450
Views
1
CrossRef citations to date
0
Altmetric
Reviews

High-density lipoproteins at the interface between central nervous system and plasma lipoprotein metabolism

, , , &
Pages 69-81 | Published online: 18 Jan 2017

References

  • Redzic Z. Molecular biology of the blood–brain and the blood–cerebrospinal fluid barriers: similarities and differences. Fluids Barriers CNS 8(1), 3 (2011).
  • Hegele RA. Plasma lipoproteins: genetic influences and clinical implications. Nat. Rev. Genet. 10(2), 109–121 (2009).
  • Linton MF, Gish R, Hubl ST et al. Phenotypes of apolipoprotein B and apolipoprotein E after liver transplantation. J. Clin. Invest. 88(1), 270–281 (1991).
  • Riwanto M, Landmesser U. High-density lipoproteins and endothelial functions: mechanistic insights and alterations in cardiovascular disease. J. Lipid Res. 54(12), 3227–3243 (2013). • describes the modification of HDL function in cardiovascular disease.
  • Toledo JB, Arnold SE, Raible K et al. Contribution of cerebrovascular disease in autopsy confirmed neurodegenerative disease cases in the National Alzheimer’s Coordinating Centre. Brain 136(Pt 9), 2697–2706 (2013).
  • Frank PG, Marcel YL. Apolipoprotein A-I: structure–function relationships. J. Lipid Res. 41(6), 853–872 (2000).
  • Möckel B, Zinke H, Flach R, Weiss B, Weiler-Güttler H, Gassen HG. Expression of apolipoprotein A-I in porcine brain endothelium in vitro. J. Neurochem. 62(2), 788–798 (1994).
  • Stukas S, Robert J, Lee M et al. Intravenously Injected Human Apolipoprotein A-I Rapidly Enters the Central Nervous System via the Choroid Plexus. J. Am. Heart Assoc. 3(6), doi:10.1161/JAHA.114.001156 (2014).
  • Elshourbagy NA, Liao WS, Mahley RW, Taylor JM. Apolipoprotein E mRNA is abundant in the brain and adrenals, as well as in the liver, and is present in other peripheral tissues of rats and marmosets. Proc. Natl Acad. Sci. USA 82(1), 203–207 (1985).
  • Xu Q, Bernardo A, Walker D, Kanegawa T, Mahley RW, Huang Y. 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(19), 4985–4994 (2006).
  • Lane-Donovan C, Philips GT, Herz J. More than cholesterol transporters: lipoprotein receptors in CNS function and neurodegeneration. Neuron 83(4), 771–787 (2014).
  • Fitzgerald ML, Mendez AJ, Moore KJ, Andersson LP, Panjeton HA, Freeman MW. ATP-binding cassette transporter A1 contains an NH2-terminal signal anchor sequence that translocates the protein’s first hydrophilic domain to the exoplasmic space. J. Biol. Chem. 276(18), 15137–15145 (2001).
  • Puntoni M, Sbrana F, Bigazzi F, Sampietro T. Tangier disease: epidemiology, pathophysiology, and management. Am. J. Cardiovasc. Drugs 12(5), 303–311 (2012).
  • Bodzioch M, Orsó E, Klucken J et al. The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat. Genet. 22(4), 347–351 (1999).
  • McNeish J, Aiello RJ, Guyot D et al. High density lipoprotein deficiency and foam cell accumulation in mice with targeted disruption of ATP-binding cassette transporter-1. Proc. Natl Acad. Sci. USA 97(8), 4245–4250 (2000).
  • Hirsch-Reinshagen V, Zhou S, Burgess BL et al. Deficiency of ABCA1 impairs apolipoprotein E metabolism in brain. J. Biol. Chem. 279(39), 41197–41207 (2004).
  • Wahrle SE, Jiang H, Parsadanian M et al. Deletion of Abca1 increases Abeta deposition in the PDAPP transgenic mouse model of Alzheimer disease. J. Biol. Chem. 280(52), 43236–43242 (2005).
  • Cavelier C, Rohrer L, von Eckardstein A. ATP-Binding cassette transporter A1 modulates apolipoprotein A-I transcytosis through aortic endothelial cells. Circ. Res. 99(10), 1060–1066 (2006).
  • Cavelier C, Ohnsorg PM, Rohrer L, von Eckardstein A. The β-chain of cell surface F(0)F(1) ATPase modulates apoA-I and HDL transcytosis through aortic endothelial cells. Arterioscler. Thromb. Vasc. Biol. 32(1), 131–139 (2012).
