Apolipoprotein e increases cell association of amyloid-β 40 through heparan sulfate and LRP1 dependent pathways

Amyloid

Volumn 21, Issue 2, 2014, Pages 76-87

  O'Callaghan, Paul ^a,b   Noborn, Fredrik ^b   Sehlin, Dag ^a   Li, Jin Ping ^b   Lannfelt, Lars ^a   Lindahl, Ulf ^b   Zhang, Xiao ^a,b  

^a UPPSALA UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

Amyloid ; Apolipoprotein E; Cell association; Heparan sulfate; Low density lipoprotein receptor related protein 1

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; APOLIPOPROTEIN E; APOLIPOPROTEIN E4; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; PROTEOHEPARAN SULFATE; AMYLOID BETA PROTEIN; HEPARAN SULFATE; LRP1 PROTEIN, HUMAN; PROTEIN BINDING;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; BIOACCUMULATION; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; CEREBROSPINAL FLUID; CHO CELL LINE; CONTROLLED STUDY; DOWN SYNDROME; HOMEOSTASIS; HUMAN; HUMAN TISSUE; NONHUMAN; PARENCHYMA; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; RISK FACTOR; TRANSCYTOSIS; BRAIN; HIPPOCAMPUS; IN VITRO STUDY; METABOLISM; MICROVASCULATURE; PATHOLOGY;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; APOLIPOPROTEINS E; BRAIN; HEPARITIN SULFATE; HIPPOCAMPUS; HUMANS; IN VITRO TECHNIQUES; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; MICROVESSELS; PROTEIN BINDING;

EID: 84900556912     PISSN: 13506129     EISSN: 17442818     Source Type: Journal    
DOI: 10.3109/13506129.2013.879643     Document Type: Article

References (61)

