Skip to main content
PMC home page
Protein & Cell logoLink to Protein & Cell
. 2011 Mar 12;2(2):116–127. doi: 10.1007/s13238-011-1013-6

Apolipoproteins and amyloid fibril formation in atherosclerosis

Chai Lean Teoh 1,2, Michael D W Griffin 1,2, Geoffrey J Howlett 1,2,✉
PMCID: PMC4723368  PMID: 21400045

Abstract

Amyloid fibrils arise from the aggregation of misfolded proteins into highly-ordered structures. The accumulation of these fibrils along with some non-fibrillar constituents within amyloid plaques is associated with the pathogenesis of several human degenerative diseases. A number of plasma apolipoproteins, including apolipoprotein (apo) A-I, apoA-II, apoC-II and apoE are implicated in amyloid formation or influence amyloid formation by other proteins. We review present knowledge of amyloid formation by apolipoproteins in disease, with particular focus on atherosclerosis. Further insights into the molecular mechanisms underlying their amyloidogenic propensity are obtained from in vitro studies which describe factors affecting apolipoprotein amyloid fibril formation and interactions. Additionally, we outline the evidence that amyloid fibril formation by apolipoproteins might play a role in the development and progression of atherosclerosis, and highlight possible molecular mechanisms that could contribute to the pathogenesis of this disease.

Keywords: misfolding, apolipoproteins, amyloid fibril, atherosclerosis

References

  1. Acharya P., Segall M.L., Zaiou M., Morrow J., Weisgraber K.H., Phillips M.C., Lund-Katz S., Snow J. Comparison of the stabilities and unfolding pathways of human apolipoprotein E isoforms by differential scanning calorimetry and circular dichroism. Biochim Biophys Acta. 2002;1584:9–19. doi: 10.1016/s1388-1981(02)00263-9. [DOI] [PubMed] [Google Scholar]
  2. Alexandrescu A.T. Amyloid accomplices and enforcers. Protein Sci. 2005;14:1–12. doi: 10.1110/ps.04887005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anantharamaiah G.M., Hughes T.A., Iqbal M., Gawish A., Neame P.J., Medley M.F., Segrest J.P. Effect of oxidation on the properties of apolipoproteins A-I and A-II. J Lipid Res. 1988;29:309–318. [PubMed] [Google Scholar]
  4. Andersen C.B., Yagi H., Manno M., Martorana V., Ban T., Christiansen G., Otzen D.E., Goto Y., Rischel C. Branching in amyloid fibril growth. Biophys J. 2009;96:1529–1536. doi: 10.1016/j.bpj.2008.11.024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Andreola A., Bellotti V., Giorgetti S., Mangione P., Obici L., Stoppini M., Torres J., Monzani E., Merlini G., Sunde M. Conformational switching and fibrillogenesis in the amyloidogenic fragment of apolipoprotein a-I. J Biol Chem. 2003;278:2444–2451. doi: 10.1074/jbc.M204801200. [DOI] [PubMed] [Google Scholar]
  6. Anfinsen C.B. Principles that govern the folding of protein chains. Science. 1973;181:223–230. doi: 10.1126/science.181.4096.223. [DOI] [PubMed] [Google Scholar]
  7. Ban T., Hamada D., Hasegawa K., Naiki H., Goto Y. Direct observation of amyloid fibril growth monitored by thioflavin T fluorescence. J Biol Chem. 2003;278:16462–16465. doi: 10.1074/jbc.C300049200. [DOI] [PubMed] [Google Scholar]
  8. Ban T., Hoshino M., Takahashi S., Hamada D., Hasegawa K., Naiki H., Goto Y. Direct observation of Abeta amyloid fibril growth and inhibition. J Mol Biol. 2004;344:757–767. doi: 10.1016/j.jmb.2004.09.078. [DOI] [PubMed] [Google Scholar]
  9. Ban T., Morigaki K., Yagi H., Kawasaki T., Kobayashi A., Yuba S., Naiki H., Goto Y. Real-time and single fibril observation of the formation of amyloid beta spherulitic structures. J Biol Chem. 2006;281:33677–33683. doi: 10.1074/jbc.M606072200. [DOI] [PubMed] [Google Scholar]
  10. Ban T., Yamaguchi K., Goto Y. Direct observation of amyloid fibril growth, propagation, and adaptation. Acc Chem Res. 2006;39:663–670. doi: 10.1021/ar050074l. [DOI] [PubMed] [Google Scholar]
  11. Benson M.D., Liepnieks J.J., Yazaki M., Yamashita T., Hamidi Asl K., Guenther B., Kluve-Beckerman B. A new human hereditary amyloidosis: the result of a stop-codon mutation in the apolipoprotein AII gene. Genomics. 2001;72:272–277. doi: 10.1006/geno.2000.6499. [DOI] [PubMed] [Google Scholar]