  • Rohrer L, Ohnsorg PM, Lehner M, Landolt F, Rinninger F, von Eckardstein A. High-density lipoprotein transport through aortic endothelial cells involves scavenger receptor BI and ATP-binding cassette transporter G1. Circ. Res. 104(10), 1142–1150 (2009).
  • Robert J, Lehner M, Frank S, Perisa D, von Eckardstein A, Rohrer L. Interleukin 6 stimulates endothelial binding and transport of high-density lipoprotein through induction of endothelial lipase. Arterioscler. Thromb. Vasc. Biol. 33(12), 2699–2706 (2013).
  • Kozyraki R, Fyfe J, Kristiansen M et al. The intrinsic factor-vitamin B12 receptor, cubilin, is a high-affinity apolipoprotein A-I receptor facilitating endocytosis of high-density lipoprotein. Nat. Med. 5(6), 656–661 (1999).
  • Hammad SM. Megalin acts in concert with cubilin to mediate endocytosis of high density lipoproteins. J. Biol. Chem. 275(16), 12003–12008 (2000).
  • Kratzer I, Wernig K, Panzenboeck U et al. Apolipoprotein A-I coating of protamine-oligonucleotide nanoparticles increases particle uptake and transcytosis in an in vitro model of the blood–brain barrier. J. Control. Release 117(3), 301–311 (2007).
  • Rosenson RS, Brewer HB, Davidson WS et al. Cholesterol efflux and atheroprotection: advancing the concept of reverse cholesterol transport. Circulation 125(15), 1905–1919 (2012).
  • Shah AS, Tan L, Lu Long J, Davidson WS. The proteomic diversity of high density lipoproteins: our emerging understanding of its importance in lipid transport and beyond. J. Lipid Res. 54(10), 2575–2585 (2013). •• Emphasizes the complexity of the plasma HDL proteom.
  • Riwanto M, Rohrer L, Roschitzki B et al. Altered activation of endothelial anti- and proapoptotic pathways by high-density lipoprotein from patients with coronary artery disease: role of high-density lipoprotein-proteome remodeling. Circulation 127(8), 891–904 (2013).
  • Jahangiri A. High-density lipoprotein and the acute phase response. Curr. Opin. Endocrinol. Diabetes Obes. 17(2), 156–160 (2010). • Provides information on HDL modification during the accute phase.
  • Holzer M, Wolf P, Curcic S et al. Psoriasis alters HDL composition and cholesterol efflux capacity. J. Lipid Res. 53(8), 1618–1624 (2012).
  • Weichhart T, Kopecky C, Kubicek M et al. Serum amyloid A in uremic HDL promotes inflammation. J. Am. Soc. Nephrol. 23(5), 934–947 (2012).
  • Demeester N, Castro G, Desrumaux C et al. Characterization and functional studies of lipoproteins, lipid transfer proteins, and lecithin: cholesterol acyltransferase in CSF of normal individuals and patients with Alzheimer’s disease. J. Lipid Res. 41(6), 963–974 (2000).
  • Koch S, Donarski N, Goetze K et al. Characterization of four lipoprotein classes in human cerebrospinal fluid. J. Lipid Res. 42(7), 1143–1151 (2001). • Characterizes four lipoproteins in the CSF.
  • Muffat J, Walker DW. Apolipoprotein D: an overview of its role in aging and age-related diseases. Cell Cycle 9(2), 269–273 (2010).
  • Liu C-C, Liu C-C, Kanekiyo T, Xu H, Bu G. Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy. Nat. Rev. Neurol. 9(2), 106–118 (2013). •• Provides comprehensive information regarding the common polymorphism in the apoE gene, and how they contribute differential risks to AD and other dementias. the known neurological functions of apoe are also summarized.
  • Eisenberg DTA, Kuzawa CW, Hayes MG. Worldwide allele frequencies of the human apolipoprotein E gene: climate, local adaptations, and evolutionary history. Am. J. Phys. Anthropol. 143(1), 100–111 (2010).
  • Chartier-Harlin MC, Parfitt M, Legrain S et al. Apolipoprotein E, epsilon 4 allele as a major risk factor for sporadic early and late-onset forms of Alzheimer’s disease: analysis of the 19q13.2 chromosomal region. Hum. Mol. Genet. 3(4), 569–574 (1994).
  • Houlden H, Crook R, Backhovens H et al. ApoE genotype is a risk factor in nonpresenilin early-onset Alzheimer’s disease families. Am. J. Med. Genet. 81(1), 117–121 (1998).
  • Harold D, Abraham R, Hollingworth P et al. Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer’s disease. Nat. Genet. 41(10), 1088–1093 (2009).
  • Lambert J-C, Heath S, Even G et al. Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer’s disease. Nat. Genet. 41(10), 1094–1099 (2009).
