Fluorescence as a method to reveal structures and membrane-interactions of amyloidogenic proteins

Biochimica et Biophysica Acta - Biomembranes

Volumn 1768, Issue 8, 2007, Pages 1862-1885

  Munishkina, Larissa A ^a   Fink, Anthony L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aggregation; Amyloid; Fibrils; Fluorescence anisotropy; Fluorescence correlation spectroscopy; Fluorescence probes; Fluorescence resonance energy transfer; Membrane permeability; Oligomers; Protofibrils; Toxicity

Indexed keywords

ALPHA SYNUCLEIN; AMYLIN; AMYLOID; AMYLOID A PROTEIN; APOLIPOPROTEIN; FLUORESCENT DYE; IMMUNOGLOBULIN LIGHT CHAIN; POLYPEPTIDE; PREALBUMIN; PRION PROTEIN; RO ANTIBODY;

ALZHEIMER DISEASE; AMYLOIDOSIS; ANISOTROPY; BLOOD LEVEL; CELL DEATH; CORRELATION ANALYSIS; CYTOTOXICITY; FIBER; FLUORESCENCE; FLUORESCENCE CORRELATION SPECTROSCOPY; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; MEASUREMENT; MEMBRANE PERMEABILITY; MEMBRANE STRUCTURE; MOLECULAR INTERACTION; NON INSULIN DEPENDENT DIABETES MELLITUS; OLIGOMERIZATION; PARKINSON DISEASE; POLARIZATION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; REVIEW; STEADY STATE;

AMYLOID; AMYLOIDOSIS; ANIMALS; CELL DEATH; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; FLUORESCENCE; FLUOROMETRY; HUMANS; NEURODEGENERATIVE DISEASES; PROTEIN FOLDING; PROTEIN STRUCTURE, QUATERNARY;

EID: 34547174917     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2007.03.015     Document Type: Review

References (122)

1. Ragone R., Colonna G., Balestrieri C., Servillo L., and Irace G. Determination of tyrosine exposure in proteins by 2nd-derivative spectroscopy. Biochemistry 23 (1984) 1871-1875
2. Royer C.A. Probing protein folding and conformational transitions with fluorescence. Chem. Rev. 106 (2006) 1769-1784
3. LeVine H. Thioflavine T interaction with amyloid β-sheets structures. Amyloid 2 (1995) 1-6
4. Naiki H., Higuchi K., Hosokawa M., and Takeda T. Fluorometric determination of amyloid fibrils in vitro using the fluorescent dye, Thioflavin T. Anal. Biochem. 177 (1989) 244-249
5. Voropay E.S.S.M.P., Kaplevsky K.N., Maskevich A.A., Stepuro V.I., Povarova O.I., Kuznetsova I.M., Turoverov K.K., Fink A.L., and Uversky V.N. Spectral properties of Thioflavin T and its complexes with amyloid fibrils. J. Appl. Spectrosc. (Moscow) 70 (2003) 767-773
6. Hammarstrom P., Kalman B., Jonsson B.H., and Carlsson U. Pyrene excimer fluorescence as a proximity probe for investigation of residual structure in the unfolded state of human carbonic anhydrase II. FEBS Lett. 420 (1997) 63-68
7. Flora K., Brennan J.D., Baker G.A., Doody M.A., and Bright F.V. Unfolding of acrylodan-labeled human serum albumin probed by steady-state and time-resolved fluorescence methods. Biophys. J. 75 (1998) 1084-1096
8. Fradkov A.F., Verkhusha V.V., Staroverov D.B., Bulina M.E., Yanushevich Y.G., Martynov V.I., Lukyanov S., and Lukyanov K.A. Far-red fluorescent tag for protein labelling. Biochem. J. 368 (2002) 17-21
9. Griffin B.A., Adams S.R., and Tsien R.Y. Specific covalent labeling of recombinant protein molecules inside live cells. Science 281 (1998) 269-272
10. Stubbs C.D., and Williams B.W. Fluorescence in Membranes (1992), Plenum Press, New York 231-265
11. Lakowicz J.R. Principles of Fluorescence Spectroscopy (1983), Plenum Press, NY
12. Steiner R.F. Fluorescence Anisotropy: Theory and Applications (1992), Plenum Press, New York 1-52