  12. Binger K.J., Griffin M.D., Heinemann S.H., Howlett G.J. Methionine-oxidized amyloid fibrils are poor substrates for human methionine sulfoxide reductases A and B2. Biochemistry. 2010;49:2981–2983. doi: 10.1021/bi902203m. [DOI] [PubMed] [Google Scholar]
  13. Binger K.J., Griffin M.D., Howlett G.J. Methionine oxidation inhibits assembly and promotes disassembly of apolipoprotein C-II amyloid fibrils. Biochemistry. 2008;47:10208–10217. doi: 10.1021/bi8009339. [DOI] [PubMed] [Google Scholar]
  14. Binger K.J., Pham C.L., Wilson L.M., Bailey M.F., Lawrence L.J., Schuck P., Howlett G.J. Apolipoprotein C-II amyloid fibrils assemble via a reversible pathway that includes fibril breaking and rejoining. J Mol Biol. 2008;376:1116–1129. doi: 10.1016/j.jmb.2007.12.055. [DOI] [PubMed] [Google Scholar]
  15. Booth D.R., Tan S.Y., Booth S.E., Hsuan J.J., Totty N.F., Nguyen O., Hutton T., Vigushin D.M., Tennent G.A., Hutchinson W.L., et al. A new apolipoprotein Al variant, Trp50Arg, causes hereditary amyloidosis. QJM. 1995;88:695–702. [PubMed] [Google Scholar]
  16. Booth D.R., Tan S.Y., Booth S.E., Tennent G.A., Hutchinson W.L., Hsuan J.J., Totty N.F., Truong O., Soutar A.K., Hawkins P.N., et al. Hereditary hepatic and systemic amyloidosis caused by a new deletion/insertion mutation in the apolipoprotein AI gene. J Clin Invest. 1996;97:2714–2721. doi: 10.1172/JCI118725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Bosco D.A., Fowler D.M., Zhang Q., Nieva J., Powers E.T., Wentworth P., Jr, Lerner R.A., Kelly J.W. Elevated levels of oxidized cholesterol metabolites in Lewy body disease brains accelerate alpha-synuclein fibrilization. Nat Chem Biol. 2006;2:249–253. doi: 10.1038/nchembio782. [DOI] [PubMed] [Google Scholar]
  18. Calero M., Rostagno A., Matsubara E., Zlokovic B., Frangione B., Ghiso J. Apolipoprotein J (clusterin) and Alzheimer’s disease. Microsc Res Tech. 2000;50:305–315. doi: 10.1002/1097-0029(20000815)50:4<305::AID-JEMT10>3.0.CO;2-L. [DOI] [PubMed] [Google Scholar]
  19. Castaño E.M., Prelli F., Pras M., Frangione B. Apolipoprotein E carboxyl-terminal fragments are complexed to amyloids A and L. Implications for amyloidogenesis and Alzheimer’s disease. J Biol Chem. 1995;270:17610–17615. doi: 10.1074/jbc.270.29.17610. [DOI] [PubMed] [Google Scholar]
  20. Cedazo-Mínguez A., Cowburn R.F. Apolipoprotein E: a major piece in the Alzheimer’s disease puzzle. J Cell Mol Med. 2001;5:254–266. doi: 10.1111/j.1582-4934.2001.tb00159.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Chauhan V., Wang X., Ramsamy T., Milne R.W., Sparks D.L. Evidence for lipid-dependent structural changes in specific domains of apolipoprotein B100. Biochemistry. 1998;37:3735–3742. doi: 10.1021/bi9718853. [DOI] [PubMed] [Google Scholar]
  22. Chisolm G.M., Steinberg D. The oxidative modification hypothesis of atherogenesis: an overview. Free Radic Biol Med. 2000;28:1815–1826. doi: 10.1016/s0891-5849(00)00344-0. [DOI] [PubMed] [Google Scholar]
  23. Chiti F., Webster P., Taddei N., Clark A., Stefani M., Ramponi G., Dobson C.M. Designing conditions for in vitro formation of amyloid protofilaments and fibrils. Proc Natl Acad Sci U S A. 1999;96:3590–3594. doi: 10.1073/pnas.96.7.3590. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Cho H.S., Hyman B.T., Greenberg S.M., Rebeck G.W. Quantitation of apoE domains in Alzheimer disease brain suggests a role for apoE in Abeta aggregation. J Neuropathol Exp Neurol. 2001;60:342–349. doi: 10.1093/jnen/60.4.342. [DOI] [PubMed] [Google Scholar]
  25. Clark J.I., Muchowski P.J. Small heat-shock proteins and their potential role in human disease. Curr Opin Struct Biol. 2000;10:52–59. doi: 10.1016/s0959-440x(99)00048-2. [DOI] [PubMed] [Google Scholar]
  26. Corder E.H., Saunders A.M., Strittmatter W.J., Schmechel D.E., Gaskell P.C., Small G.W., Roses A.D., Haines J.L., Pericak-Vance M.A. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer’s disease in late onset families. Science. 1993;261:921–923. doi: 10.1126/science.8346443. [DOI] [PubMed] [Google Scholar]