  • Coon KD, Myers AJ, Craig DW et al. A high-density wholegenome association study reveals that APOE is the major susceptibility gene for sporadic late-onset Alzheimer’s disease. J. Clin. Psychiatry 68(4), 613–618 (2007).
  • Bertram L, Lange C, Mullin K et al. Genome-wide association analysis reveals putative Alzheimer’s disease susceptibility loci in addition to APOE. Am. J. Hum. Genet. 83(5), 623–632 (2008).
  • Burns LC, Minster RL, Demirci FY et al. Replication study of genome-wide associated SNPs with late-onset Alzheimer’s disease. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 156B(4), 507–512 (2011).
  • Wijsman EM, Pankratz ND, Choi Y et al. Genome-wide association of familial late-onset Alzheimer’s disease replicates BIN1 and CLU and nominates CUGBP2 in interaction with APOE. PLoS Genet. 7(2), e1001308 (2011).
  • Kamboh MI, Demirci FY, Wang X et al. Genome-wide association study of Alzheimer’s disease. Transl. Psychiatry 2, e117 (2012).
  • Kamboh MI, Barmada MM, Demirci FY et al. Genome-wide association analysis of age-at-onset in Alzheimer’s disease. Mol. Psychiatry 17(12), 1340–1346 (2012).
  • Saunders AM, Strittmatter WJ, Schmechel D et al. Association of apolipoprotein E allele 4 with late-onset familial and sporadic Alzheimer’s disease. Neurology 43(8), 1467–1467 (1993).
  • Apolipoprotein E genotyping in Alzheimer’s disease. National Institute on Aging/Alzheimer’s Association Working Group . Lancet 347(9008), 1091–1095 (1996).
  • Sando SB, Melquist S, Cannon A et al. APOE epsilon 4 lowers age at onset and is a high risk factor for Alzheimer’s DISEASE;ACASECONTROLSTUDYFROMCENTRALNORWAY.BMC Neurol. 8, 9 (2008).
  • Yoshizawa T, Yamakawa-Kobayashi K, Komatsuzaki Y et al. Dose-dependent association of apolipoprotein E allele epsilon 4 with late-onset, sporadic Alzheimer’s disease. Ann. Neurol. 36(4), 656–659 (1994).
  • Brousseau T, Legrain S, Berr C, Gourlet V, Vidal O, Amouyel P. Confirmation of the epsilon 4 allele of the apolipoprotein E gene as a risk factor for late-onset Alzheimer’s disease. Neurology 44(2), 342–344 (1994).
  • Corder EH, Saunders AM, Strittmatter WJ et al. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer’s disease in late onset families. Science 261(5123), 921–923 (1993).
  • Poirier J, Davignon J, Bouthillier D, Kogan S, Bertrand P, Gauthier S. Apolipoprotein E polymorphism and Alzheimer’s disease. Lancet 342(8873), 697–699 (1993).
  • Gomez-Isla T, West HL, Rebeck GW et al. Clinical and pathological correlates of apolipoprotein E epsilon 4 in Alzheimer’s disease. Ann. Neurol. 39(1), 62–70 (1996).
  • Dai XY, Nanko S, Hattori M et al. Association of apolipoprotein E4 with sporadic Alzheimer’s disease is more pronounced in early onset type. Neurosci. Lett. 175(1–2), 74–76 (1994).
  • Hyman BT, Gomez-Isla T, Rebeck GW et al. Epidemiological, clinical, and neuropathological study of apolipoprotein E genotype in Alzheimer’s disease. Ann. NY Acad. Sci. 802, 1–5 (1996).
  • Corder EH, Saunders AM, Risch NJ et al. Protective effect of apolipoprotein E type 2 allele for late onset Alzheimer disease. Nat. Genet. 7(2), 180–184 (1994).
  • Kok E, Haikonen S, Luoto T et al. Apolipoprotein E-dependent accumulation of Alzheimer disease-related lesions begins in middle age. Ann. Neurol. 65(6), 650–657 (2009).
  • Polvikoski T, Sulkava R, Haltia M et al. Apolipoprotein E, dementia, and cortical deposition of beta-amyloid protein. N. Engl. J. Med. 333(19), 1242–1247 (1995).
  • Schmechel DE, Saunders AM, Strittmatter WJ et al. Increased amyloid beta-peptide deposition in cerebral cortex as a consequence of apolipoprotein E genotype in late-onset Alzheimer disease. Proc. Natl Acad. Sci. USA 90(20), 9649–9653 (1993).
