Amino-terminal Domain Stability Mediates Apolipoprotein E Aggregation into Neurotoxic Fibrils

Journal of Molecular Biology

Volumn 361, Issue 5, 2006, Pages 932-944

  Hatters, Danny M ^a,b   Zhong, Ning ^a,b   Rutenber, Earl ^a   Weisgraber, Karl H ^a,b  

^a GLADSTONE INSTITUTE OF NEUROLOGICAL DISEASE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

aggregate toxicity; Alzheimer's disease; amyloid; apolipoproteins; protein misfolding

Indexed keywords

AMYLOID; APOLIPOPROTEIN E; CONGO RED; SODIUM CHLORIDE; TETRAMER; THIOFLAVINE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CONCENTRATION (PARAMETERS); IN VITRO STUDY; MOUSE; NERVE CELL CULTURE; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN;

EID: 33746932145     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.06.080     Document Type: Article

References (82)

1. Farrer L.A., Cupples L.A., Haines J.L., Hyman B., Kukull W.A., Mayeux R., et al. Effects of age, sex, and ethnicity on the association between apolipoprotein E genotype and Alzheimer disease. A meta-analysis. J. Am. Med. Assoc. 278 (1997) 1349-1356
2. Weisgraber K.H., Rall Jr. S.C., and Mahley R.W. Human E apoprotein heterogeneity. Cysteine-arginine interchanges in the amino acid sequence of the apo-E isoforms. J. Biol. Chem. 256 (1981) 9077-9083
3. Strittmatter W., Weisgraber K., Huang D., Dong L., Salvesen G., Pericak-Vance M., et al. Binding of human apolipoprotein E to synthetic amyloid β- peptide: Isoform-specific effects and implications for late-onset Alzheimer disease. Proc. Natl Acad. Sci. USA 90 (1993) 8098-8102
4. Nicoll J.A.R., Roberts G.W., and Graham D.I. Apolipoprotein E e4 allele is associated with deposition of amyloid β-protein following head injury. Nature Med. 1 (1995) 135-137
5. -/- mice: Isoform-specific effects on neurodegeneration. J. Neurosci. 19 (1999) 4867-4880
6. Holtzman D.M., Bales K.R., Tenkova T., Fagan A.M., Parsadanian M., Sartorius L.J., et al. Apolipoprotein E isoform-dependent amyloid deposition and neuritic degeneration in a mouse model of Alzheimer's disease. Proc. Natl Acad. Sci. USA 97 (2000) 2892-2897
7. Huang Y., Liu X.Q., Wyss-Coray T., Brecht W.J., Sanan D.A., and Mahley R.W. Apolipoprotein E fragments present in Alzheimer's disease brains induce neurofibrillary tangle-like intracellular inclusions in neurons. Proc. Natl Acad. Sci. USA 98 (2001) 8838-8843
8. Ji Z.-S., Miranda R.D., Newhouse Y.M., Weisgraber K.H., Huang Y., and Mahley R.W. Apolipoprotein E4 potentiates amyloid b peptide-induced lysosomal leakage and apoptosis in neuronal cells. J. Biol. Chem. 277 (2002) 21821-21828
9. Harris F.M., Brecht W.J., Xu Q., Tesseur I., Kekonius L., Wyss-Coray T., et al. Carboxyl-terminal-truncated apolipoprotein E4 causes Alzheimer's disease-like neurodegeneration and behavioral deficits in transgenic mice. Proc. Natl Acad. Sci. USA 100 (2003) 10966-10971
10. Marques M.A., and Crutcher K.A. Apolipoprotein E-related neurotoxicity as a therapeutic target for Alzheimer's disease. J. Mol. Neurosci. 20 (2003) 327-337
11. Dolev I., and Michaelson D.M. A nontransgenic mouse model shows inducible amyloid-β (Aβ) peptide deposition and elucidates the role of apolipoprotein E in the amyloid cascade. Proc. Natl Acad. Sci. USA 101 (2004) 13909-13914