  27. Damaschun G., Damaschun H., Fabian H., Gast K., Kröber R., Wieske M., Zirwer D. Conversion of yeast phosphoglycerate kinase into amyloid-like structure. Proteins. 2000;39:204–211. doi: 10.1002/(sici)1097-0134(20000515)39:3<204::aid-prot20>3.0.co;2-8. [DOI] [PubMed] [Google Scholar]
  28. de Sousa M.M., Vital C., Ostler D., Fernandes R., Pouget-Abadie J., Carles D., Saraiva M.J. Apolipoprotein AI and transthyretin as components of amyloid fibrils in a kindred with apoAI Leu178His amyloidosis. Am J Pathol. 2000;156:1911–1917. doi: 10.1016/S0002-9440(10)65064-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Derham B.K., Harding J.J. Alpha-crystallin as a molecular chaperone. Prog Retin Eye Res. 1999;18:463–509. doi: 10.1016/s1350-9462(98)00030-5. [DOI] [PubMed] [Google Scholar]
  30. Dobson C.M. Getting out of shape. Nature. 2002;418:729–730. doi: 10.1038/418729a. [DOI] [PubMed] [Google Scholar]
  31. Dobson C.M. Protein folding and misfolding. Nature. 2003;426:884–890. doi: 10.1038/nature02261. [DOI] [PubMed] [Google Scholar]
  32. Eriksson M., Schönland S., Yumlu S., Hegenbart U., von Hutten H., Gioeva Z., Lohse P., Büttner J., Schmidt H., Röcken C. Hereditary apolipoprotein AI-associated amyloidosis in surgical pathology specimens: identification of three novel mutations in the APOA1 gene. J Mol Diagn. 2009;11:257–262. doi: 10.2353/jmoldx.2009.080161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Evans K.C., Berger E.P., Cho C.G., Weisgraber K.H., Lansbury P.T., Jr. Apolipoprotein E is a kinetic but not a thermodynamic inhibitor of amyloid formation: implications for the pathogenesis and treatment of Alzheimer disease. Proc Natl Acad Sci U S A. 1995;92:763–767. doi: 10.1073/pnas.92.3.763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Fändrich M., Fletcher M.A., Dobson C.M. Amyloid fibrils from muscle myoglobin. Nature. 2001;410:165–166. doi: 10.1038/35065514. [DOI] [PubMed] [Google Scholar]
  35. Frangione B., Castaño E.M., Wisniewski T., Ghiso J., Prelli F., Vidal R. Apolipoprotein E and amyloidogenesis. Ciba Found Symp. 1996;199:132–141. doi: 10.1002/9780470514924.ch9. [DOI] [PubMed] [Google Scholar]
  36. Garner B., Waldeck A.R., Witting P.K., Rye K.A., Stocker R. Oxidation of high density lipoproteins. II. Evidence for direct reduction of lipid hydroperoxides by methionine residues of apolipoproteins AI and AII. J Biol Chem. 1998;273:6088–6095. doi: 10.1074/jbc.273.11.6088. [DOI] [PubMed] [Google Scholar]
  37. Genschel J., Haas R., Pröpsting M.J., Schmidt H.H. Apolipoprotein A-I induced amyloidosis. FEBS Lett. 1998;430:145–149. doi: 10.1016/s0014-5793(98)00668-1. [DOI] [PubMed] [Google Scholar]
  38. Griffin M.D., Mok M.L., Wilson L.M., Pham C.L., Waddington L.J., Perugini M.A., Howlett G.J. Phospholipid interaction induces molecular-level polymorphism in apolipoprotein C-II amyloid fibrils via alternative assembly pathways. J Mol Biol. 2008;375:240–256. doi: 10.1016/j.jmb.2007.10.038. [DOI] [PubMed] [Google Scholar]
  39. Gunzburg M.J., Perugini M.A., Howlett G.J. Structural basis for the recognition and cross-linking of amyloid fibrils by human apolipoprotein E. J Biol Chem. 2007;282:35831–35841. doi: 10.1074/jbc.M706425200. [DOI] [PubMed] [Google Scholar]
  40. Häggqvist B., Näslund J., Sletten K., Westermark G.T., Mucchiano G., Tjernberg L.O., Nordstedt C., Engström U., Westermark P. Medin: an integral fragment of aortic smooth muscle cellproduced lactadherin forms the most common human amyloid. Proc Natl Acad Sci U S A. 1999;96:8669–8674. doi: 10.1073/pnas.96.15.8669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Hatters D.M., Howlett G.J. The structural basis for amyloid formation by plasma apolipoproteins: a review. Eur Biophys J. 2002;31:2–8. doi: 10.1007/s002490100172. [DOI] [PubMed] [Google Scholar]
  42. Hatters D.M., Lawrence L.J., Howlett G.J. Submicellar phospholipid accelerates amyloid formation by apolipoprotein C-II. FEBS Lett. 2001;494:220–224. doi: 10.1016/s0014-5793(01)02355-9. [DOI] [PubMed] [Google Scholar]