  • Tiraboschi P, Hansen LA, Masliah E, Alford M, Thal LJ, Corey-Bloom J. Impact of APOE genotype on neuropathologic and neurochemical markers of Alzheimer disease. Neurology 62(11), 1977–1983 (2004).
  • Hultman K, Strickland S, Norris EH. The APOE 4/4 genotype potentiates vascular fibrin(ogen) deposition in amyloid-laden vessels in the brains of Alzheimer’s disease patients. J. Cereb. Blood Flow Metab. 33(8), 1251–1258 (2013).
  • Sunderland T, Mirza N, Putnam KT et al. Cerebrospinal fluid beta-amyloid1–42 and tau in control subjects at risk for Alzheimer’s disease: the effect of APOE epsilon4 allele. Biol. Psychiatry 56(9), 670–676 (2004).
  • Morris JC, Roe CM, Xiong C et al. APOE predicts amyloid-beta but not tau Alzheimer pathology in cognitively normal aging. Ann. Neurol. 67(1), 122–131 (2010).
  • Fagan AM, Mintun MA, Mach RH et al. Inverse relation between in vivo amyloid imaging load and cerebrospinal fluid Abeta42 in humans. Ann. Neurol. 59(3), 512–519 (2006).
  • Risacher SL, Saykin AJ. Neuroimaging and other biomarkers for Alzheimer’s disease: the changing landscape of early detection. Annu. Rev. Clin. Psychol. 9, 621–648 (2013).
  • Ramanan VK, Risacher SL, Nho K et al. APOE and BCHE as modulators of cerebral amyloid deposition: a florbetapir PET genome-wide association study. Mol. Psychiatry 19(3), 351–357 (2014).
  • Rebeck GW, Reiter JS, Strickland DK, Hyman BT. Apolipoprotein E in sporadic Alzheimer’s disease: allelic variation and receptor interactions. Neuron 11(4), 575–580 (1993).
  • Shao Y, Gearing M, Mirra SS. Astrocyte-apolipoprotein E associations in senile plaques in Alzheimer disease and vascular lesions: a regional immunohistochemical study. J. Neuropathol. Exp. Neurol. 56(4), 376–381 (1997).
  • Namba Y, Tomonaga M, Kawasaki H, Otomo E, Ikeda K. Apolipoprotein E immunoreactivity in cerebral amyloid deposits and neurofibrillary tangles in Alzheimer’s disease and kuru plaque amyloid in Creutzfeldt-Jakob disease. Brain Res. 541(1), 163–166 (1991).
  • Wisniewski T, Frangione B. Apolipoprotein E: a pathological chaperone protein in patients with cerebral and systemic amyloid. Neurosci. Lett. 135(2), 235–238 (1992).
  • LaDu MJ, Falduto MT, Manelli AM, Reardon CA, Getz GS, Frail DE. Isoform-specific binding of apolipoprotein E to beta-amyloid. J. Biol. Chem. 269(38), 23403–23406 (1994).
  • LaDu MJ, Pederson TM, Frail DE, Reardon CA, Getz GS, Falduto MT. Purification of apolipoprotein E attenuates isoform-specific binding to beta-amyloid. J. Biol. Chem. 270(16), 9039–9042 (1995).
  • Strittmatter WJ, Saunders AM, Schmechel D et al. Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc. Natl Acad. Sci. USA 90(5), 1977–1981 (1993).
  • Wisniewski T, Golabek A, Matsubara E, Ghiso J, Frangione B. Apolipoprotein E: binding to soluble Alzheimer’s beta-amyloid. Biochem. Biophys. Res. Commun. 192(2), 359–365 (1993).
  • Sanan DA, Weisgraber KH, Russell SJ et al. Apolipoprotein E associates with beta amyloid peptide of Alzheimer’s disease to form novel monofibrils. Isoform apoE4 associates more efficiently than apoE3. J. Clin. Invest. 94(2), 860–869 (1994).
  • Aleshkov S, Abraham CR, Zannis VI. Interaction of nascent ApoE2, ApoE3, and ApoE4 isoforms expressed in mammalian cells with amyloid peptide beta (1–40). Relevance to Alzheimer’s disease. Biochemistry 36(34), 10571–10580 (1997).
  • Yang DS, Smith JD, Zhou Z, Gandy SE, Martins RN. Characterization of the binding of amyloid-beta peptide to cell culture-derived native apolipoprotein E2, E3, and E4 isoforms and to isoforms from human plasma. J. Neurochem. 68(2), 721–725 (1997).
  • Hashimoto T, Serrano-Pozo A, Hori Y et al. Apolipoprotein E, especially apolipoprotein E4, increases the oligomerization of amyloid β peptide. J. Neurosci. 32(43), 15181–15192 (2012).
