Cholesterol metabolism-associated molecules in late onset Alzheimer disease

Journal of Biological Regulators and Homeostatic Agents

Volumn 27, Issue 2 SUPPL., 2013, Pages 23-35

  Fiorenza, Maria Teresa ^a   Dardis, A ^b   Canterini, S ^a   Erickson, R P ^c  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b SANTA MARIA DELLA MISERICORDIA UNIVERSITY HOSPITAL   (Italy)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

cyclodextrins; LOAD susceptibility genes; Niemann Pick C1

Indexed keywords

AMYLOID BETA PROTEIN; APOLIPOPROTEIN E4; BETA CYCLODEXTRIN; CHOLESTEROL; HYPOCHOLESTEROLEMIC AGENT;

ALZHEIMER DISEASE; CHOLESTEROL METABOLISM; DEMENTIA; GENOTYPE; HOMEOSTASIS; HUMAN; HYPERCHOLESTEROLEMIA; NIEMANN PICK DISEASE; NONHUMAN; REVIEW;

EID: 84886774516     PISSN: 0393974X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (151)

1. Hebert LE, Weuve J, Scherr PA, Evans DA. Alzheimer's disease in the United States (2010-2050) estimated using the 2010 Census. Neurology 2013; 80: 1778-83.
2. Alzheimer's disease facts and figures. Alzheimer's & Dementia 2013; 9: 208-45.
3. Goate A, Chartier-Harlin MC, Mullan M, Brown J, Crawford F, Fidani L et al. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 1991; 349:704-6.
4. Sherrington R, Froelich S. Sorbi S, Campion D, Chi H, Rogaeva EA et al. Alzheimer's disease associated with mutations in presenilin 2 is rare and variably penetrant. Hum Mol Genet 1996; 5:985-8.
5. Levy-Lahad E, Wasco W, Poorkaj P, Romano DM, Oshima J, Pettingell WH et al. Candidate gene for the chromosome 1 familial Alzheimer's disease locus.Science 1995; 269:973-7.
6. Rogaev EI, Sherrington R, Rogaeva EA, Levesque G, Ikeda M, Liang Y et al. Familial Alzheimer's disease in kindreds with missense mutations in a gene on chromosome 1 related to the Alzheimer's disease type 3 gene. Nature 1995; 376:775-8.
7. Blennow K, de Leon MJ, Zetterberg H. Alzheimer's disease. Lancet 2006; 368: 387-403.
8. Ordovas JM, Litwack-Klein L, Wilson PW, Schaefer MM, Schaefer EJ. Apolipoprotein E isoform phenotyping methodology and population frequency with identification of apoE1 and apoE5 isoforms. J Lipid Res 1987; 28: 371-80.
9. Tyrrell J, Cosgrave M, Hawi Z, McPherson J, O'Brien, McCalvert CJ et al. A protective effect of apolipoprotein E e2 allele on dementia in Down's syndrome. Biol Psychiatry 1998; 43: 397-400.
10. Nicoll JAR, Savva GM, Stewart J, Matthews FE, Brayne C, Ince P. Neuropathol Appl Neurobiology 2011; 37: 285-94.
11. Eisenberg DT, Kuzawa CW, Hayes MG. Worldwide allele frequencies of the human apolipoprotein E gene: climate, local adaptations, and evolutionary history. Am J Phys Anthropol 2010; 143:100-11.
12. Bignall J. APOE gene dose in Alzheimer's disease. Lancet 1993; 342: 426.
13. Asada T, Kariya T, Yamagata Z, Kinoshita T, Asaka A. ApoE epsilon 4 allele and cognitive decline in patients with Alzheimer's disease. Neurology 1996; 47: 603.
14. Coon KD, Myers AJ, Craig DW, Webster JA, Pearson JV, Lince DH et al. A high-density whole-genome association study reveals that APOE is the major susceptibility gene for sporadic late-onset Alzheimer's disease. J Clin Psychiatry 2007; 68: 613-8.
15. Castellano JM, Kim J, Stewart FR, Jiang H, DeMattos RB, Patterson BW et al. Human apoE isoforms differentially regulate brain amyloid-β peptide clearance. Sci Transl Med 2011; 3: 89.
16. Koistinaho M, Lin S, Wu X, Esterman M, Koger D, Hanson J et al. Apolipoprotein E promotes astrocyte colocalization and degradation of deposited amyloid-beta peptides. Nat Med 2004; 10: 719-26.