12. Schmechel D., Saunders A., Strittmatter W., Crain B., Hulette C., Joo S., et al. Increased amyloid β-peptide deposition in cerebral cortex as a consequence of apolipoprotein E genotype in late-onset Alzheimer disease. Proc. Natl Acad. Sci. USA 90 (1993) 9649-9653
13. Wisniewski T., Lalowski M., Golabek A., Vogel T., and Frangione B. Is Alzheimer's disease an apolipoprotein E amyloidosis?. Lancet 345 (1995) 956-958
14. Cho H.S., Hyman B.T., Greenberg S.M., and Rebeck G.W. Quantitation of apoE domains in Alzheimer disease brain suggests a role for apoE in Aβ aggregation. J. Neuropathol. Exp. Neurol. 60 (2001) 342-349
15. Namba Y., Tomonaga M., Kawasaki H., Otomo E., and 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 (1991) 163-166
16. Wisniewski T., and Frangione B. Apolipoprotein E: A pathological chaperone protein in patients with cerebral and systemic amyloid. Neurosci. Letters 135 (1992) 235-238
17. Sheng J.G., Mrak R.E., and Griffin W.S. Apolipoprotein E distribution among different plaque types in Alzheimer's disease: Implications for its role in plaque progression. Neuropathol. Appl. Neurobiol. 22 (1996) 334-341
18. Naidu A., Catalano R., Bales K., Wu S., Paul S.M., and Cordell B. Conversion of brain apolipoprotein E to an insoluble form in a mouse model of Alzheimer disease. Neuroreport 12 (2001) 1265-1270
19. Matsutani H., Hoshii Y., Setoguchi M., Kawano H., Gondo T., Takahashi M., et al. Vascular amyloid of unknown origin and senile transthyretin amyloid in the lung and gastrointestinal tract of old age: histological and immunohistochemical studies. Path. Int. 51 (2001) 326-332
20. Hatters D.M., and Howlett G.J. The structural basis for amyloid formation by plasma apolipoproteins: a review. Eur. Biophys. J. 31 (2002) 2-8
21. Aggerbeck L.P., Wetterau J.R., Weisgraber K.H., Wu C.-S.C., and Lindgren F.T. Human apolipoprotein E3 in aqueous solution. II. Properties of the amino- and carboxyl-terminal domains. J. Biol. Chem. 263 (1988) 6249-6258
22. Yokoyama S., Kawai Y., Tajima S., and Yamamoto A. Behavior of human apolipoprotein E in aqueous solutions and at interfaces. J. Biol. Chem. 260 (1985) 16375-16382
23. Perugini M.A., Schuck P., and Howlett G.J. Self-association of human apolipoprotein E3 and E4 in the presence and absence of phospholipid. J. Biol. Chem. 275 (2000) 36758-36765
24. Van Holde K.E., and Weischet W.O. Boundary analysis of sedimentation-velocity experiments with monodisperse and paucidisperse solutes. Biopolymers 17 (1978) 1387-1403
25. Schuck P. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys. J. 78 (2000) 1606-1619
26. Chamberlain A.K., MacPhee C.E., Zurdo J., Morozova-Roche L.A., Hill H.A.O., Dobson C.M., et al. Ultrastructural organization of amyloid fibrils by atomic force microscopy. Biophys. J. 79 (2000) 3282-3293
27. Hatters D.M., MacPhee C.E., Lawrence L.J., Sawyer W.H., and Howlett G.J. Human apolipoprotein C-II forms twisted amyloid ribbons and closed loops. Biochemistry 39 (2000) 8276-8283
28. Goldsbury C.S., Cooper G.J.S., Goldie K.N., Müller S.A., Saafi E.L., Gruijters W.T.M., et al. Polymorphic fibrillar assembly of human amylin. J. Struct. Biol. 119 (1997) 17-27
29. LeVine III H. Quantification of b-sheet amyloid fibril structures with thioflavin T. Methods Enzymol. 309 (1999) 274-284
30. Klunk W.E., Jacob R.F., and Mason R.P. Quantifying amyloid β-peptide (Aβ) aggregation using the Congo red-Aβ (CR-Aβ) spectrophotometric assay. Anal. Biochem. 266 (1999) 66-76