  • Verghese PB, Castellano JM, Garai K et al. ApoE influences amyloid-β (Aβ) clearance despite minimal apoE/Aβ association in physiological conditions. Proc. Natl Acad. Sci. USA 110(19), E1807–E1816 (2013).
  • Deane R, Sagare A, Hamm K et al. apoE isoform-specific disruption of amyloid beta peptide clearance from mouse brain. J. Clin. Invest. 118(12), 4002–4013 (2008).
  • Bales KR, Verina T, Dodel RC et al. Lack of apolipoprotein E dramatically reduces amyloid beta-peptide deposition. Nat. Genet. 17(3), 263–264 (1997).
  • Bien-Ly N, Gillespie AK, Walker D, Yoon SY, Huang Y. Reducing human apolipoprotein E levels attenuates age-dependent Aβ accumulation in mutant human amyloid precursor protein transgenic mice. J. Neurosci. 32(14), 4803–4811 (2012).
  • Kim J, Jiang H, Park S et al. Haploinsufficiency of human APOE reduces amyloid deposition in a mouse model of amyloid-β amyloidosis. J. Neurosci. 31(49), 18007–18012 (2011).
  • Garai K, Verghese PB, Baban B, Holtzman DM, Frieden C. The binding of apoE to oligomers and fibrils of amyloid-β alters the kinetics of amyloid aggregation. Biochemistry 53(40), 6323–6331 (2014).
  • Nagy Z, Esiri MM, Jobst KA et al. Influence of the apolipoprotein E genotype on amyloid deposition and neurofibrillary tangle formation in Alzheimer’s disease. Neuroscience 69(3), 757–761 (1995).
  • Ohm TG, Scharnagl H, März W, Bohl J. Apolipoprotein E isoforms and the development of low and high Braak stages of Alzheimer’s disease-related lesions. Acta Neuropathol. 98(3), 273–280 (1999).
  • Huang Y, Liu XQ, Wyss-Coray T, Brecht WJ, Sanan DA, Mahley RW. Apolipoprotein E fragments present in Alzheimer’s disease brains induce neurofibrillary tangle-like intracellular inclusions in neurons. Proc. Natl Acad. Sci. USA 98(15), 8838–8843 (2001).
  • Rohn TT, Catlin LW, Coonse KG, Habig JW. Identification of an amino-terminal fragment of apolipoprotein E4 that localizes to neurofibrillary tangles of the Alzheimer’s disease brain. Brain Res. 1475, 106–115 (2012).
  • Blomberg M, Jensen M, Basun H, Lannfelt L, Wahlund LO. Increasing cerebrospinal fluid tau levels in a subgroup of Alzheimer patients with apolipoprotein E allele epsilon 4 during 14 months follow-up. Neurosci. Lett. 214(2–3), 163–166 (1996).
  • Huey ED, Mirza N, Putnam KT et al. Stability of CSF beta-amyloid(1–42) and tau levels by APOE genotype in Alzheimer patients. Dement. Geriatr. Cogn. Disord. 22(1), 48–53 (2006).
  • Sacre SM, Stannard AK, Owen JS. Apolipoprotein E (apoE) isoforms differentially induce nitric oxide production in endothelial cells. FEBS Lett. 540(1–3), 181–187 (2003).
  • Hafezi-Moghadam A, Thomas KL, Wagner DD. ApoE deficiency leads to a progressive age-dependent blood–brain barrier leakage. Am. J. Physiol. Cell Physiol. 292(4), C1256–C1262 (2007).
  • Nishitsuji K, Hosono T, Nakamura T, Bu G, Michikawa M. Apolipoprotein E regulates the integrity of tight junctions in an isoform-dependent manner in an in vitro blood–brain barrier model. J. Biol. Chem. 286(20), 17536–17542 (2011).
  • Di Angelantonio E, Sarwar N, Perry P et al. Major lipids, apolipoproteins, and risk of vascular disease. JAMA 302(18), 1993–2000 (2009).
  • Kawano M, Kawakami M, Otsuka M, Yashima H, Yaginuma T, Ueki A. Marked decrease of plasma apolipoprotein AI and AII in Japanese patients with late-onset non-familial Alzheimer’s disease. Clin. Chim. Acta 239(2), 209–211 (1995).
  • Kuriyama M, Takahashi K, Yamano T et al. Low levels of serum apolipoprotein A I and A II in senile dementia. Jpn J. Psychiatry Neurol. 48(3), 589–593 (1994).
  • Merched A, Xia Y, Visvikis S, Serot JM, Siest G. Decreased high-density lipoprotein cholesterol and serum apolipoprotein AI concentrations are highly correlated with the severity of Alzheimer’s disease. Neurobiol. Aging 21(1), 27–30 (2000).