17. Strittmatter WJ, Weisgraber KH, Huang DY, Dong LM, Salvesen GS, Pericak-Vance M et al. Binding of human apolipoprotein E to synthetic amyloid beta peptide: isoform-specific effects and implications for late-onset Alzheimer disease. Proc Natl Acad Sci USA 1993; 90: 8098-102.
18. Xue Y, Lee S, Ha Y. Crystal structure of amyloid precursor-like protein 1 and heparin complex suggests a dual role of heparin in E2 dimerization. Proc Natl Acad Sci USA 2011; 108: 16229-34.
19. Gupta VB, Laws SM, Villemagne VL, Ames D, Bush AI, Ellis KA et al. Plasma apolipoprotein E and Alzheimer disease risk: the AIBL study of aging. Neurology 2011; 76: 1091-8.
20. Bales KR, Liu F, Wu S, Lin S, Koger D, DeLong C et al. Human APOE isoform-dependent effects on brain beta-amyloid levels in PDAPP transgenic mice. J Neurosci 2009; 29: 6771-9.
21. Morgan K. The three new pathway leading to Alzheimer disease. Neuropathol Appl Neurobiol 2011; 37: 353-7.
22. Karch CM, Jeng AT, Nowotny P, Cady J, Cruchaga C, Goate AM. Expression of novel Alzheimer's disease risk genes in control and Alzheimer's disease brains. PloSOne 2012, 7(11):e50976.
23. Erickson RP, Larson-Thome K, Weberg L, Szybinska A, Mossakowska M, Stycyznska M et al. Variation in NPC1, the gene encoding Niemann-Pick C1, a protein involved in intracellular cholesterol transport, is associated with Alzheimer disease and/or aging in the Polish population. Neurosci Lett 2008; 447: 153-7.
24. Rodriguez-Rodriguez E, Vazques-Higuera JL, Sanchez-Juan P, Mateo I, Posueta A, Martinez-Garcia A et al. Epistasis between intracellular cholesterol trafficking-related gene (NPC1 and ABCA1) and Alzheimer's disease risk. J Alzheimers Dis 2010; 21: 619-25.
25. Borbon IA, Erickson RP. "Interaction of Npc1 and amyloid accumulation/deposition in the APP/PS1 mouse model of Alzheimer's" J Applied Genetics 2010; 52: 213-8.
26. Refolo LM, Pappolla MA, Malester B et al. Hypercholesterolemia accelerates the Alzheimer's amyloid pathology in a transgenic mouse model. Neurobiol Dis 2000; 7: 321-31.
27. Shie FS, Jin LW, Cook DG, Leverenz JB, LeBoeuf RC. Diet-induced hypercholesterolemia enhances brain Aβ accumulation in transgenic mice. Neuroreport 2002; 13: 455-9.
28. Sparks DL, Kuo YM, Roher A, Martin T, Lukas RJ. Alterations of Alzheimer's disease in the cholesterol-fed rabbit, including vascular inflammation. Preliminary observations. Ann N Y Acad Sci. 2000; 903: 335-44.
29. Shepardson NE, Shankar GM, Selkoe DJ. Cholesterol level and statin use in Alzheimer disease: I. Review of epidemiological and preclinical studies. Arch Neurol. 2011; 68: g1239-44.
30. Pfrieger FW. Cholesterol homeostasis and function in neurons of the central nervous system. Cell Mol Life Sci. 2003; 60: 1158-71.
31. Ikonen E. Mechanisms for cellular cholesterol transport: defects and human disease. Physiol Rev 2006; 86: 1237-61.
32. Miller WL. Structure of genes encoding steroidogenic enzymes. J Steroid Biochem 1987; 27: 759-66.
33. Dietschy JM, Turley SD. Thematic review series: brain Lipids. Cholesterol metabolism in the central nervous system during early development and in the mature animal. J lipid 2004; es.45: 1375-97.
34. Beffert U, Danik M, Krzywkowski P, Ramassamy C, Berrada F,Poirier J. The neurobiology of apolipoproteins and their receptors in the CNS and Alzheimer's disease. Brain Res Brain Res Rev 1998; 27: 119-42.
35. Wahrle S, Das P, Nyborg AC, McLendon C, Shoji M, Kawarabayashi T et al. Cholesterol-dependent gamma-secretase activity in buoyant cholesterol-rich membrane microdomains. Neurobiol Dis 2002; 9: 11-23.