1. Mawuenyega KG, Sigurdson W, Ovod V, Munsell L, Kasten T, Morris JC, Yarasheski KE, et al. Decreased clearance of CNS beta-amyloid in Alzheimer's disease. Science 2010; 330: 1774.
2. Castellano JM, Kim J, Stewart FR, Jiang H, DeMattos RB, Patterson BW, Fagan AM, et al. Human apoE isoforms differentially regulate brain amyloid-beta peptide clearance. Science Transl Med 2011; 3: 89ra57.
3. Bu G. Apolipoprotein E and its receptors in Alzheimer's disease: pathways, pathogenesis and therapy. Nat Rev Neurosci 2009; 10: 333-44.
4. Tokuda T, Calero M, Matsubara E, Vidal R, Kumar A, Permanne B, Zlokovic B, et al. Lipidation of apolipoprotein E influences its isoform-specific interaction with Alzheimer's amyloid beta peptides. Biochem J 2000; 348: 359-65.
5. Weisgraber KH, Rall SC, Mahley RW. Human E apoprotein heterogeneity. Cysteine-arginine interchanges in the amino acid sequence of the apo-E isoforms. J Biol Chem 1981; 256: 9077-83.
6. Zhong N, Weisgraber KH. Understanding the association of apolipoprotein E4 with Alzheimer disease: clues from its structure. J Biol Chem 2009; 284: 6027-31.
7. Fuentealba RA, Liu Q, Zhang J, Kanekiyo T, Hu X, Lee JM, LaDu MJ, et al. Low-density lipoprotein receptor-related protein 1 (LRP1) mediates neuronal Abeta42 uptake and lysosomal trafficking. PLoS One 2010; 5: e11884.
8. Sandwall E, O'Callaghan P, Zhang X, Lindahl U, Lannfelt L, Li JP. Heparan sulfate mediates amyloid-beta internalization and cytotoxicity. Glycobiology 2010; 20: 533-41.
9. Kanekiyo T, Zhang J, Liu Q, Liu CC, Zhang L, Bu G. Heparan sulphate proteoglycan and the low-density lipoprotein receptorrelated protein 1 constitute major pathways for neuronal amyloidbeta uptake. J Neurosci 2011; 31: 1644-51.
10. Giulian D, Haverkamp LJ, Yu J, Karshin W, Tom D, Li J, Kazanskaia A, et al. The HHQK domain of beta-amyloid provides a structural basis for the immunopathology of Alzheimer's disease. J Biol Chem 1998; 273: 29719-26.
11. Lindahl B, Westling C, Giménez-Gallego G, Lindahl U, Salmivirta M. Common binding sites for b-amyloid fibrils and fibroblast growth factor-2 in heparan sulfate from human cerebral cortex. J Biol Chem 1999; 274: 30631-5.
12. Woods AG, Cribbs DH, Whittemore ER, Cotman CW. Heparan sulfate and chondroitin sulfate glycosaminoglycan attenuate b-amyloid(25-35) induced neurodegeneration in cultured hippocampal neurons. Brain Res 1995; 697: 53-62.
13. Timmer NM, Schirris TJJ, Bruinsma IB, Otte-Höller I, van Kuppevelt TH, de Waal RMW, Verbeek MM. Aggregation and cytotoxic properties towards cultured cerebrovascular cells of Dutch-mutated Ab40 (DAb1-40) are modulated by sulfate moieties of heparin. Neurosci Res 2009; 66: 380-9.
14. Deane R, Wu Z, Sagare A, Davis J, Du Yan S, Hamm K, Xu F, et al. LRP/amyloid beta-peptide interaction mediates differential brain efflux of Abeta isoforms. Neuron 2004; 43: 333-44.
15. Bell RD, Deane R, Chow N, Long X, Sagare A, Singh I, Streb JW, et al. SRF and myocardin regulate LRP-mediated amyloid-beta clearance in brain vascular cells. Nat Cell Biol 2009; 11: 143-53.
16. Pflanzner T, Janko MC, Andre-Dohmen B, Reuss S, Weggen S, Roebroek AJ, Kuhlmann CR, et al. LRP1 mediates bidirectional transcytosis of amyloid-beta across the blood-brain barrier. Neurobiol Aging 2011; 32: 2323.e1-11.
17. Nazer B, Hong S, Selkoe DJ. LRP promotes endocytosis and degradation, but not transcytosis, of the amyloid-[beta] peptide in a blood-brain barrier in vitro model. Neurobiol Dis 2008; 30: 94-102.
18. Shibata M, Yamada S, Kumar SR, Calero M, Bading J, Frangione B, Holtzman DM, et al. Clearance of Alzheimer's amyloid-b1-40 peptide from brain by LDL receptor-related protein-1 at the bloodbrain barrier. J Clin Invest 2000; 106: 1489-99.
19. Cardin AD, Hirose N, Blankenship DT, Jackson RL, Harmony JA, Sparrow DA, Sparrow JT. Binding of a high reactive heparin to human apolipoprotein E: identification of two heparin-binding domains. Biochem Biophys Res Commun 1986; 134: 783-9.
20. Yamauchi Y, Deguchi N, Takagi C, Tanaka M, Dhanasekaran P, Nakano M, Handa T, et al. Role of the N- and C-terminal domains in binding of apolipoprotein E isoforms to heparan sulfate and dermatan sulfate: a surface plasmon resonance study. Biochemistry (Mosc) 2008; 47: 6702-10.