  43. Hatters D.M., Lindner R.A., Carver J.A., Howlett G.J. The molecular chaperone, alpha-crystallin, inhibits amyloid formation by apolipoprotein C-II. J Biol Chem. 2001;276:33755–33761. doi: 10.1074/jbc.M105285200. [DOI] [PubMed] [Google Scholar]
  44. Hatters D.M., MacPhee C.E., Lawrence L.J., Sawyer W.H., Howlett G.J. Human apolipoprotein C-II forms twisted amyloid ribbons and closed loops. Biochemistry. 2000;39:8276–8283. doi: 10.1021/bi000002w. [DOI] [PubMed] [Google Scholar]
  45. Hatters D.M., MacRaild C.A., Daniels R., Gosal W.S., Thomson N.H., Jones J.A., Davis J.J., MacPhee C.E., Dobson C.M., Howlett G.J. The circularization of amyloid fibrils formed by apolipoprotein C-II. Biophys J. 2003;85:3979–3990. doi: 10.1016/S0006-3495(03)74812-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Hatters D.M., Wilson M.R., Easterbrook-Smith S.B., Howlett G. J. Suppression of apolipoprotein C-II amyloid formation by the extracellular chaperone, clusterin. Eur J Biochem. 2002;269:2789–2794. doi: 10.1046/j.1432-1033.2002.02957.x. [DOI] [PubMed] [Google Scholar]
  47. Hatters D.M., Zhong N., Rutenber E., Weisgraber K.H. Amino-terminal domain stability mediates apolipoprotein E aggregation into neurotoxic fibrils. J Mol Biol. 2006;361:932–944. doi: 10.1016/j.jmb.2006.06.080. [DOI] [PubMed] [Google Scholar]
  48. Havel R.J., Fielding C.J., Olivecrona T., Shore V.G., Fielding P.E., Egelrud T. Cofactor activity of protein components of human very low density lipoproteins in the hydrolysis of triglycerides by lipoproteins lipase from different sources. Biochemistry. 1973;12:1828–1833. doi: 10.1021/bi00733a026. [DOI] [PubMed] [Google Scholar]
  49. Higgins G.A., Large C.H., Rupniak H.T., Barnes J.C. Apolipoprotein E and Alzheimer’s disease: a review of recent studies. Pharmacol Biochem Behav. 1997;56:675–685. doi: 10.1016/s0091-3057(96)00420-0. [DOI] [PubMed] [Google Scholar]
  50. Higuchi K., Kitagawa K., Naiki H., Hanada K., Hosokawa M., Takeda T. Polymorphism of apolipoprotein A-II (apoA-II) among inbred strains of mice. Relationship between the molecular type of apoA-II and mouse senile amyloidosis. Biochem J. 1991;279:427–433. doi: 10.1042/bj2790427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Higuchi K., Naiki H., Kitagawa K., Hosokawa M., Takeda T. Mouse senile amyloidosis. ASSAM amyloidosis in mice presents universally as a systemic age-associated amyloidosis. Virchows Arch B Cell Pathol Incl Mol Pathol. 1991;60:231–238. [PubMed] [Google Scholar]
  52. Howlett G.J., Moore K.J. Untangling the role of amyloid in atherosclerosis. Curr Opin Lipidol. 2006;17:541–547. doi: 10.1097/01.mol.0000245260.63505.4f. [DOI] [PubMed] [Google Scholar]
  53. Humphreys D.T., Carver J.A., Easterbrook-Smith S.B., Wilson M.R. Clusterin has chaperone-like activity similar to that of small heat shock proteins. J Biol Chem. 1999;274:6875–6881. doi: 10.1074/jbc.274.11.6875. [DOI] [PubMed] [Google Scholar]
  54. Hung A., Griffin M.D., Howlett G.J., Yarovsky I. Effects of oxidation, pH and lipids on amyloidogenic peptide structure: implications for fibril formation? Eur Biophys J. 2008;38:99–110. doi: 10.1007/s00249-008-0363-3. [DOI] [PubMed] [Google Scholar]
  55. Hung A., Griffin M.D., Howlett G.J., Yarovsky I. Lipids enhance apolipoprotein C-II-derived amyloidogenic peptide oligomerization but inhibit fibril formation. J Phys Chem B. 2009;113:9447–9453. doi: 10.1021/jp901051n. [DOI] [PubMed] [Google Scholar]
  56. 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. 1995;239:209–211. doi: 10.1016/0009-8981(95)06115-t. [DOI] [PubMed] [Google Scholar]
  57. Kinnunen P.K., Jackson R.L., Smith L.C., Gotto A.M., Jr, Sparrow J.T. Activation of lipoprotein lipase by native and synthetic fragments of human plasma apolipoprotein C-II. Proc Natl Acad Sci U S A. 1977;74:4848–4851. doi: 10.1073/pnas.74.11.4848. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Kisilevsky R. The relation of proteoglycans, serum amyloid P and apo E to amyloidosis current status, 2000. Amyloid. 2000;7:23–25. doi: 10.3109/13506120009146820. [DOI] [PubMed] [Google Scholar]