36. Karten B, Campenot RB, Vance DE, Vance JE. Expression of ABCG1, but not ABCA1, correlates with cholesterol release by cerebellar astroglia. J Biol Chem 2006; 281: 4049-57.
37. Herz J. Apolipoprotein E receptors in the nervous system. Curr Opin Lipidol 2009; 20: 190-6.
38. Vance JE. Lipid imbalance in the neurological disorder, Niemann-Pick C disease. FEBS Lett 2006; 580: 5518-24.
39. Wang ML, Motamed M, Infante RE, Abi-Mosleh L, Kwon HJ, Brown MS et al. Identification of surface residues on Niemann-Pick C2 essential for hydrophobic handoff of cholesterol to NPC1 in lysosomes. Cell Meteb 2010; 12: 166-73.
40. Allinson TM, Parkin El, Turner AJ, Hooper NM. ADAMs family members as amyloid precursor protein alpha-secretases. J Neurosci Res. 2003; 74:342-52.
41. Kojro E, Fahrenholz F. The non-amyloidogenic pathway: structure and function of alpha-secretases. Subcell Biochem 2005; 38: 105-27.
42. Esch FS, Keim PS, Beattie EC, Blacher RW, Culwell AR, Oltersdorf T et al. Cleavage of amyloid beta peptide during constitutive processing of its precursor. Science 1990; 248: 1122-4.
43. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, Denis P et al. Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 1999; 286: 735-41.
44. Selkoe DJ (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 2001; 81: 741-7.
45. Grziwa B, Grimm MO, Masters CL, Beyreuther K, Hartmann T, Lichtenthaler SF. The transmembrane domain of the amyloid precursor protein in microsomal membranes is on both sides shorter than predicted. J Biol Chem 2003; 278: 6803-08.
46. Qi-Takahara Y, Morishima-Kawashima M, Tanimura Y, Dolios G, Hirotani N, Horikoshi Yet al. Longer forms of amyloid beta protein: implications for the mechanism of intramembrane cleavage by gamma-secretase. J Neurosci 2005; 25: 436-45.
47. Selkoe DJ, Wolfe MS. Presenilin: running with scissors in the membrane. Cell 2007; 131: 215-2.
48. Selkoe DJ. Biochemistry and molecular biology of amyloid beta-protein and the mechanism of Alzheimer's disease. Handb Clin Neurol 2008; 89: 245-60.
49. Thinakaran G, Koo EH. Amyloid precursor protein trafficking, processing, and function. J Biol Chem 2008; 283: 29615-9.
50. Lichtenthaler SF. Alpha-secretase cleavage of the amyloid precursor protein: proteolysis regulated by signaling pathways and protein trafficking. Curr Alzheimer Res 2012; 9: 165-77.
51. Koo EH, Squazzo SL. Evidence that production and release of amyloid beta-protein involves the endocytic pathway. J Biol Chem 1994; 269: 17386-9.
52. Cook DG, Forman MS, Sung JC, Leight S, Kolson DL, Iwatsubo T et al. Alzheimer's A beta(1-42) is generated in the endoplasmic reticulum/intermediate compartment of NT2N cells. Nat Med 1997; 3: 1021-3.
53. Greenfield JP, Tsai J, Gouras GK, Hai B, Thinakaran G, Checler F et al. Endoplasmic reticulum and trans-Golgi network generate distinct populations of Alzheimer beta-amyloid peptides. Proc Natl Acad Sci USA 1999; 96: 742-7.
54. Takahashi RH, Milner TA, Li F, Nam EE, Edgar MA, Yamaguchi H et al. Intraneuronal Alzheimer abeta42 accumulates in multivesicular bodies and is associated with synaptic pathology. Am J Pathol 2002; 161: 1869-79.
55. LaFerla FM, Green KN, Oddo S. Intracellular amyloidbeta in Alzheimer's disease. Nat Rev Neurosci 2007; 8: 499-509.
56. Kojro E, Gimpl G, Lammich S, Marz W, Fahrenholz F. Low cholesterol stimulates the nonamyloidogenic pathway by its effect on the alpha-secretase ADAM 10. Proc Natl Acad Sci USA 2001; 98: 5815-20.
57. Vetrivel KS, Cheng H, Lin W, Sakurai T, Li T, Nukina N et al. Association of gamma-secretase with lipid rafts in post-Golgi and endosome membranes. J Biol Chem 2004; 279: 44945-4.