13. Michalet X., Weiss S., and Jager M. Single-molecule fluorescence studies of protein folding and conformational dynamics. Chem. Rev. 106 (2006) 1785-1813
14. Stryer L. Fluorescence energy-transfer as a spectroscopic ruler. Annu. Rev. Biochem. 47 (1978) 819-846
15. Stryer L., and Haugland R.P. Energy transfer: a spectroscopic ruler. Proc. Natl. Acad. Sci. U. S. A. 58 (1967) 719-726
16. Haustein E., and Schwille P. Ultrasensitive investigations of biological systems by fluorescence correlation spectroscopy. Methods 29 (2003) 153-166
17. Bacia K., and Schwille P. A dynamic view of cellular processes by in vivo fluorescence auto- and cross-correlation spectroscopy. Methods 29 (2003) 74-85
18. Icenogle R.D., and Elson E.L. Fluorescence correlation spectroscopy and photobleaching recovery of multiple binding reactions. 1. Theory and FCS measurements. Biopolymers 22 (1983) 1919-1948
19. Elson E.L. Fluorescence Correlation Spectroscopy. I. Conceptual Basis and Theory (1974) 1-27
20. Yamaguchi K.I., Takahashi S., Kawai T., Naiki H., and Goto Y. Seeding-dependent propagation and maturation of amyloid fibril conformation. J. Mol. Biol. (2005)
21. Denk W., Strickler J.H., and Webb W.W. Two-Photon Laser Scanning Fluorescence Microscopy (1990) 73-76
22. Tycko R. Molecular structure of amyloid fibrils: insights from solid-state NMR. Q. Rev. Biophys. (2006) 1-55
23. Chan J.C., Oyler N.A., Yau W.M., and Tycko R. Parallel beta-Sheets and polar zippers in amyloid fibrils formed by residues 10-39 of the yeast prion protein Ure2p. Biochemistry 44 (2005) 10669-10680
24. Kajava A.V., Aebi U., and Steven A.C. The parallel superpleated beta-structure as a model for amyloid fibrils of human amylin. J. Mol. Biol. 348 (2005) 247-252
25. Luhrs T., Ritter C., Adrian M., Riek-Loher D., Bohrmann B., Dobeli H., Schubert D., and Riek R. 3D structure of Alzheimer's amyloid-beta(1-42) fibrils. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 17342-17347
26. Balbach J.J., Petkova A.T., Oyler N.A., Antzutkin O.N., Gordon D.J., Meredith S.C., and Tycko R. Supramolecular structure in full-length Alzheimer's beta-amyloid fibrils: evidence for a parallel beta-sheet organization from solid-state nuclear magnetic resonance. Biophys. J. 83 (2002) 1205-1216
27. Volles M.J., and Lansbury Jr. P.T. Zeroing in on the pathogenic form of alpha-synuclein and its mechanism of neurotoxicity in Parkinson's disease. Biochemistry 42 (2003) 7871-7878
28. Trojanowski J.Q., and Lee V.M. Parkinson's disease and related alpha-synucleinopathies are brain amyloidoses. Ann. N. Y. Acad. Sci. 991 (2003) 107-110
29. Uversky V.N. What does it mean to be natively unfolded?. Eur. J. Biochem. 269 (2002) 2-12
30. Dunker A.K., Brown C.J., and Obradovic Z. Identification and functions of usefully disordered proteins. Adv. Protein Chem. 62 (2002) 25-49
31. Li J., Uversky V.N., and Fink A.L. Conformational behavior of human alpha-synuclein is modulated by familial Parkinson's disease point mutations A30P and A53T. Neurotoxicology 23 (2002) 553-567
32. Davidson W.S., Jonas A., Clayton D.F., and George J.M. Stabilization of alpha-synuclein secondary structure upon binding to synthetic membranes. J. Biol. Chem. 273 (1998) 9443-9449
33. Bisaglia M., Tessari I., Pinato L., Bellanda M., Giraudo S., Fasano M., Bergantino E., Bubacco L., and Mammi S. A topological model of the interaction between alpha-Synuclein and sodium dodecyl sulfate micelles. Biochemistry 44 (2005) 329-339