21. Mahley RW, Ji Z-S. Remnant lipoprotein metabolism: key pathways involving cell-surface heparan sulfate proteoglycans and apolipoprotein E. J Lipid Res 1999; 40: 1-16.
22. Wilsie LC, Orlando RA. The low density lipoprotein receptorrelated protein complexes with cell surface heparan sulfate proteoglycans to regulate proteoglycan-mediated lipoprotein catabolism. J Biol Chem 2003; 278: 15758-64.
23. Holtzman DM, Bales KR, Tenkova T, Fagan AM, Parsadanian M, Sartorius LJ, Mackey B, et al. Apolipoprotein E isoform-dependent amyloid deposition and neuritic degeneration in a mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 2000; 97: 2892-7.
24. Jiang Q, Lee CY, Mandrekar S, Wilkinson B, Cramer P, Zelcer N, Mann K, et al. ApoE promotes the proteolytic degradation of Abeta. Neuron 2008; 58: 681-93.
25. Bruinsma IB, Wilhelmus MMM, Kox M, Veerhuis R, de Waal RMW, Verbeek MM. Apolipoprotein E protects cultured pericytes and astrocytes from D-Abeta 1-40-mediated cell death. Brain Res 2010; 1315: 169-80.
26. Bruinsma I, te Riet L, Gevers T, ten Dam G, van Kuppevelt T, David G, Küsters B, et al. Sulfation of heparan sulfate associated with amyloid-b plaques in patients with Alzheimer's disease. Acta Neuropathol (Berl) 2010; 119: 211-20.
27. Näslund J, Haroutunian V, Mohs R, Davis KL, Davies P, Greengard P, Buxbaum JD. Correlation between elevated levels of amyloid b-peptide in the brain and cognitive decline. JAMA 2000; 283: 1571-7.
28. Sehlin D, Hedlund M, Lord A, Englund H, Gellerfors P, Paulie S, Lannfelt L, et al. Heavy-chain complementarity-determining regions determine conformation selectivity of anti-Ab antibodies. Neurodegener Dis 2011; 8: 117-23.
29. Englund H, Sehlin D, Johansson A-S, Nilsson LNG, Gellerfors P, Paulie S, Lannfelt L, et al. Sensitive ELISA detection of amyloid-b protofibrils in biological samples. J Neurochem 2007; 103: 334-45.
30. Staatz WD, Toyoda H, Kinoshita-Toyoda A, Chhor K, Selleck SB. Analysis of proteoglycans and glycosaminoglycans from Drosophila. Methods Mol Biol 2001; 171: 41-52.
31. Hook GE, Gilmore LB. Hydrolases of pulmonary lysosomes and lamellar bodies. J Biol Chem 1982; 257: 9211-20.
32. Kreuger J, Lindahl U, Jemth P. Nitrocellulose filter binding to assess binding of glycosaminoglycans to proteins. Meth Enzymol 2003; 363: 327-39.
33. Donahue J, Flaherty S, Johanson C, Duncan J, Silverberg G, Miller M, Tavares R, et al. RAGE, LRP-1, and amyloid-beta protein in Alzheimer's disease. Acta Neuropathol (Berl) 2006; 112: 405-15.
34. O'Callaghan P, Sandwall E, Li J-P, Yu H, Ravid R, Guan Z-Z, Van Kuppevelt TH, et al. Heparan sulfate accumulation with Ab deposits in Alzheimer's disease and Tg2576 mice is contributed by glial cells. Brain Pathol 2008; 18: 548-61.
35. Yamada K, Hashimoto T, Yabuki C, Nagae Y, Tachikawa M, Strickland DK, Liu Q, et al. The low density lipoprotein receptorrelated protein 1 mediates uptake of amyloid beta peptides in an in vitro model of the blood-brain barrier cells. J Biol Chem 2008; 283: 34554-62.
36. Lemere CA, Blusztajn JK, Yamaguchi H, Wisniewski T, Saido TC, Selkoe DJ. Sequence of deposition of heterogeneous amyloid b-peptides and ApoE in Down Syndrome: implications for initial events in amyloid plaque formation. Neurobiol Dis 1996; 3: 16-32.
37. Gearing M, Schneider JA, Robbins RS, Hollister RD, Mori H, Games D, Hyman BT, et al. Regional variation in the distribution of apolipoprotein E and Abeta in Alzheimer's disease. J Neuropathol Exp Neurol 1995; 54: 833-41.
38. Marques MA, Tolar M, Harmony JA, Crutcher KA. A thrombin cleavage fragment of apolipoprotein E exhibits isoform-specific neurotoxicity. Neuroreport 1996; 7: 2529-32.
39. Tolar M, Marques MA, Harmony JA, Crutcher KA. Neurotoxicity of the 22 kDa thrombin-cleavage fragment of apolipoprotein E and related synthetic peptides is receptor-mediated. J Neurosci 1997; 17: 5678-86.
40. Li J, Kanekiyo T, Shinohara M, Zhang Y, LaDu MJ, Xu H, Bu G. Differential regulation of amyloid-b endocytic trafficking and lysosomal degradation by apolipoprotein E isoforms. J Biol Chem 2012; 287: 44593-601.
41. Chen J, Li Q, Wang J. Topology of human apolipoprotein E3 uniquely regulates its diverse biological functions. Proc Natl Acad Sci USA 2011; 108: 14813-18.
