gene after proteotoxic stress: implication of HSF1–HSF2 heterocomplexes. Biochem. J. 395 (2006), 223–231.
59. Mawuenyega, K.G., et al. Decreased clearance of CNS β-amyloid in Alzheimer's disease. Science, 330, 2010, 1774.
60. Morgen, K., et al. Genetic interaction of PICALM and APOE is associated with brain atrophy and cognitive impairment in Alzheimer's disease. Alzheimers Dement. 10 (2014), S269–S276.
61. Naj, A.C., et al. Common variants at MS4A4/MS4A6E, CD2AP, CD33 and EPHA1 are associated with late-onset Alzheimer's disease. Nat. Genet. 43 (2011), 436–441.
62. Nuutinen, T., et al. Induction of clusterin/apoJ expression by histone deacetylase inhibitors in neural cells. Neurochem. Int. 47 (2005), 528–538.
63. Pant, S., et al. AMPH-1/Amphiphysin/Bin1 functions with RME-1/Ehd1 in endocytic recycling. Nat. Cell Biol. 11 (2009), 1399–1410.
64. Parikh, I., Fardo, D.W., Estus, S., Genetics of PICALM expression and Alzheimer's disease. PLoS One, 9, 2014, e91242.
65. Pietrzik, C.U., Jaeger, S., Functional role of lipoprotein receptors in Alzheimer's disease. Curr. Alzheimer Res. 5 (2008), 15–25.
66. Raj, T., et al. Alzheimer disease susceptibility loci: evidence for a protein network under natural selection. Am. J. Hum. Genet. 90 (2012), 720–726.
67. Rauhala, H.E., et al. Clusterin is epigenetically regulated in prostate cancer. Int. J. Cancer 123 (2008), 1601–1609.
68. Reitz, C., Dyslipidemia and dementia: current epidemiology, genetic evidence, and mechanisms behind the associations. J. Alzheimers Dis. 30 (2012), S127–S145.
69. Reitz, C., Mayeux, R., Alzheimer disease: epidemiology, diagnostic criteria, risk factors and biomarkers. Biochem. Pharmacol. 88 (2014), 640–651.
70. Roberts, K.F., et al. Amyloid-β efflux from the central nervous system into the plasma. Ann. Neurol. 76 (2014), 837–844.
71. Rogaeva, E., The neuronal sortilin-related receptor SORL1 is genetically associated with Alzheimer disease. Nat. Genet. 39 (2007), 168–177.
72. Roses, M., Allen, D., Apolipoprotein E alleles as risk factors in Alzheimer's disease. Annu. Rev. Med. 47 (1996), 387–400.
73. Saunders, A.M., et al. Association of apolipoprotein E allele ϵ4 with late-onset familial and sporadic Alzheimer's disease. Neurology, 43, 1993, 1467.
74. Scherzer, C.R., et al. Loss of apolipoprotein E receptor LR11 in Alzheimer disease. Arch. Neurol. 61 (2004), 1200–1205.
75. Schrijvers, E.M., Koudstaal, P.J., Hofman, A., Breteler, M.M., Plasma clusterin and the risk of Alzheimer disease. JAMA 305 (2011), 1322–1326.
76. Seshadri, S., et al. Plasma homocysteine as a risk factor for dementia and Alzheimer's disease. N. Engl. J. Med. 346 (2002), 476–483.
77. Shibata, M., et al. Clearance of Alzheimer's amyloid-β 1-40 peptide from brain by LDL receptor–related protein-1 at the blood-brain barrier. J. Clin. Invest. 106 (2000), 1489–1499.
78. Silverberg, G.D., et al. Alzheimer's disease, normal-pressure hydrocephalus, and senescent changes in CSF circulatory physiology: a hypothesis. Lancet Neurol. 2 (2003), 506–511.
79. Snipes, G.J., Suter, U., Cholesterol and myelin, Cholesterol. 1997, Springer, 173–204.
80. Szymanski, M., Wang, R., Bassett, S.S., Avramopoulos, D., Alzheimer's risk variants in the clusterin gene are associated with alternative splicing. Transl. Psychiatry, 1, 2011, e18.
81. Talwar, P., et al. Genomic convergence and network analysis approach to identify candidate genes in Alzheimer's disease. BMC Genomics, 15, 2014, 1.
82. Thambisetty, M., et al. Association of plasma clusterin concentration with severity, pathology, and progression in Alzheimer disease. Arch. Gen. Psychiatry 67 (2010), 739–748.
83. Tokuda, T., et al. Lipidation of apolipoprotein E influences its isoform-specific interaction with Alzheimer's amyloid β peptides. Biochem. J. 348 (2000), 359–365.
84. Valla, J., et al. Reduced posterior cingulate mitochondrial activity in expired young adult carriers of the APOE ε4 allele, the major late-onset Alzheimer's susceptibility gene. J. Alzheimers Dis. 22 (2010), 307–313.
85. Van Cauwenberghe, C., Van Broeckhoven, C., Sleegers, K., The genetic landscape of Alzheimer disease: clinical implications and perspectives. Genet. Med. 18 (2015), 421–430.
86. Van Uden, E., et al. Increased extracellular amyloid deposition and neurodegeneration in human amyloid precursor protein transgenic mice deficient in receptor-associated protein. J. Neurosci. 22 (2002), 9298–9304.
87. Wahrle, S.E., et al. ABCA1 is required for normal central nervous system ApoE levels and for lipidation of astrocyte-secreted apoE. J. Biol. Chem. 279 (2004), 40987–40993.
88. Wang, S.-C., Oelze, B., Schumacher, A., Age-specific epigenetic drift in late-onset Alzheimer's disease. PLoS One, 3, 2008, e2698.
89. Weller, R., et al. Perivascular drainage of amyloid-b peptides from the brain and its failure in cerebral amyloid angiopathy and Alzheimer's disease. Brain Pathol. 18 (2008), 253–266.
90. Xing, Y.-Y., et al. Blood clusterin levels, rs9331888 polymorphism, and the risk of Alzheimer's disease. J. Alzheimers Dis. 29 (2012), 515–519.
91. Yang, D.S., et al. Characterization of the Binding of Amyloid-β Peptide to Cell Culture-Derived Native Apolipoprotein E2, E3, and E4 Isoforms and to Isoforms from Human Plasma. J. Neurochem. 68 (1997), 721–725.
92. Yang, S., Comparative proteomic analysis of brains of naturally aging mice. Neuroscience 154 (2008), 1107–1120.
93. Yeo, B.T., et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J. Neurophysiol. 106 (2011), 1125–1165.
94. Yu, C.-E., et al. Epigenetic signature and enhancer activity of the human APOE gene. Hum. Mol. Genet., 2013 (ddt354).
95. Zhang, S., et al. CLU rs9331888 polymorphism contributes to Alzheimer's disease susceptibility in Caucasian but not East Asian populations. Mol. Neurobiol. 53 (2016), 1446–1451.
96. Zhao, Z., et al. Central role for PICALM in amyloid-[beta] blood-brain barrier transcytosis and clearance. Nat. Neurosci. 18 (2015), 978–987.