  59. Knight J.D., Miranker A.D. Phospholipid catalysis of diabetic amyloid assembly. J Mol Biol. 2004;341:1175–1187. doi: 10.1016/j.jmb.2004.06.086. [DOI] [PubMed] [Google Scholar]
  60. Koistinaho M., Lin S., Wu X., Esterman M., Koger D., Hanson J., Higgs R., Liu F., Malkani S., Bales K.R., et al. Apolipoprotein E promotes astrocyte colocalization and degradation of deposited amyloid-beta peptides. Nat Med. 2004;10:719–726. doi: 10.1038/nm1058. [DOI] [PubMed] [Google Scholar]
  61. Kuriyama M., Takahashi K., Yamano T., Hokezu Y., Togo S., Osame M., Igakura T. Low levels of serum apolipoprotein A I and A II in senile dementia. Jpn J Psychiatry Neurol. 1994;48:589–593. doi: 10.1111/j.1440-1819.1994.tb03019.x. [DOI] [PubMed] [Google Scholar]
  62. Lange U., Boss B., Teichmann J., Klör H.U., Neeck G. Serum amyloid A—an indicator of inflammation in ankylosing spondylitis. Rheumatol Int. 2000;19:119–122. doi: 10.1007/s002960050114. [DOI] [PubMed] [Google Scholar]
  63. LaRosa J.C., Levy R.I., Herbert P., Lux S.E., Fredrickson D.S. A specific apoprotein activator for lipoprotein lipase. Biochem Biophys Res Commun. 1970;41:57–62. doi: 10.1016/0006-291x(70)90468-7. [DOI] [PubMed] [Google Scholar]
  64. Legge F.S., Binger K.J., Griffin M.D., Howlett G.J., Scanlon D., Treutlein H., Yarovsky I. Effect of oxidation and mutation on the conformational dynamics and fibril assembly of amyloidogenic peptides derived from apolipoprotein C-II. J Phys Chem B. 2009;113:14006–14014. doi: 10.1021/jp903842u. [DOI] [PubMed] [Google Scholar]
  65. Legge F.S., Treutlein H., Howlett G.J., Yarovsky I. Molecular dynamics simulations of a fibrillogenic peptide derived from apolipoprotein C-II. Biophys Chem. 2007;130:102–113. doi: 10.1016/j.bpc.2007.08.002. [DOI] [PubMed] [Google Scholar]
  66. Li Q., Min J., Ahn Y.H., Namm J., Kim E.M., Lui R., Kim H.Y., Ji Y., Wu H., Wisniewski T., et al. Styryl-based compounds as potential in vivo imaging agents for beta-amyloid plaques. Chembiochem. 2007;8:1679–1687. doi: 10.1002/cbic.200700154. [DOI] [PubMed] [Google Scholar]
  67. MacRaild C.A., Hatters D.M., Howlett G.J., Gooley P.R. NMR structure of human apolipoprotein C-II in the presence of sodium dodecyl sulfate. Biochemistry. 2001;40:5414–5421. doi: 10.1021/bi002821m. [DOI] [PubMed] [Google Scholar]
  68. MacRaild C.A., Hatters D.M., Lawrence L.J., Howlett G.J. Sedimentation velocity analysis of flexible macromolecules: self-association and tangling of amyloid fibrils. Biophys J. 2003;84:2562–2569. doi: 10.1016/S0006-3495(03)75061-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. MacRaild C.A., Howlett G.J., Gooley P.R. The structure and interactions of human apolipoprotein C-II in dodecyl phosphocholine. Biochemistry. 2004;43:8084–8093. doi: 10.1021/bi049817l. [DOI] [PubMed] [Google Scholar]
  70. MacRaild C.A., Stewart C.R., Mok Y.F., Gunzburg M.J., Perugini M.A., Lawrence L.J., Tirtaatmadja V., Cooper-White J.J., Howlett G.J. Non-fibrillar components of amyloid deposits mediate the self-association and tangling of amyloid fibrils. J Biol Chem. 2004;279:21038–21045. doi: 10.1074/jbc.M314008200. [DOI] [PubMed] [Google Scholar]
  71. Mak P.A., Laffitte B.A., Desrumaux C., Joseph S.B., Curtiss L.K., Mangelsdorf D.J., Tontonoz P., Edwards P.A. Regulated expression of the apolipoprotein E/C-I/C-IV/C-II gene cluster in murine and human macrophages. A critical role for nuclear liver X receptors alpha and beta. J Biol Chem. 2002;277:31900–31908. doi: 10.1074/jbc.M202993200. [DOI] [PubMed] [Google Scholar]
  72. May P.C., Finch C.E. Sulfated glycoprotein 2: new relationships of this multifunctional protein to neurodegeneration. Trends Neurosci. 1992;15:391–396. doi: 10.1016/0166-2236(92)90190-j. [DOI] [PubMed] [Google Scholar]
  73. Medeiros L.A., Khan T., El Khoury J.B., Pham C.L., Hatters D.M., Howlett G.J., Lopez R., O’Brien K.D., Moore K.J. Fibrillar amyloid protein present in atheroma activates CD36 signal transduction. J Biol Chem. 2004;279:10643–10648. doi: 10.1074/jbc.M311735200. [DOI] [PubMed] [Google Scholar]