58. Kalvodova L, Kahya N, Schwille P, Ehehalt R, Verkade P, Drechsel D et al. Lipids as modulators of proteolytic activity of BACE: involvement of cholesterol, glycosphingolipids, and anionic phospholipids in vitro. J Biol Chem 2005; 280: 36815-23.
59. Osenkowski P, Ye W, Wang R, Wolfe MS, Selkoe DJ. Direct and potent regulation of gamma-secretase by its lipid microenvironment. J Biol Chem 2008; 283: 22529-4.
60. Ehehalt R, Keller P, Haass C, Thiele C, Simons K. Amyloidogenic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts. J Cell Biol 2003; 160: 113-23.
61. Bodovitz S, Klein WL. Cholesterol modulates alphasecretase cleavage of amyloid precursor protein. J Biol Chem 1996; 271: 4436-40.
62. Frears ER, Stephens DJ, Walters CE, Davies H, Austen BM. The role of cholesterol in the biosynthesis of betaamyloid. Neuroreport 1999; 10: 1699-705.
63. Simons M, Keller P, De Strooper B, Beyreuther K, Dotti CG et al. Cholesterol depletion inhibits the generation of beta-amyloid in hippocampal neurons. Proc Natl Acad Sci USA 1998; 95: 6460-4.
64. Fassbender K, Simons M, Bergmann C, Stroick M, Lutjohann D, Keller P et al Simvastatin strongly reduces levels of Alzheimer's disease beta-amyloid peptides Abeta 42 and Abeta 40 in vitro and in vivo. Proc Natl Acad Sci USA 2001; 98: 5856-61.
65. Abad-Rodriguez J, Ledesma MD, Craessaerts K, Perga S, Medina M, Delacourte A et al Neuronal membrane cholesterol loss enhances amyloid peptide generation. J Cell Biol 2004, 167: 953-6.
66. Yamazaki TY, Chang C, Haass Y. Accumulation and aggregation of amyloid beta-protein in late endosomes of Niemann-Pick type C cells. J Biol Chem 2001; 276: 4454-60.
67. Burns M, Gaynor K, Olm V, Mercken M, LaFrancois J, Wang L et al. Presenilin redistribution associated with aberrant cholesterol transport enhances beta-amyloid production in vivo. J Neurosci 2003; 23: 5645-9.
68. Runz H, Rietdorfi, Tomic I, de Bernard M, Beyreuther K, Pepperkok R et al. Inhibition of intracellular cholesterol transport alters presenilin localization and amyloid precursor protein processing in neuronal cells. J Neurosci 2002; 22: 1679-89.
69. Kosicek M, Malnar M, Goate A, Hecimovic S. Cholesterol accumulation in Niemann Pick type C model cells causes a shift in APP localization to lipid rafts. Biochem Biophys Res Commun 2010; 293: 404-9.
70. Malnar M, Kosicek M, Mitterreiter S, Omerbasic D, Lichtenthaler SF, Goate A et al. Niemann-Pick type C cells show cholesterol dependent decrease of APP expression at the cell surface and its increased processing through the beta-secretase pathway. Biochim Biophys Acta 2010; 1802: 682-71.
71. Kodam A, Maulik M, Peake K, Amritraj A, Vetrivel KS, Thinakaran G et al. Altered levels and distribution of amyloid precursor protein and its processing enzymes in Niemann-Pick type C1-deficient mouse brains. Glia 2010; 58:1267-81.
72. Mattsson N, Zetterberg H, Bianconi S, Yanjanin NM, Fu R, Mansson JE et al. Gamma-secretase-dependent amyloid-beta is increased in Niemann-Pick type C: a cross-sectional study Neurology 2011; 76: 366-72.
73. Malnar M, Kosicek M, Lisica A, Posavec M, Krolo A, Njavro J, et al. Cholesterol-depletion corrects APP and BACE1 misstrafficking in NPC1-deficient cells. Biochim Biophys Acta. 2012; 1822: 1270-83.
74. Carstea ED, Morris JA, Coleman KG, Loftus SK, Zhang D, Cummings C et al. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 1997; 277: 228-31.
75. Loftus SK, Morris JA, Carstea ED, Gu JZ, Cummings C, Brown A et al. Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science 1997; 277: 232-5.
76. Garver WS, Heidenreich RA, Erickson RP, Thomas MA, Wilson JM. Localization of the murine Niemann-Pick C1 protein to two distinct intracellular compartments. J Lipid Res 2000; 41: 673-87.