  • Vollbach H, Heun R, Morris CM et al. APOA1 polymorphism influences risk for early-onset nonfamiliar AD. Ann. Neurol. 58(3), 436–441 (2005).
  • Smach MA, Edziri H, Charfeddine B et al. Polymorphism in apoA1 influences high-density lipoprotein cholesterol levels but is not a major risk factor of alzheimer’s disease. Dement. Geriatr. Cogn. Dis. Extra 1(1), 249–257 (2011).
  • Puchades M, Hansson SF, Nilsson CL, Andreasen N, Blennow K, Davidsson P. Proteomic studies of potential cerebrospinal fluid protein markers for Alzheimer’s disease. Brain Res. Mol. Brain Res. 118(1–2), 140–146 (2003).
  • Roher AE, Maarouf CL, Sue LI, Hu Y, Wilson J, Beach TG. Proteomics-derived cerebrospinal fluid markers of autopsy-confirmed Alzheimer’s disease. Biomarkers 14(7), 493–501 (2009).
  • Castaño EM, Roher AE, Esh CL, Kokjohn TA, Beach T. Comparative proteomics of cerebrospinal fluid in neuropathologically-confirmed Alzheimer’s disease and non-demented elderly subjects. Neurol. Res. 28(2), 155–163 (2006).
  • Song H, Saito K, Seishima M, Noma A, Urakami K, Nakashima K. Cerebrospinal fluid apo E and apo A-I concentrations in early- and late-onset Alzheimer’s disease. Neurosci. Lett. 231(3), 175–178 (1997).
  • Harr SD, Uint L, Hollister R, Hyman BT, Mendez AJ. Brain expression of apolipoproteins E, J, and A-I in Alzheimer’s disease. J. Neurochem. 66(6), 2429–2435 (1996).
  • Lefterov I, Fitz NF, Cronican AA et al. Apolipoprotein A-I deficiency increases cerebral amyloid angiopathy and cognitive deficits in APP/PS1DeltaE9 mice. J. Biol. Chem. 285(47), 36945–36957 (2010).
  • Lewis TL, Cao D, Lu H et al. Overexpression of human apolipoprotein A-I preserves cognitive function and attenuates neuroinflammation and cerebral amyloid angiopathy in a mouse model of Alzheimer disease. J. Biol. Chem. 285(47), 36958–36968 (2010).
  • Paula-Lima AC, Tricerri MA, Brito-Moreira J et al. Human apolipoprotein A-I binds amyloid-beta and prevents Abetainduced neurotoxicity. Int. J. Biochem. Cell Biol. 41(6), 1361–1370 (2009).
  • Borja MS, Zhao L, Hammerson B et al. HDL-apoA-I exchange: rapid detection and association with atherosclerosis. PLoS ONE 8(8), e71541 (2013).
  • Shao B, Oda MN, Oram JF, Heinecke JW. Myeloperoxidase: an oxidative pathway for generating dysfunctional high-density lipoprotein. Chem. Res. Toxicol. 23(3), 447–454 (2010).
  • Shao B, Tang C, Heinecke JW, Oram JF. Oxidation of apolipoprotein A-I by myeloperoxidase impairs the initial interactions with ABCA1 required for signaling and cholesterol export. J. Lipid Res. 51(7), 1849–1858 (2010).
  • Wu Z-C, Yu J-T, Li Y, Tan L. Clusterin in Alzheimer’s disease. Adv. Clin. Chem. 56, 155–173 (2012).
  • Fan J, Stukas S, Wong C et al. An ABCA1-independent pathway for recycling a poorly lipidated 8.1 nm apolipoprotein E particle from glia. J. Lipid Res. 52(9), 1605–1616 (2011).
  • Wilson MR, Yerbury JJ, Poon S. Potential roles of abundant extracellular chaperones in the control of amyloid formation and toxicity. Mol. Biosyst. 4(1), 42–52 (2008).
  • DeMattos RB, Cirrito JR, Parsadanian M et al. ApoE and clusterin cooperatively suppress Abeta levels and deposition: evidence that ApoE regulates extracellular Abeta metabolism in vivo. Neuron. 41(2), 193–202 (2004).
  • Cole GM, Ard MD. Influence of lipoproteins on microglial degradation of Alzheimer’s amyloid beta-protein. Microsc. Res. Tech. 50(4), 316–324 (2000).
  • Hammad SM, Ranganathan S, Loukinova E, Twal WO, Argraves WS. Interaction of apolipoprotein J-amyloid beta-peptide complex with low density lipoprotein receptor-related protein-2/megalin. A mechanism to prevent pathological accumulation of amyloid beta-peptide. J. Biol. Chem. 272(30), 18644–18649 (1997).