  74. Merched A., Xia Y., Visvikis S., Serot J.M., Siest G. Decreased high-density lipoprotein cholesterol and serum apolipoprotein AI concentrations are highly correlated with the severity of Alzheimer’s disease. Neurobiol Aging. 2000;21:27–30. doi: 10.1016/s0197-4580(99)00103-7. [DOI] [PubMed] [Google Scholar]
  75. Mok, Y.F., Ryan, T.M., Yang, S., Hatters, D.M., Howlett, G.J., and Griffin, M.D. (2010). Sedimentation velocity analysis of amyloid oligomers and fibrils using fluorescence detection. Methods. doi: 10.1016/j.ymeth.2010.10.004. [DOI] [PubMed]
  76. Moore K.J., El Khoury J., Medeiros L.A., Terada K., Geula C., Luster A.D., Freeman M.W. A CD36-initiated signaling cascade mediates inflammatory effects of beta-amyloid. J Biol Chem. 2002;277:47373–47379. doi: 10.1074/jbc.M208788200. [DOI] [PubMed] [Google Scholar]
  77. Mucchiano G., Cornwell G.G., 3rd, Westermark P. Senile aortic amyloid. Evidence for two distinct forms of localized deposits. Am J Pathol. 1992;140:871–877. [PMC free article] [PubMed] [Google Scholar]
  78. Mucchiano G.I., Häggqvist B., Sletten K., Westermark P. Apolipoprotein A-1-derived amyloid in atherosclerotic plaques of the human aorta. J Pathol. 2001;193:270–275. doi: 10.1002/1096-9896(2000)9999:9999<::AID-PATH753>3.0.CO;2-S. [DOI] [PubMed] [Google Scholar]
  79. Mucchiano G.I., Jonasson L., Häggqvist B., Einarsson E., Westermark P. Apolipoprotein A-I-derived amyloid in atherosclerosis. Its association with plasma levels of apolipoprotein A-I and cholesterol. Am J Clin Pathol. 2001;115:298–303. doi: 10.1309/PJE6-X9E5-LX6K-NELY. [DOI] [PubMed] [Google Scholar]
  80. Myers S.L., Jones S., Jahn T.R., Morten I.J., Tennent G.A., Hewitt E.W., Radford S.E. A systematic study of the effect of physiological factors on beta2-microglobulin amyloid formation at neutral pH. Biochemistry. 2006;45:2311–2321. doi: 10.1021/bi052434i. [DOI] [PubMed] [Google Scholar]
  81. Naiki H., Gejyo F., Nakakuki K. Concentrationdependent inhibitory effects of apolipoprotein E on Alzheimer’s beta-amyloid fibril formation in vitro. Biochemistry. 1997;36:6243–6250. doi: 10.1021/bi9624705. [DOI] [PubMed] [Google Scholar]
  82. Naiki H., Hasegawa K., Yamaguchi I., Nakamura H., Gejyo F., Nakakuki K. Apolipoprotein E and antioxidants have different mechanisms of inhibiting Alzheimer’s beta-amyloid fibril formation in vitro. Biochemistry. 1998;37:17882–17889. doi: 10.1021/bi980550y. [DOI] [PubMed] [Google Scholar]
  83. Näslund J., Thyberg J., Tjernberg L.O., Wernstedt C., Karlström A. R., Bogdanovic N., Gandy S.E., Lannfelt L., Terenius L., Nordstedt C. Characterization of stable complexes involving apolipoprotein E and the amyloid beta peptide in Alzheimer’s disease brain. Neuron. 1995;15:219–228. doi: 10.1016/0896-6273(95)90079-9. [DOI] [PubMed] [Google Scholar]
  84. O’Brien K.D., Olin K.L., Alpers C.E., Chiu W., Ferguson M., Hudkins K., Wight T.N., Chait A. Comparison of apolipoprotein and proteoglycan deposits in human coronary atherosclerotic plaques: colocalization of biglycan with apolipoproteins. Circulation. 1998;98:519–527. doi: 10.1161/01.cir.98.6.519. [DOI] [PubMed] [Google Scholar]
  85. Obici L., Franceschini G., Calabresi L., Giorgetti S., Stoppini M., Merlini G., Bellotti V. Structure, function and amyloidogenic propensity of apolipoprotein A-I. Amyloid. 2006;13:191–205. doi: 10.1080/13506120600960288. [DOI] [PubMed] [Google Scholar]
  86. Ozawa D., Yagi H., Ban T., Kameda A., Kawakami T., Naiki H., Goto Y. Destruction of amyloid fibrils of a beta2-microglobulin fragment by laser beam irradiation. J Biol Chem. 2009;284:1009–1017. doi: 10.1074/jbc.M805118200. [DOI] [PubMed] [Google Scholar]
  87. Pepys M.B. Amyloidosis. Annu Rev Med. 2006;57:223–241. doi: 10.1146/annurev.med.57.121304.131243. [DOI] [PubMed] [Google Scholar]
  88. Pepys M.B., Booth D.R., Huchinson W.L., Gallimore J.R., Collins P.M., Hohenester E. Amyloid P component. A critical review. AMYLOID. 1997;4:274–295. [Google Scholar]
  89. Pepys M.B., Herbert J., Hutchinson W.L., Tennent G.A., Lachmann H.J., Gallimore J.R., Lovat L.B., Bartfai T., Alanine A., Hertel C., et al. Targeted pharmacological depletion of serum amyloid P component for treatment of human amyloidosis. Nature. 2002;417:254–259. doi: 10.1038/417254a. [DOI] [PubMed] [Google Scholar]