31. Nilsson M.R. Techniques to study amyloid fibril formation in vitro. Methods 34 (2004) 151-160
32. Sunde M., Serpell L.C., Bartlam M., Fraser P.E., Pepys M.B., and Blake C.C.F. Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J. Mol. Biol. 273 (1997) 729-739
33. Provencher S.W., and Glöckner J. Estimation of globular protein secondary structure from circular dichroism. Biochemistry 20 (1981) 33-37
34. Johnson W.C. Analyzing protein circular dichroism spectra for accurate secondary structures. Proteins: Struct. Funct. Genet. 35 (1999) 307-312
35. Sreerama N., and Woody R.W. Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287 (2000) 252-260
36. Mendes Sousa M., Cardoso I., Fernandes R., Guimaraes A., and Saraiva M.J. Deposition of transthyretin in early stages of familial amyloidotic polyneuropathy: evidence for toxicity of nonfibrillar aggregates. Am. J. Pathol. 159 (2001) 1993-2000
37. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., et al. Naturally secreted oligomers of amyloid β-protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416 (2002) 535-539
38. Bucciantini M., Giannoni E., Chiti F., Baroni F., Formigli L., Zurdo J., et al. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416 (2002) 507-511
39. Kayed R., Head E., Thompson J.L., McIntire T.M., Milton S.C., Cotman C.W., et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300 (2003) 486-489
40. Boyles J.K., Pitas R.E., Wilson E., Mahley R.W., and Taylor J.M. Apolipoprotein E associated with astrocytic glia of the central nervous system and with non-myelinating glia of the peripheral nervous system. J. Clin. Invest. 76 (1985) 1501-1513
41. Weisgraber K.H., and Mahley R.W. Human apolipoprotein E: the Alzheimer's disease connection. FASEB J. 10 (1996) 1485-1494
42. Dong L.-M., and Weisgraber K.H. Human apolipoprotein E4 domain interaction. Arginine 61 and glutamic acid 255 interact to direct the preference for very low density lipoproteins. J. Biol. Chem. 271 (1996) 19053-19057
43. Morrow J.A., Hatters D.M., Lu B., Höchtl P., Oberg K.A., Rupp B., et al. Apolipoprotein E4 forms a molten globule: a potential basis for its association with disease. J. Biol. Chem. 277 (2002) 50380-50385
44. Hatters D.M., Budamagunta M.S., Voss J.C., and Weisgraber K.H. Modulation of apolipoprotein E structure by domain interaction: differences in lipid-bound and lipid-free forms. J. Biol. Chem. 280 (2005) 34288-34295
45. Morrow J.A., Segall M.L., Lund-Katz S., Phillips M.C., Knapp M., Rupp B., et al. Differences in stability among the human apolipoprotein E isoforms determined by the amino-terminal domain. Biochemistry 39 (2000) 11657-11666
46. Weers P.M.M., Narayanaswami V., Choy N., Luty R., Hicks L., Kay C.M., et al. Lipid binding ability of human apolipoprotein E N-terminal domain isoforms: correlation with protein stability?. Biophys. Chem. 100 (2003) 481-492
47. Dobson C.M. Protein folding and misfolding. Nature 426 (2003) 884-890
48. Wetterau J.R., Aggerbeck L.P., Rall Jr. S.C., and Weisgraber K.H. Human apolipoprotein E3 in aqueous solution. I. Evidence for two structural domains. J. Biol. Chem. 263 (1988) 6240-6248
49. Raffai R.L., Dong L.-M., Farese Jr. R.V., and Weisgraber K.H. Introduction of human apolipoprotein E4 "domain interaction" into mouse apolipoprotein E. Proc. Natl Acad. Sci. USA 98 (2001) 11587-11591