34. Zhu M., Li J., and Fink A.L. The association of alpha-synuclein with membranes affects bilayer structure, stability, and fibril formation. J. Biol. Chem. 278 (2003) 40186-40197
35. Kaylor J., Bodner N., Edridge S., Yamin G., Hong D.P., and Fink A.L. Characterization of oligomeric intermediates in alpha-synuclein fibrillation: FRET studies of Y125W/Y133F/Y136F alpha-synuclein. J. Mol. Biol. 353 (2005) 357-372
36. Dusa A., Kaylor J., Edridge S., Bodner N., Hong D.P., and Fink A.L. Characterization of oligomers during alpha-synuclein aggregation using intrinsic tryptophan fluorescence. Biochemistry 45 (2006) 2752-2760
37. Uversky V.N., Li J., and Fink A.L. Evidence for a partially folded intermediate in alpha-synuclein fibril formation. J. Biol. Chem. 276 (2001) 10737-10744
38. Lee J.C., Langen R., Hummel P.A., Gray H.B., and Winkler J.R. {alpha}-Synuclein structures from fluorescence energy-transfer kinetics: implications for the role of the protein in Parkinson's disease. Proc. Natl. Acad. Sci U. S. A. 101 (2004) 16466-16471
39. Perrin R.J., Woods W.S., Clayton D.F., and George J.M. Interaction of human alpha-Synuclein and Parkinson's disease variants with phospholipids. Structural analysis using site-directed mutagenesis. J. Biol. Chem. 275 (2000) 34393-34398
40. Jo E., McLaurin J., Yip C.M., George-Hyslop P., and Fraser P.E. alpha-Synuclein membrane interactions and lipid specificity. J. Biol. Chem. 275 (2000) 34328-34334
41. Rhoades E., Ramlall T.F., Webb W.W., and Eliezer D. Quantification of {alpha}-Synuclein binding to lipid vesicles using fluorescence correlation spectroscopy. Biophys. J. 90 (2006) 4692-4700
42. Nuscher B., Kamp F., Mehnert T., Odoy S., Haass C., Kahle P.J., and Beyer K. alpha -Synuclein has a high affinity for packing defects in a bilayer membrane. A thermodynamics study. J. Biol. Chem. 279 (2004) 21966-21975
43. Kubo S., Nemani V.M., Chalkley R.J., Anthony M.D., Hattori N., Mizuno Y., Edwards R.H., and Fortin D.L. A combinatorial code for the interaction of alpha-synuclein with membranes. J. Biol. Chem. 280 (2005) 31664-31672
44. Eliezer D., Kutluay E., Bussell Jr. R., and Browne G. Conformational properties of alpha-synuclein in its free and lipid- associated states. J. Mol. Biol. 307 (2001) 1061-1073
45. Bussell Jr. R., and Eliezer D. A structural and functional role for 11-mer repeats in alpha-synuclein and other exchangeable lipid binding proteins. J. Mol. Biol. 329 (2003) 763-778
46. Bussell Jr. R., and Eliezer D. Effects of Parkinson's disease-linked mutations on the structure of lipid-associated alpha-synuclein. Biochemistry 43 (2004) 4810-4818
47. Dedmon M.M., Lindorff-Larsen K., Christodoulou J., Vendruscolo M., and Dobson C.M. Mapping long-range interactions in alpha-synuclein using spin-label NMR and ensemble molecular dynamics simulations. J. Am. Chem. Soc. 127 (2005) 476-477
48. Ulmer T.S., Bax A., Cole N.B., and Nussbaum R.L. Structure and dynamics of micelle-bound human alpha-synuclein. J. Biol. Chem. 280 (2005) 9595-9603
49. Chandra S., Chen X., Rizo J., Jahn R., and Sudhof T.C. A broken alpha -helix in folded alpha -synuclein. J. Biol. Chem. 278 (2003) 15313-15318
50. Perrin R.J., Woods W.S., Clayton D.F., and George J.M. Exposure to long chain polyunsaturated fatty acids triggers rapid multimerization of synucleins. J. Biol. Chem. 276 (2001) 41958-41962