  90. Permanne B., Perez C., Soto C., Frangione B., Wisniewski T. Detection of apolipoprotein E/dimeric soluble amyloid beta complexes in Alzheimer’s disease brain supernatants. Biochem Biophys Res Commun. 1997;240:715–720. doi: 10.1006/bbrc.1997.7727. [DOI] [PubMed] [Google Scholar]
  91. Pham C.L., Hatters D.M., Lawrence L.J., Howlett G.J. Cross-linking and amyloid formation by N- and C-terminal cysteine derivatives of human apolipoprotein C-II. Biochemistry. 2002;41:14313–14322. doi: 10.1021/bi026070v. [DOI] [PubMed] [Google Scholar]
  92. Puchtler H., Sweat F. Amidoblack as a stain for hemoglobin. Arch Pathol. 1962;73:245–249. [PubMed] [Google Scholar]
  93. Röcken C., Tautenhahn J., Bühling F., Sachwitz D., Vöckler S., Goette A., Bürger T. Prevalence and pathology of amyloid in atherosclerotic arteries. Arterioscler Thromb Vasc Biol. 2006;26:676–677. doi: 10.1161/01.ATV.0000201930.10103.be. [DOI] [PubMed] [Google Scholar]
  94. Ross R. Atherosclerosis—an inflammatory disease. N Engl J Med. 1999;340:115–126. doi: 10.1056/NEJM199901143400207. [DOI] [PubMed] [Google Scholar]
  95. Ryan T.M., Griffin M.D., Teoh C.L., Ooi J., Howlett G.J. High-Affinity Amphipathic Modulators of Amyloid Fibril Nucleation and Elongation. J Mol Biol. 2011;406:416–429. doi: 10.1016/j.jmb.2010.12.023. [DOI] [PubMed] [Google Scholar]
  96. Ryan T.M., Howlett G.J., Bailey M.F. Fluorescence detection of a lipid-induced tetrameric intermediate in amyloid fibril formation by apolipoprotein C-II. J Biol Chem. 2008;283:35118–35128. doi: 10.1074/jbc.M804004200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. Ryan T.M., Teoh C.L., Griffin M.D., Bailey M.F., Schuck P., Howlett G.J. Phospholipids enhance nucleation but not elongation of apolipoprotein C-II amyloid fibrils. J Mol Biol. 2010;399:731–740. doi: 10.1016/j.jmb.2010.04.042. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Saczynski J.S., White L., Peila R.L., Rodriguez B.L., Launer L. J. The relation between apolipoprotein A-I and dementia: the Honolulu-Asia aging study. Am J Epidemiol. 2007;165:985–992. doi: 10.1093/aje/kwm027. [DOI] [PubMed] [Google Scholar]
  99. Saunders A.M., Strittmatter W.J., Schmechel D., George-Hyslop P. H., Pericak-Vance M.A., Joo S.H., Rosi B.L., Gusella J.F., Crapper-MacLachlan D.R., Alberts M.J., et al. Association of apolipoprotein E allele epsilon 4 with late-onset familial and sporadic Alzheimer’s disease. Neurology. 1993;43:1467–1472. doi: 10.1212/wnl.43.8.1467. [DOI] [PubMed] [Google Scholar]
  100. Segrest J.P., Garber D.W., Brouillette C.G., Harvey S.C., Anantharamaiah G.M. The amphipathic alpha helix: a multifunctional structural motif in plasma apolipoproteins. Adv Protein Chem. 1994;45:303–369. doi: 10.1016/s0065-3233(08)60643-9. [DOI] [PubMed] [Google Scholar]
  101. Sipe J.D., Cohen A.S. Review: history of the amyloid fibril. J Struct Biol. 2000;130:88–98. doi: 10.1006/jsbi.2000.4221. [DOI] [PubMed] [Google Scholar]
  102. Soto C., Castaño E.M., Prelli F., Kumar R.A., Baumann M. Apolipoprotein E increases the fibrillogenic potential of synthetic peptides derived from Alzheimer’s, gelsolin and AA amyloids. FEBS Lett. 1995;371:110–114. doi: 10.1016/0014-5793(95)00863-5. [DOI] [PubMed] [Google Scholar]
  103. Stadtman E.R., Levine R.L. Protein oxidation. Ann N Y Acad Sci. 2000;899:191–208. doi: 10.1111/j.1749-6632.2000.tb06187.x. [DOI] [PubMed] [Google Scholar]
  104. Stewart C.R., Wilson L.M., Zhang Q., Pham C.L., Waddington L.J., Staples M.K., Stapleton D., Kelly J.W., Howlett G.J. Oxidized cholesterol metabolites found in human atherosclerotic lesions promote apolipoprotein C-II amyloid fibril formation. Biochemistry. 2007;46:5552–5561. doi: 10.1021/bi602554z. [DOI] [PubMed] [Google Scholar]