50. Hatters D.M., Peters-Libeu C.A., and Weisgraber K.H. Engineering conformational destabilization into mouse apolipoprotein E: a model for a unique property of human apolipoprotein E4. J. Biol. Chem. 280 (2005) 26477-26482
51. Yoshida K., Shibata T., Masai J., Sato K., Noguti T., Go M., et al. Protein anatomy: spontaneous formation of filamentous helical structures from the N-terminal module of barnase. Biochemistry 32 (1993) 2162-2166
52. Saiki M., Honda S., Kawasaki K., Zhou D., Kaito A., Konakahara T., et al. Higher-order molecular packing in amyloid-like fibrils constructed with linear arrangements of hydrophobic and hydrogen-bonding side-chains. J. Mol. Biol. 348 (2005) 983-998
53. Hatters D.M., MacRaild C.A., Daniels R., Gosal W.S., Thomson N.H., Jones J.A., et al. The circularization of amyloid fibrils formed by apolipoprotein C-II. Biophys. J. 85 (2003) 3979-3990
54. Choy N., Raussens V., and Narayanaswami V. Inter-molecular coiled-coil formation in human apolipoprotein E C-terminal domain. J. Mol. Biol. 334 (2003) 527-539
55. Ogihara N.L., Ghirlanda G., Bryson J.W., Gingery M., DeGrado W.F., and Eisenberg D. Design of three-dimensional domain-swapped dimers and fibrous oligomers. Proc. Natl Acad. Sci. USA 98 (2001) 1404-1409
56. Bariola P., Retelska D., Stasiak A., Kammerer R., Fleming A., Hijri M., et al. Remorins form a novel family of coiled coil-forming oligomeric and filamentous proteins associated with apical, vascular and embryonic tissues in plants. Plant Mol. Biol. 55 (2004) 579-594
57. Mucke N., Wedig T., Burer A., Marekov L.N., Steinert P.M., Langowski J., et al. Molecular and biophysical characterization of assembly-starter units of human vimentin. J. Mol. Biol. 340 (2004) 97-114
58. Borhani D.W., Rogers D.P., Engler J.A., and Brouillette C.G. Crystal structure of truncated human apolipoprotein A-I suggests a lipid-bound conformation. Proc. Natl Acad. Sci. USA 94 (1997) 12291-12296
59. Kumar M.S., Carson M., Hussain M.M., and Murthy H.M.K. Structures of apolipoprotein A-II and a lipid-surrogate complex provide insights into apolipoprotein-lipid interactions. Biochemistry 41 (2002) 11681-11691
60. Ajees A.A., Anantharamaiah G.M., Mishra V.K., Hussain M.M., and Murthy H.M.K. Crystal structure of human apolipoprotein A-I: Insights into its protective effect against cardiovascular diseases. Proc. Natl Acad. Sci. USA 103 (2006) 2126-2131
61. Sorci-Thomas M.G., and Thomas M.J. The effects of altered apolipoprotein A-I structure on plasma HDL concentration. Trends Cardiovasc. Med. 12 (2002) 121-128
62. Gursky O. Apolipoprotein structure and dynamics. Curr. Opin. Lipidol. 16 (2005) 287-294
63. Raussens V., Fisher C.A., Goormaghtigh E., Ryan R.O., and Ruysschaert J.-M. The low density lipoprotein receptor active conformation of apolipoprotein E. Helix organization in N-terminal domain-phospholipid disc particles. J. Biol. Chem. 273 (1998) 25825-25830
64. Fisher C.A., and Ryan R.O. Lipid binding-induced conformational changes in the N-terminal domain of human apolipoprotein E. J. Lipid Res. 40 (1999) 93-99
65. Lu B., Morrow J.A., and Weisgraber K.H. Conformational reorganization of the four-helix bundle of human apolipoprotein E in binding to phospholipid. J. Biol. Chem. 275 (2000) 20775-20781
66. Narayanaswami V., Szeto S.S.W., and Ryan R.O. Lipid association-induced N- and C-terminal domain reorganization in human apolipoprotein E3. J. Biol. Chem. 276 (2001) 37853-37860