51. Cole N.B., Murphy D.D., Grider T., Rueter S., Brasaemle D., and Nussbaum R.L. Lipid droplet binding and oligomerization properties of the Parkinson's disease protein alpha-synuclein. J. Biol. Chem. 277 (2002) 6344-6352
52. Lee H.J., Choi C., and Lee S.J. Membrane-bound alpha-synuclein has a high aggregation propensity and the ability to seed the aggregation of the cytosolic form. J. Biol. Chem. 277 (2002) 671-678
53. Zhu M., and Fink A.L. Lipid binding inhibits alpha-synuclein fibril formation. J. Biol. Chem. 278 (2003) 16873-16877
54. Jo E., Darabie A.A., Han K., Tandon A., Fraser P.E., and McLaurin J. alpha-Synuclein-synaptosomal membrane interactions: implications for fibrillogenesis. Eur. J. Biochem. 271 (2004) 3180-3189
55. Kamp F., and Beyer K. Binding of alpha-synuclein affects the lipid packing in bilayers of small vesicles. J. Biol. Chem. 281 (2006) 9251-9259
56. Volles M.J., and Lansbury Jr. P.T. Vesicle permeabilization by protofibrillar alpha-synuclein is sensitive to Parkinson's disease-linked mutations and occurs by a pore-like mechanism. Biochemistry 41 (2002) 4595-4602
57. Outeiro T.F., and Lindquist S. Yeast cells provide insight into alpha-synuclein biology and pathobiology. Science 302 (2003) 1772-1775
58. Jo E., Fuller N., Rand R.P., George-Hyslop P., and Fraser P.E. Defective membrane interactions of familial Parkinson's disease mutant A30P alpha-synuclein. J. Mol. Biol. 315 (2002) 799-807
59. Fortin D.L., Troyer M.D., Nakamura K., Kubo S., Anthony M.D., and Edwards R.H. Lipid rafts mediate the synaptic localization of alpha-synuclein. J. Neurosci. 24 (2004) 6715-6723
60. Fortin D.L., Nemani V.M., Voglmaier S.M., Anthony M.D., Ryan T.A., and Edwards R.H. Neural activity controls the synaptic accumulation of alpha-synuclein. J. Neurosci. 25 (2005) 10913-10921
61. Kakio A., Nishimoto S.I., Yanagisawa K., Kozutsumi Y., and Matsuzaki K. Cholesterol-dependent formation of GM1 ganglioside-bound amyloid beta-protein, an endogenous seed for Alzheimer amyloid. J. Biol. Chem. 276 (2001) 24985-24990
62. Kakio A., Yano Y., Takai D., Kuroda Y., Matsumoto O., Kozutsumi Y., and Matsuzaki K. Interaction between amyloid beta-protein aggregates and membranes. J. Pept. Sci. 10 (2004) 612-621
63. Mandal P.K., and Pettegrew J.W. Alzheimer's disease: soluble oligomeric Abeta(1-40) peptide in membrane mimic environment from solution NMR and circular dichroism studies. Neurochem. Res. 29 (2004) 2267-2272
64. Kremer J.j., Sklansky D.J., and Murphy R.M. Profile of changes in lipid bilayer structure caused by beta amyloid peptide. Biochemistry 40 (2001) 8563-8571
65. Ban T., Hoshino M., Takahashi S., Hamada D., Hasegawa K., Naiki H., and Goto Y. Direct observation of Abeta amyloid fibril growth and inhibition. J. Mol. Biol. 344 (2004) 757-767
66. Chen Y.R., and Glabe C.G. Distinct early folding and aggregation properties of Alzheimer amyloid-beta peptide Abeta 40 and Abeta 42: stable trimer or tetramer formation by Abeta 42. J. Biol. Chem. 281 (2006) 24414-24422
67. Prusiner S.B. The prion diseases. Sci. Am. 272 (1995) 48-51
68. Taylor D.R., and Hooper N.M. The prion protein and lipid rafts. (Review). Mol. Membr. Biol. 23 (2006) 89-99
69. Zahn R., Guntert P., von Schroetter C., and Wuthrich K. NMR structure of a variant human prion protein with two disulfide bridges. J. Mol. Biol. 326 (2003) 225-234
70. Zahn R. The octapeptide repeats in mammalian prion protein constitute a pH-dependent folding and aggregation site. J. Mol. Biol. 334 (2003) 477-488