  • 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. 271(1), 130–141 (2001).
  • Kirszbaum L, Bozas SE, Walker ID. SP-40,40, a protein involved in the control of the complement pathway, possesses a unique array of disulphide bridges. FEBS Lett. 297(1–2), 70–76 (1992).
  • Kang S-W, Shin Y-J, Shim Y-J, Jeong S-Y, Park I-S, Min B-H. Clusterin interacts with SCLIP (SCG10-like protein) and promotes neurite outgrowth of PC12 cells. Exp. Cell Res. 309(2), 305–315 (2005).
  • Sarma JV, Ward PA. The complement system. Cell Tissue Res. 343(1), 227–235 (2011).
  • Crehan H, Holton P, Wray S, Pocock J, Guerreiro R, Hardy J. Complement receptor 1 (CR1) and Alzheimer’s disease. Immunobiology 217(2), 244–250 (2012). •• Provides detailed information regarding the genetic and protein structure of the complement receptor 1, and how its polymorphism may influence AD risk.
  • Eikelenboom P, van Exel E, Veerhuis R, Rozemuller AJM, van Gool WA, Hoozemans JJM. Innate immunity and the etiology of late-onset Alzheimer’s disease. Neurodegener. Dis. 10(1–4), 271–273 (2012).
  • Eikelenboom P, Stam FC. An immunohistochemical study on cerebral vascular and senile plaque amyloid in Alzheimer’s dementia. Virchows Arch. B Cell Pathol. Incl. Mol. Pathol. 47(1), 17–25 (1984).
  • McGeer PL, Akiyama H, Itagaki S, McGeer EG. Activation of the classical complement pathway in brain tissue of Alzheimer patients. Neurosci. Lett. 107(1–3), 341–346 (1989).
  • Rogers J, Schultz J, Brachova L et al. Complement activation and beta-amyloid-mediated neurotoxicity in Alzheimer’s disease. Res. Immunol. 143(6), 624–630 (1992).
  • Fan R, DeFilippis K, Van Nostrand WE. Induction of complement proteins in a mouse model for cerebral microvascular A beta deposition. J. Neuroinflammation. 4, 22 (2007).
  • Wirz KTS, Bossers K, Stargardt A et al. Cortical beta amyloid protein triggers an immune response, but no synaptic changes in the APPswe/PS1dE9 Alzheimer’s disease mouse model. Neurobiol. Aging 34(5), 1328–1342 (2013).
  • Strohmeyer R, Shen Y, Rogers J. Detection of complement alternative pathway mRNA and proteins in the Alzheimer’s disease brain. Brain Res. Mol. Brain Res. 81(1–2), 7–18 (2000).
  • Yasojima K, Schwab C, McGeer EG, McGeer PL. Up-regulated production and activation of the complement system in Alzheimer’s disease brain. Am. J. Pathol. 154(3), 927–936 (1999).
  • Watson MD, Roher AE, Kim KS, Spiegel K, Emmerlin MR. Complement interactions with amyloid β1–42: a nidus for inflammation in AD brains. Amyloid 4(3), 147–156 (1997).
  • Smyth MD, Cribbs DH, Tenner AJ et al. Decreased levels of C1q in cerebrospinal fluid of living Alzheimer patients correlate with disease state. Neurobiol. Aging 15(5), 609–614.
  • Fonseca MI, Zhou J, Botto M, Tenner AJ. Absence of C1q leads to less neuropathology in transgenic mouse models of Alzheimer’s disease. J. Neurosci. 24(29), 6457–6465 (2004).
  • Wyss-Coray T, Yan F, Lin AH-T et al. Prominent neurodegeneration and increased plaque formation in complement-inhibited Alzheimer’s mice. Proc. Natl Acad. Sci. USA 99(16), 10837–10842 (2002).
  • Maier M, Peng Y, Jiang L, Seabrook TJ, Carroll MC, Lemere CA. Complement C3 deficiency leads to accelerated amyloid beta plaque deposition and neurodegeneration and modulation of the microglia/macrophage phenotype in amyloid precursor protein transgenic mice. J. Neurosci. 28(25), 6333–6341 (2008).
  • Thambisetty M, Simmons A, Velayudhan L et al. Association of plasma clusterin concentration with severity, pathology, and progression in Alzheimer disease. Arch. Gen. Psychiatry 67(7), 739–748 (2010).
  • Zhang R, Barker L, Pinchev D et al. Mining biomarkers in human sera using proteomic tools. Proteomics 4(1), 244–256 (2004).