67. Peters-Libeu C.A., Newhouse Y., Hatters D.M., and Weisgraber K.H. Model of biologically active apolipoprotein E bound to dipalmitoylphosphatidylcholine. J. Biol. Chem. 281 (2006) 1073-1079
68. Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., et al. Diffusible, nonfibrillar ligands derived from Aβ1-42 are potent central nervous system neurotoxins. Proc. Natl Acad. Sci. USA 95 (1998) 6448-6453
69. Sanan D.A., Weisgraber K.H., Russell S.J., Mahley R.W., Huang D., Saunders A., et al. Apolipoprotein E associates with β amyloid peptide of Alzheimer's disease to form novel monofibrils. Isoform apoE4 associates more efficiently than apoE3. J. Clin. Invest. 94 (1994) 860-869
70. Ma J., Yee A., Brewer H.B., Das S., and Potter H. Amyloid-associated proteins α1-antichymotrypsin and apolipoprotein E promote assembly of Alzheimer β-protein into filaments. Nature 372 (1994) 92-94
71. Wahrle S.E., Jiang H., Parsadanian M., Legleiter J., Han X., Fryer J.D., 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
72. Hirsch-Reinshagen V., Zhou S., Burgess B.L., Bernier L., McIsaac S.A., Chan J.Y., et al. Deficiency of ABCA1 impairs apolipoprotein E metabolism in brain. J. Biol. Chem. 279 (2004) 41197-41207
73. Hirsch-Reinshagen V., Maia L.F., Burgess B.L., Blain J.-F., Naus K.E., McIsaac S.A., et al. The absence of ABCA1 decreases soluble apoE levels but does not diminish amyloid deposition in two murine models of Alzheimer's disease. J. Biol. Chem. 280 (2005) 43243-43256
74. Koldamova R., Staufenbiel M., and Lefterov I. Lack of ABCA1 considerably decreases brain ApoE level and increases amyloid deposition in APP23 mice. J. Biol. Chem. 280 (2005) 43224-43235
75. Wahrle S.E., Jiang H., Parsadanian M., Hartman R.E., Bales K.R., Paul S.M., et al. Deletion of ABCA1 increases Aβ deposition in the PDAPP transgenic mouse model of Alzheimer's disease. J. Biol. Chem. 280 (2005) 43236-43242
76. Huang Y., von Eckardstein A., Wu S., Maeda N., and Assmann G. A plasma lipoprotein containing only apolipoprotein E and with γ mobility on electrophoresis releases cholesterol from cells. Proc. Natl Acad. Sci. USA 91 (1994) 1834-1838
77. Burgess J.W., Gould D.R., and Marcel Y.L. The HepG2 extracellular matrix contains separate heparinase- and lipid-releasable pools of apoE. J. Biol. Chem. 273 (1998) 5645-5654
78. Zhang W.-Y., Gaynor P.M., and Kruth H.S. Apolipoprotein E produced by human monocyte-derived macrophages mediates cholesterol efflux that occurs in the absence of added cholesterol acceptors. J. Biol. Chem. 271 (1996) 28641-28646
79. Lin C.-Y., Huang Z.H., and Mazzone T. Interaction with proteoglycans enhances the sterol efflux produced by endogenous expression of macrophage apoE. J. Lipid Res. 42 (2001) 1125-1133
80. Fagan A.M., Younkin L.H., Morris J.C., Fryer J.D., Cole T.G., Younkin S.G., et al. Differences in the Aβ40/Aβ42 ratio associated with cerebrospinal fluid lipoproteins as a function of apolipoprotein E genotype. Ann. Neurol. 48 (2000) 201-210
81. Morrow J.A., Arnold K.S., and Weisgraber K.H. Functional characterization of apolipoprotein E isoforms overexpressed in Escherichia coli. Protein Expr. Purif. 16 (1999) 224-230
82. Abramoff M.D., Magelhaes P.J., and Ram S.J. Image processing with ImageJ. Biophoton. Internat. 11 (2004) 36-42