77. Higgins ME, Davies JP, Chen FW, Ioannou YA. Niemann-Pick C1 is a late endosome-resident protein that transiently associates with lysosomes and the trans-Golgi network. Mol Genet Metab 1999; 68: 1-13.
78. Neufeld EB, Wastney M, Patel S, Suresh S, Cooney AM, Dwyer NK et al. The Niemann-Pick C1 protein resides in a vesicular compartment linked to retrograde transport of multiple lysosomal cargo. J Biol Chem 1999; 274: 9627-35.
79. Lloyd-Evans E, Morgan AJ, He X, Smith DA, Elliot-Smith E, Sillence DJ et al. Niemann-Pick disease type C1 is a sphingosine storage disease that causes dysregulation of lysosomal calcium. Nat Med 2008; 14:1247-55.
80. Vincent I, Bu B, Erickson RP. Understanding Niemann-Pick type C disease: A fat problem. Curr Opin Neurol 2003; 16: 155-61.
81. Borbon I, Totenhagen J, Fiorenza MT, Canterini S, Ke W, Trouard T, Erickson RP. Niemann-Pick C1 mice, a model of "juvenile Alzheimer's disease", with normal gene expression in neurons and fibrillary astrocytes show long term survival and delayed neurodegeneration. J Alzheimers Dis 2012; 30: 875-87.
82. Mann KM, Thorngate FE, Katoh-Fukui Y, Hamanaka H, Williams DL, Fujita S, et al. Indipendent effects of APOE on cholesterol metabolism and brain Abeta levels in an Alzheimer disease mouse model. Hum Mol Genet 2004; 13: 1959-68.
83. Suzuki K, Parker CC, Pentchev PG, Katz D, Ghetti B, D'Agostino AN, et al. Neurofibrillary tangles in Niemann-Pick disease type C. Acta Neuropathol 1995; 89: 227-38.
84. Yamaguchi H, Sugihara S, Ogawa A, Oshima N, Ihara Y. Alzheimer beta amyloid deposition enhanced by apoE epsilon4 gene precedes neurofibrillary pathology in the frontal association cortex of nondemented senior subjects. J Neuropathol Exp Neurol 2001; 60: 731-9.
85. Distl R, Meske V, Ohm TG. Tanglebearing Neurons contain more free cholesterol than adjacent tanglefree neurons. Acta Neuropatho 2001; 101: 547-54.
86. Saito Y, Suzuki K, Nanba E, Yamamoto T, Ohno K, Murayama S. Niemann-Pick type C disease: accelerated neurofibrillary tangle formation and amyloid beta deposition associated with apolipoprotein E epsilon 4 homozygosity. Ann Neurol 2002; 52: 351-5.
87. Horton JD, Shah NA, Warrington JA, Anderson NN, Park SW, Brown MS, Goldstein JL. Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proc Natl Acad Sci U S A 2003; 100:12027-32.
88. Brown MS, Goldstein JL. A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood. Proc Natl Acad Sci USA 1999; 96: 11041-8.
89. Pierrot N, Tyteca D, D'auria L, Dewachter I, Gailly P, Hendrickx Ai et al. Amyloid precursor protein controls cholesterol turnover needed for neuronal activity. EMBO Mol Med 2013; 5: 608-90
90. Dean, M, Rzhetsky, A, Allikmets R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res. 2001; 11: 1156-66.
91. Kim WS, Weickert CS, Garner B. Role of ATP-binding cassette transporters in brain lipid transport and neurological disease. J Neurochem 2008; 104: 1145-66.
92. Brewer HB, Jr and Santamarina-Fojo S. New insights into the role of the adenosine triphosphate-binding cassette transporters in high-density lipoprotein metabolism and reverse cholesterol transport. Am J Cardiol 2003; 91: 3E-11E.
93. Fagan AM, Holtzman DM, Munson G, Mathur T, Schneider D, Chang LK et al. Unique lipoproteins secreted by primary astrocytes from wild type, apoE (-/-), and human apoE transgenic mice. J Biol Chem 1999; 274: 30001-7.
94. DeMattos RB, Brendza RP Heuser JE, Kierson M, Cirrito JR, Fryer J et al. Purification and characterization of astrocyte-secreted apolipoprotein E and J-containing lipoproteins from wild-type and human apoE transgenic mice. Neurochem Int 2001; 39: 415-25.