71. Legname G., Baskakov I.V., Nguyen H.O.B., Riesner D., Cohen F.E., DeArmond S.J., and Prusiner S.B. Synthetic mammalian prions. Science 305 (2004) 673-676
72. Laws D.D., Bitter H.M.L., Liu K., Ball H.L., Kaneko K., Wille H., Cohen F.E., Prusiner S.B., Pines A., and Wemmer D.E. Solid-state NMR studies of the secondary structure of a mutant prion protein fragment of 55 residues that induces neurodegeneration. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 11686-11690
73. Baskakov I.V., and Bocharova O.V. In vitro conversion of mammalian prion protein into amyloid fibrils displays unusual features. Biochemistry 44 (2005) 2339-2348
74. Wadsworth J.D., Hill A.F., Joiner S., Jackson G.S., Clarke A.R., and Collinge J. Strain-specific prion-protein conformation determined by metal ions. Nat. Cell Biol. 1 (1999) 55-59
75. Morillas M., Swietnicki W., Gambetti P., and Surewicz W.K. Membrane environment alters the conformational structure of the recombinant human prion protein. J. Biol. Chem. 274 (1999) 36859-36865
76. Renner C., Fiori S., Fiorino F., Landgraf D., Deluca D., Mentler M., Grantner K., Parak F.G., Kretzschmar H., and Moroder L. Micellar environments induce structuring of the N-terminal tail of the prion protein. Biopolymers 73 (2004) 421-433
77. Chattopadhyay M., Walter E.D., Newell D.J., Jackson P.J., Aronoff-Spencer E., Peisach J., Gerfen G.J., Bennett B., Antholine W.E., and Millhauser G.L. The octarepeat domain of the prion protein binds Cu(II) with three distinct coordination modes at pH 7.4. J. Am. Chem. Soc. 127 (2005) 12647-12656
78. Burns C.S., Aronoff-Spencer E., Dunham C.M., Lario P., Avdievich N.I., Antholine W.E., Olmstead M.M., Vrielink A., Gerfen G.J., Peisach J., Scott W.G., and Millhauser G.L. Molecular features of the copper binding sites in the octarepeat domain of the prion protein. Biochemistry 41 (2002) 3991-4001
79. Whittal R.M., Ball H.L., Cohen F.E., Burlingame A.L., Prusiner S.B., and Baldwin M.A. Copper binding to octarepeat peptides of the prion protein monitored by mass spectrometry. Protein Sci. 9 (2000) 332-343
80. Jackson G.M., Murray I., Hosszu L.L., Gibbs N., Waltho J.P., Clarke A.R., and Collinge J. Location and properties of metal-binding sites on the human prion protein. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 8531-8535
81. Novitskaya V., Makarava N., Bellon A., Bocharova O.V., Bronstein I.B., Williamson R.A., and Baskakov I.V. Probing the conformation of the prion protein within a single amyloid fibril using a novel immunoconformational assay. J. Biol. Chem. 281 (2006) 15536-15545
82. Bocharova O.V., Breydo L., Parfenov A.S., Salnikov V.V., and Baskakov I.V. In vitro conversion of full-length mammalian prion protein produces amyloid form with physical properties of PrPSc. J. Mol. Biol. 346 (2005) 645-659
83. Benkemoun L., and Saupe S.J. Prion proteins as genetic material in fungi. Fungal Genet. Biol. 43 (2006) 789-803
84. Krishnan R., and Lindquist S.L. Structural insights into a yeast prion illuminate nucleation and strain diversity. Nature 435 (2005) 765-772
85. Solomon A. Clinical implications of monoclonal light chains. Semin. Oncol. 13 (1986) 341-349
86. Gallo G., Picken M., Buxbaum J., and Frangione B. The spectrum of monoclonal immunoglobulin deposition disease associated with immunocytic dyscrasias. Semin. Hematol. 26 (1989) 234-245