  105. Strittmatter W.J., Weisgraber K.H., Huang D.Y., Dong L.M., Salvesen G.S., Pericak-Vance M., Schmechel D., Saunders A. M., Goldgaber D., Roses A.D. Binding of human apolipoprotein E to synthetic amyloid beta peptide: isoform-specific effects and implications for late-onset Alzheimer disease. Proc Natl Acad Sci U S A. 1993;90:8098–8102. doi: 10.1073/pnas.90.17.8098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. Tennent G.A., Lovat L.B., Pepys M.B. Serum amyloid P component prevents proteolysis of the amyloid fibrils of Alzheimer disease and systemic amyloidosis. Proc Natl Acad Sci U S A. 1995;92:4299–4303. doi: 10.1073/pnas.92.10.4299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Teoh C.L., Pham C.L., Todorova N., Hung A., Lincoln C.N., Lees E., Lam Y.H., Binger K.J., Thomson N.H., Radford S.E., et al. A structural model for apolipoprotein C-II amyloid fibrils: experimental characterization and molecular dynamics simulations. J Mol Biol. 2011;405:1246–1266. doi: 10.1016/j.jmb.2010.12.006. [DOI] [PubMed] [Google Scholar]
  108. Teoh C.L., Yagi H., Griffin M.D., Goto Y., Howlett G.J. Visualization of polymorphism in apolipoprotein C-II amyloid fibrils. J Biochem. 2011;149:67–74. doi: 10.1093/jb/mvq117. [DOI] [PubMed] [Google Scholar]
  109. Todorova N., Hung A., Maaser S.M., Griffin M.D., Karas J., Howlett G.J., Yarovsky I. Effects of mutation on the amyloidogenic propensity of apolipoprotein C-II(60–70) peptide. Phys Chem Chem Phys. 2010;12:14762–14774. doi: 10.1039/c0cp00299b. [DOI] [PubMed] [Google Scholar]
  110. Westermark G.T., Johnson K.H., Westermark P. Staining methods for identification of amyloid in tissue. Methods Enzymol. 1999;309:3–25. doi: 10.1016/s0076-6879(99)09003-5. [DOI] [PubMed] [Google Scholar]
  111. Westermark P., Mucchiano G., Marthin T., Johnson K.H., Sletten K. Apolipoprotein A1-derived amyloid in human aortic atherosclerotic plaques. Am J Pathol. 1995;147:1186–1192. [PMC free article] [PubMed] [Google Scholar]
  112. Wilson L.M., Mok Y.F., Binger K.J., Griffin M.D., Mertens H.D., Lin F., Wade J.D., Gooley P.R., Howlett G.J. A structural core within apolipoprotein C-II amyloid fibrils identified using hydrogen exchange and proteolysis. J Mol Biol. 2007;366:1639–1651. doi: 10.1016/j.jmb.2006.12.040. [DOI] [PubMed] [Google Scholar]
  113. Wisniewski T., Lalowski M., Golabek A., Vogel T., Frangione B. Is Alzheimer’s disease an apolipoprotein E amyloidosis? Lancet. 1995;345:956–958. doi: 10.1016/s0140-6736(95)90701-7. [DOI] [PubMed] [Google Scholar]
  114. Wong Y.Q., Binger K.J., Howlett G.J., Griffin M.D. Methionine oxidation induces amyloid fibril formation by full-length apolipoprotein A-I. Proc Natl Acad Sci U S A. 2010;107:1977–1982. doi: 10.1073/pnas.0910136107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  115. Yagi H., Ban T., Morigaki K., Naiki H., Goto Y. Visualization and classification of amyloid beta supramolecular assemblies. Biochemistry. 2007;46:15009–15017. doi: 10.1021/bi701842n. [DOI] [PubMed] [Google Scholar]
  116. Yagi H., Ozawa D., Sakurai K., Kawakami T., Kuyama H., Nishimura O., Shimanouchi T., Kuboi R., Naiki H., Goto Y. Laser-induced propagation and destruction of amyloid beta fibrils. J Biol Chem. 2010;285:19660–19667. doi: 10.1074/jbc.M109.076505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  117. Zhang Q., Powers E.T., Nieva J., Huff M.E., Dendle M.A., Bieschke J., Glabe C.G., Eschenmoser A., Wentworth P., Jr, Lerner R.A., et al. Metabolite-initiated protein misfolding may trigger Alzheimer’s disease. Proc Natl Acad Sci U S A. 2004;101:4752–4757. doi: 10.1073/pnas.0400924101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  118. Zhao H., Tuominen E.K., Kinnunen P.K. Formation of amyloid fibers triggered by phosphatidylserine-containing membranes. Biochemistry. 2004;43:10302–10307. doi: 10.1021/bi049002c. [DOI] [PubMed] [Google Scholar]
  119. Zheng L., Nukuna B., Brennan M.L., Sun M., Goormastic M., Settle M., Schmitt D., Fu X., Thomson L., Fox P.L., et al. Apolipoprotein A-I is a selective target for myeloperoxidase-catalyzed oxidation and functional impairment in subjects with cardiovascular disease. J Clin Invest. 2004;114:529–541. doi: 10.1172/JCI21109. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Protein & Cell are provided here courtesy of Oxford University Press

RESOURCES