95. Wahrle SE, Jiang H, Parsadanian M, Legleiter J, Han X, Fryer JD et al. ABCA1 is required for normal central nervous system ApoE levels and for lipidation of astrocyte-secreted apoE. J Biol Chem 2004; 279: 40987-93.
96. Tokuda T, Calero M, Matsubara E, Vidal R, Kumar A, Permanne B et al. Lipidation of apolipoprotein E influences its isoform-specific interaction with Alzheimer's amyloid beta peptides. Biochem J 2000; 2: 359-65.
97. Holtzman DM, Herz J, Bu G. Apolipoprotein E and apolipoprotein E receptors: normal biology and roles in Alzheimer disease. Cold Spring Harb Perspect Med 2012; 2(3):a006312.
98. Fukumoto H, Deng A, Irizarry MC, Fitzgerald ML, Rebeck GW. Induction of the cholesterol transporter ABCA1 in central nervous system cells by liver X receptor agonists increases secreted Abeta levels. J Biol Chem 2002; 277: 48508-13.
99. Sun Y, Hao M, Luo Y, Liang CP, Silver DL, Cheng C et al. Stearoyl-CoA desaturase inhibits ATP-binding cassette transporter A1-mediated cholesterol efflux and modulates membrane domain structure. J Biol Chem 2003; 278: 5813-20.
100. Chan SL, Kim WS, Kwok JB, Hill AF, Cappai R, Rye KA, Garner B. ATP-binding cassette transporter A7 regulates processing of amyloid precursor protein in vitro. J Neurochem 2008; 106: 793-804.
101. Wang N, Lan D, Gerbod-Giannone M, Linsel-Nitschke P, Jehle AW, Chen W et al. ATP-binding cassette transporter A7 (ABCA7) binds apolipoprotein A-I and mediates cellular phospholipid but not cholesterol efflux J Biol Chem 2003; 278: 42906-12.
102. Kim WS, Fitzgerald ML, Kang K, Okuhira K, Bell SA, Manning JJ et al. Abca7 null mice retain normal macrophage phosphatidylcholine and cholesterol efflux activity despite alterations in adipose mass and serum cholesterol levels. J Biol Chem 2005; 280: 3989-95.
103. Choi HY, Karten B, Chan T, Vance JE, Greer WL, Heidenreich RA et al. Impaired ABCA1-dependent lipid efflux and hypoalphalipoproteinemia in human Niemann-Pick type C disease. J Biol Chem. 2003; 278: 32569-77.
104. Boadu E, Choi HY, Lee DW, Waddington EI, Chan T, Asztalos B et al. Correction of apolipoprotein A-I-mediated lipid efflux and high density lipoprotein particle formation in human Niemann-Pick type C disease fibroblasts. J Biol Chem 2006; 281: 37081-90.
105. Neufeld EB, Stonik JA, Demosky SJ Jr, Knapper CL, Combs CA, Cooney A, et al. The ABCA1 transporter modulates late endocytic trafficking: insights from the correction of the genetic defect in Tangier disease. J Biol Chem 2004; 279: 15571-8.
106. Kim WS, Bhatia S, Elliott DA, Agholme L, Kågedal K, McCann H et al. Increased ATP-binding cassette transporter A1 expression in Alzheimer's disease hippocampal neurons. J Alzheimers Dis 2010; 21: 193-205.
107. Whitney KD, Watson MA, Collins JL, Benson WG, Stone TM, Numerick MJ et al. Regulation of cholesterol homeostasis by the liver X receptors in the central nervous system. Mol Endocrinol 2002;16: 1378-85.
108. Shafaati M, Marutle A, Pettersson H, Lövgren-Sandblom A, Olin M, Pikuleva I et al. Marked accumulation of 27-hydroxycholesterol in the brains of Alzheimer's patients with the Swedish APP 670/671 mutation. J Lipid Res 201; 52: 1004-10.
109. Rayner KJ, Suárez Y, Dávalos A, Parathath S, Fitzgerald ML, Tamehiro N et al MiR-33 contributes to the regulation of cholesterol homeostasis. Science 2010; 328: 1570-3.
110. Lillis AP, Greenlee MC, Mikhailenko I, Pizzo SV, Tenner AJ, Strickland DK et al. Murine low-density lipoprotein receptor-related protein 1 (LRP) is required for phagocytosis of targets bearing LRP ligands but is not required for C1q-triggered enhancement of phagocytosis J Immunol 2008; 181: 364-73.