  • Kiddle SJ, Thambisetty M, Simmons A et al. Plasma based markers of [11C] PiB-PET brain amyloid burden. PLoS ONE 7(9), e44260 (2012).
  • Hye A, Lynham S, Thambisetty M et al. Proteome-based plasma biomarkers for Alzheimer’s disease. Brain 129(Pt 11), 3042–3050 (2006).
  • Thambisetty M, Hye A, Foy C et al. Proteome-based identification of plasma proteins associated with hippocampal metabolism in early Alzheimer’s disease. J. Neurol. 255(11), 1712–1720 (2008).
  • Schwartz M, Baruch K. The resolution of neuroinflammation in neurodegeneration: leukocyte recruitment via the choroid plexus. EMBO J. 33(1), 7–22 (2014).
  • Hoozemans JJM, Rozemuller AJM, van Haastert ES, Eikelenboom P, van Gool WA. Neuroinflammation in Alzheimer’s disease wanes with age. J. Neuroinflammation. 8, 171 (2011).
  • Khovidhunkit W, Kim M-S, Memon RA et al. Effects of infection and inflammation on lipid and lipoprotein metabolism: mechanisms and consequences to the host. J. Lipid Res. 45(7), 1169–1196 (2004).
  • Kindy MS, Yu J, Guo J-T, Zhu H. Apolipoprotein serum amyloid A in alzheimer’s disease. J. Alzheimers. Dis. 1(3), 155–167 (1999).
  • Miida T, Yamada T, Seino U et al. Serum amyloid A (SAA)-induced remodeling of CSF-HDL. Biochim. Biophys. Acta 1761(4), 424–433 (2006).
  • Tölle M, Huang T, Schuchardt M et al. High-density lipoprotein loses its anti-inflammatory capacity by accumulation of pro-inflammatory-serum amyloid A. Cardiovasc. Res. 94(1), 154–162 (2012).
  • Cortes-Canteli M, Paul J, Norris EH et al. Fibrinogen and beta-amyloid association alters thrombosis and fibrinolysis: a possible contributing factor to Alzheimer’s disease. Neuron 66(5), 695–709 (2010).
  • Jantaratnotai N, Schwab C, Ryu JK, McGeer PL, McLarnon JG. Converging perturbed microvasculature and microglial clusters characterize Alzheimer disease brain. Curr. Alzheimer Res. 7(7), 625–636 (2010).
  • Ahn HJ, Zamolodchikov D, Cortes-Canteli M, Norris EH, Glickman JF, Strickland S. Alzheimer’s disease peptide beta-amyloid interacts with fibrinogen and induces its oligomerization. Proc. Natl Acad. Sci. USA 107(50), 21812–21817 (2010).
  • Cortes-Canteli M, Zamolodchikov D, Ahn HJ, Strickland S, Norris EH. Fibrinogen and altered hemostasis in Alzheimer’s disease. J. Alzheimers Dis. 32(3), 599–608 (2012).
  • Paul J, Strickland S, Melchor JP. Fibrin deposition accelerates neurovascular damage and neuroinflammation in mouse models of Alzheimer’s disease. J. Exp. Med. 204(8), 1999–2008 (2007).
  • Piers TM, Heales SJ, Pocock JM. Positive allosteric modulation of metabotropic glutamate receptor 5 down-regulates fibrinogen-activated microglia providing neuronal protection. Neurosci. Lett. 505(2), 140–145 (2011).
  • Ryu JK, McLarnon JG. A leaky blood–brain barrier, fibrinogen infiltration and microglial reactivity in inflamed Alzheimer’s disease brain. J. Cell. Mol. Med. 13(9A), 2911–2925 (2009).
  • Arai T, Miklossy J, Klegeris A, Guo J-P, McGeer PL. Thrombin and prothrombin are expressed by neurons and glial cells and accumulate in neurofibrillary tangles in Alzheimer disease brain. J. Neuropathol. Exp. Neurol. 65(1), 19–25 (2006).
  • Akiyama H, Ikeda K, Kondo H, McGeer PL. Thrombin accumulation in brains of patients with Alzheimer’s disease. Neurosci. Lett. 146(2), 152–154 (1992).
  • Tripathy D, Sanchez A, Yin X, Luo J, Martinez J, Grammas P. Thrombin, a mediator of cerebrovascular inflammation in AD and hypoxia. Front. Aging Neurosci. 5, 19 (2013).
  • Arai T, Guo J-P, McGeer PL. Proteolysis of nonphosphorylated and phosphorylated tau by thrombin. J. Biol. Chem. 280(7), 5145–5153 (2005).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.