42. Strittmatter WJ, Weisgraber KH, Huang DY, Dong LM, Salvesen GS, Pericak-Vance M, Schmechel D, et al. Binding of human apolipoprotein E to synthetic amyloid beta peptide: isoformspecific effects and implications for late-onset Alzheimer disease. Proc Natl Acad Sci USA 1993; 90: 8098-102.
43. Naslund J, Thyberg J, Tjernberg LO, Wernstedt C, Karlstrom AR, Bogdanovic N, Gandy SE, et al. Characterization of stable complexes involving apolipoprotein E and the amyloid beta peptide in Alzheimer's disease brain. Neuron 1995; 15: 219-28.
44. Wolburg H, Noell S, Mack A, Wolburg-Buchholz K, Fallier-Becker P. Brain endothelial cells and the glio-vascular complex. Cell Tissue Res 2009; 335: 75-96.
45. Zlokovic BV. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008; 57: 178-201.
46. Deane R, Sagare A, Hamm K, Parisi M, Lane S, Finn MB, Holtzman DM, et al. apoE isoform specific disruption of amyloid beta peptide clearance from mouse brain. J Clin Invest 2008; 118: 4002-13.
47. Wu Z, Guo H, Chow N, Sallstrom J, Bell RD, Deane R, Brooks AI, et al. Role of the MEOX2 homeobox gene in neurovascular dysfunction in Alzheimer disease. Nat Med 2005; 11: 959-65.
48. Martel CL, Mackic JB, Matsubara E, Governale S, Miguel C, Miao W, McComb JG, et al. Isoform-specific effects of apolipoproteins E2, E3, and E4 on cerebral capillary sequestration and blood-brain barrier transport of circulating Alzheimer's amyloid b. J Neurochem 1997; 69: 1995-2004.
49. Verghese PB, Castellano JM, Garai K, Wang Y, Jiang H, Shah A, Bu G, et al. ApoE influences amyloid-b (Ab) clearance despite minimal apoE/Ab association in physiological conditions. Proc Natl Acad Sci USA 2013; 110: E1807-16.
50. Tai LM, Bilousova T, Jungbauer L, Roeske SK, Youmans KL, Yu C, Poon WW, et al. Levels of soluble apolipoprotein E/amyloid-b (Ab) complex are reduced and oligomeric Ab increased with APOE4 and Alzheimer disease in a transgenic mouse model and human samples. J Biol Chem 2013; 288: 5914-26.
51. Iwatsubo T, Saido TC, Mann DM, Lee VM, Trojanowski JQ. Full-length amyloid-beta (1-42(43)) and amino-terminally modified and truncated amyloid-beta 42(43) deposit in diffuse plaques. Am J Pathol 1996; 149: 1823-30.
52. Gunn AP, Masters CL, Cherny RA. Pyroglutamate-Abeta: role in the natural history of Alzheimer's disease. Int J Biochem Cell Biol 2010; 42: 1915-18.
53. Englund H, Degerman Gunnarsson M, Brundin RM, Hedlund M, Kilander L, Lannfelt L, Pettersson FE. Oligomerization partially explains the lowering of Abeta42 in Alzheimer's disease cerebrospinal fluid. Neurodegener Dis 2009; 6: 139-47.
54. Ji Z-S, Pitas RE, Mahley RW. Differential cellular accumulation/ retention of apolipoprotein E mediated by cell surface heparan sulfate proteoglycans. J Biol Chem 1998; 273: 13452-60.
55. Tamamizu-Kato S, Cohen JK, Drake CB, Kosaraju MG, Drury J, Narayanaswami V. Interaction with amyloid beta peptide compromises the lipid binding function of apolipoprotein E. Biochemistry (Mosc) 2008; 47: 5225-34.
56. Wahrle SE, Jiang H, Parsadanian M, Kim J, Li A, Knoten A, Jain S, et al. Overexpression of ABCA1 reduces amyloid deposition in the PDAPP mouse model of Alzheimer disease. J Clin Invest 2008; 118: 671-82.
57. Wahrle SE, Jiang H, Parsadanian M, Hartman RE, Bales KR, Paul SM, Holtzman DM. Deletion of Abca1 increases Ab deposition in the PDAPP transgenic mouse model of Alzheimer disease. J Biol Chem 2005; 280: 43236-42.
58. Koldamova R, Staufenbiel M, Lefterov I. Lack of ABCA1 considerably decreases brain ApoE level and increases amyloid deposition in APP23 mice. J Biol Chem 2005; 280: 43224-35.
59. Murphy AJ, Akhtari M, Tolani S, Pagler T, Bijl N, Kuo C-L, Wang M, et al. ApoE regulates hematopoietic stem cell proliferation, monocytosis, and monocyte accumulation in atherosclerotic lesions in mice. J Clin Invest 2011; 121: 4138-49.
60. Hatters DM, Peters-Libeu CA, Weisgraber KH. Apolipoprotein E structure: insights into function. Trends Biochem Sci 2006; 31: 445-54.
61. Gupta-Bansal R, Frederickson RC, Brunden KR. Proteoglycanmediated inhibition of A beta proteolysis. A potential cause of senile plaque accumulation. J Biol Chem 1995; 270: 18666-71.