111. Bu G. Apolipoprotein E and its receptors in Alzheimer's disease: pathways, pathogenesis and therapy. Nat Rev Neurosci 2009; 10: 333-44.
112. Marzolo MP, von Bernhardi R, Bu G, Inestrosa NC. Expression of alpha(2)-macroglobulin receptor/low density lipoprotein receptor-related protein (LRP) in rat microglial cells. J Neurosci Res 2000; 60: 401-11.
113. Bu G, Maksymovitch EA, Nerbonne JM, Schwartz AL. Expression and function of the low density lipoprotein receptor-related protein (LRP) in mammalian central neurons. J Biol Chem 1994; 269: 18521-8.
114. Wilhelmus MM, Otte-Höller I, van Triel JJ, Veerhuis R, Maat-Schieman ML, Bu G et al. Lipoprotein receptor-related protein-1 mediates amyloid-beta-mediated cell death of cerebrovascular cells. Am J Pathol 2007; 171: 1989-99.
115. Ruzali WA, Kehoe PG, Love S. Influence of LRP-1 and apolipoprotein E on amyloid-β uptake and toxicity to cerebrovascular smooth muscle cells. J Alzheimers Dis 2013; 33:95-110.
116. Herz J, Strickland DK. LRP: a multifunctional scavenger and signaling receptorJ Clin Invest. 2001; 108: 779-84.
117. Dieckmann M, Dietrich MF, Herz J. Lipoprotein receptors-an evolutionarily ancient multifunctional receptor family. Biol Chem 2010; 391:1341-63.
118. Deane R, Wu Z, Sagare A, Davis J, Du Yan S, Hamm K et al. LRP/amyloid beta-peptide interaction mediates differential brain efflux of Abeta isoforms. Neuron 2004; 43: 333-44.
119. Taylor DR, Hooper NM. The low-density lipoprotein receptor-related protein 1 (LRP1) mediates the endocytosis of the cellular prion protein. Biochem J 2007; 402: 17-23.
120. Shibata M, Yamada S, Kumar SR, Calero M, Bading J, Frangione B et al. Clearance of Alzheimer's amyloid-ss(1-40) peptide from brain by LDL receptor-related protein-1 at the blood-brain barrier. J Clin Invest 2000; 106: 1489-99.
121. Deane R, Du Yan S, Submamaryan RK, LaRue B, Jovanovic S, Hogg E et al. RAGE mediates amyloid-beta peptide transport across the blood-brain barrier and accumulation in brain. Nat Med 2003; 9: 907-13.
122. Yan SD, Chen X, Fu J, Chen M, Zhu H, Roher A et al., RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 1996; 382:685-91
123. Donahue JE, Flaherty SL, Johanson CE, Duncan JA 3rd, Silverberg GD, Miller MC et al. RAGE, LRP-1, and amyloid-beta protein in Alzheimer's disease. Acta Neuropathol 2006; 112: 405-15.
124. Miller MC, Tavares R, Johanson CE, Hovanesian V, Donahue JE, Gonzalez L et al. Hippocampal RAGE immunoreactivity in early and advanced Alzheimer's disease. Brain Res 2008;1230: 273-80.
125. Sagare A, Deane R, Bell RD, Johnson B, Hamm K, Pendu R et al. Clearance of amyloid-beta by circulating lipoprotein receptors. Nat Med 2007;13: 1029-31.
126. Sehgal N, Gupta A, Valli RK, Joshi SD, Mills JT, Hamel E et al. Withania somnifera reverses Alzheimer's disease pathology by enhancing low-density lipoprotein receptor-related protein in liver. Proc Natl Acad Sci U S A 2012; 109: 3510-5.
127. Tamaki C, Ohtsuki S, Terasaki T. Insulin facilitates the hepatic clearance of plasma amyloid beta-peptide (1 40) by intracellular translocation of low-density lipoprotein receptor-related protein 1 (LRP-1) to the plasma membrane in hepatocytes. Mol Pharmacol 2007;72: 850-5.
128. Dries DR, Yu G, Herz J. Extracting β-amyloid from Alzheimer's disease. Proc Natl Acad Sci U S A 2012; 109: 3199-200.
129. Calero, M. et al. Functional and structural properties of lipidassociated apolipoprotein J (clusterin). Biochem J 1999; 344: 375-383.
130. Ishikawa S, Deguchi T, Hara K, Takuma S, Kayaba K, Tsutsumi A et al. Lipoprotein(a) levels and apolipoprotein(a) isoforms related to life style risk factors. J Epidemiol 1999; 9: 32-9.
131. Michel D, Chatelain G, North S, Brun G. Stress-induced transcription of the clusterin/ apoJ gene. Biochem J 1997; 328: 45-50.
132. Lambert JC, Heath S, Even G, Campion D, Sleegers K et al. Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease. Nat Genet 2009; 41: 1094-1099.
133. Harold D, Abraham R, Hollingworth P, Sims R, Gerrish A et al. Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease. Nat Genet 2009; 41: 1088-1093.
134. Guerreiro RJ, Beck J, Gibbs JR, Santana I, Rossor MN et al. Genetic variability in CLU and its association with Alzheimer's disease. PLoS One 2010; 5:e9510.
135. Carrasquillo MM, Belbin O, Hunter TA, Ma L, Bisceglio GD et al. Replication of CLU, CR1, and PICALM associations with Alzheimer disease. Archives of Neurology 2010; 67: 961-4.
136. Jun G, Naj AC, Beecham GW, Wang LS, Buros J et al. Meta-analysis confirms CR1, CLU, and PICALM as Alzheimer disease risk loci and reveals interactions with APOE genotypes. Arch Neurol 2010; 67: 1473-84.
137. May PC, Lampert-Etchells M, Johnson SA, Poirier J, Masters JN et al. Dynamics of gene expression for a hippocampal glycoprotein elevated in Alzheimer's disease and in response to experimental lesions in rat. Neuron 1990; 5: 831-9.
138. Schrijvers EM, Koudstaal PJ, Hofman A, Breteler MM. Plasma clusterin and the risk of Alzheimer disease. JAMA: the Journal of the American Medical Association 2011; 305: 1322-6.
139. Calero M, Rostagno A, Matsubara E, Zlokovic B, Frangione B et al. Apolipoprotein J (clusterin) and Alzheimer's disease. Microsc Res Tech 2000; 50: 305-15.
140. Choi-Miura NH, Ihara Y, Fukuchi K, Takeda M, Nakano Y et al. SP-40,40 is a constituent of Alzheimer's amyloid. Acta Neuropathol 1992; 83: 260-4.
141. Bartl MM, Luckenbach T, Bergner O, Ullrich O, Koch-Brandt C. Multiple receptors mediate apoJ-dependent clearance of cellular debris into nonprofessional phagocytes. Exp Cell Res 2011; 271: 130-41.
142. Bell RD, Sagare AP, Friedman AE, Bedi GS, Holtzman DM, Deane R et al. Transport pathways for clearance of human Alzheimer's amyloid beta-peptide and apolipoproteins E and J in the mouse central nervous system. J Cereb Blood Flow Metab 2007; 27, 909-18.
143. Ling IF, Bhongsatiern J, Simpson JF, Fardo DW, Steven Estus. Genetics of Clusterin Isoform Expression and Alzheimer's Disease Risk. PLoS One 2012; 7(4):e33923.
144. Zidovetzki R, Levitan I. Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies. Biochim Biophys Acta 2007; 1768: 1311-145.
145. Coskun U, Simons K. Membrane rafting: from apical sorting to phase segregation. FEBS Lett 2010; 584: 1685-93.
146. Di Paolo G, Kim TW. Linking lipids to Alzheimer's disease: cholesterol and beyond. Nat Rev Neurosci 2011; 12: 284-96.
147. Maulik M, Ghoshal B, Kim J, Wang Y, Yang J, Westaway D, Kar S. Mutant human APP exacerbates pathology in a mouse model of NPC and its reversal by a β-cyclodextrin. Hum Mol Genet. 2012; 21: 4857-75.
148. Camargo F, Erickson RP, Garver WS, Hossain GS, Carbone PN et al. Cyclodextrins in the treatments of a mouse model of Niemann-Pick C disease. Life Sci 2001; 70: 131-42.
149. -/- Mouse. Proc Natl Acad Sci USA 2009; 106: 2377-82.
150. Yao J, Ho D, Calingasan NY, Pipalia NH, Lin MT, Beal MF. Neuroprotection by cyclodextrin in cell and mouse models of Alzheimer disease. J Exp Med 2012; 209: 2501-13.
151. Pontikis CC, Davidson CD, Walkley SU, Platt FM, Begley DJ. Cyclodextrin alleviates neuronal storage of cholesterol in Niemann-Pick C disease without evidence of detectable blood-brain barrier permeability. J Inherit Metab Dis 2013; 36: 491-8.