87. Alpers C.E., Tu W.H., Hopper Jr. J., and Biava C.G. Single light chain subclass (kappa chain) immunoglobulin deposition in glomerulonephritis. Hum. Pathol. 16 (1985) 294-304
88. Stevens P.W., Raffen R., Hanson D.K., Deng Y.L., Berrioshammond M., Westholm F.A., Murphy C., Eulitz M., Wetzel R., Solomon A., Schiffer M., and Stevens F.J. Recombinant immunoglobulin variable domains generated from synthetic genes provide a system for in-vitro characterization of light-chain amyloid proteins. Protein Sci. 4 (1995) 421-432
89. Khurana R., Gillespie J.R., Talapatra A., Minert L.J., Ionescu-Zanetti C., Millett I., and Fink A.L. Partially folded intermediates as critical precursors of light chain amyloid fibrils and amorphous aggregates. Biochemistry 40 (2001) 3525-3535
90. Teng J., Russell W.J., Gu X., Cardelli J., Jones M.L., and Herrera G.A. Different types of glomerulopathic light chains interact with mesangial cells using a common receptor but exhibit different intracellular trafficking patterns. Lab. Invest. 84 (2004) 440-451
91. X. Meng, A.L. Fink, The effect of membranes on the in vitro fibrillation of an amyloidogenic light chain variable domain. Manuscript (submitted for publication).
92. Zhu M., Souillac P.O., Ionescu-Zanetti C., Carter S.A., and Fink A.L. Surface-catalyzed amyloid fibril formation. J. Biol. Chem. 277 (2002) 50914-50922
93. Blake C.C., Geisow M.J., Oatley M.J., Regat B., and Regat C. Structure of prealbumin: secondary, tertiary and quaternary interactions determined by Fourier refinement at 1.8 Å resolution. J Mol. Biol. 121 (1978) 339-356
94. Johnson S.M., Wiseman R.L., Sekijima Y., Green N.S., Adamski-Werner S.L., and Kelly J.W. Native state kinetic stabilization as a strategy to ameliorate protein misfolding diseases: a focus on the transthyretin amyloidoses. Acct. Chem. Res. 38 (2005) 911-921
95. Lindgren M., Sorgjerd K., and Hammarstrom P. Detection and characterization of aggregates, prefibrillar amyloidogenic oligomers and protofibrils using fluorescence spectroscopy. Biophys. J. 88 (2005) 4200-4212
96. Hou X., Richardson S.J., Aguilar M.I., and Small D.H. Binding of amyloidogenic transthyretin to the plasma membrane alters membrane fluidity and induces neurotoxicity. Biochemistry 44 (2005) 11618-11627
97. Manley P.N., Ancsin J.B., and Kisilevsky R. Rapid recycling of cholesterol: the joint biologic role of C-reactive protein and serum amyloid A. Med. Hypotheses 66 (2006) 784-792
98. Bausserman L.L., Herbert P.N., Forte T., Klausner R.D., Mcadam K.P.W.J., Osborne J.C., and Rosseneu M. Interaction of the serum amyloid a proteins with phospholipid. J. Biol. Chem. 258 (1983) 681-688
99. Sipe J.D. Amyloidosis. Crit. Rev. Clin. Lab. Sci. 31 (1994) 325-354
100. Buxbaum J.N. The systemic amyloidoses. Curr. Opin. Rheumatol. 16 (2004) 67-75
101. Sipe J.D., Mcadam K.P.W.J., Torain B.F., and Pollock P.S. Isolation and structural-properties of murine saa-acute phase serum precursor of amyloid Aa. Immunol. Commun. 6 (1977) 1-12
102. Hirakura Y., Carreras I., Sipe J.D., and Kagan B.L. Channel formation by serum amyloid A: a potential mechanism for amyloid pathogenesis and host defense. Amyloid 9 (2002) 13-23
103. Takahashi M., Yokota T., Kawano H., Gondo T., Ishihara T., and Uchino F. Ultrastructural evidence for intracellular formation of amyloid fibrils in macrophages. Virch. Arch., A Pathol. Anat. Histopathol. 415 (1989) 411-419
104. Shirahama T., and Cohen A.S. Intralysosomal formation of amyloid fibrils. Am. J. Pathol. 81 (1975) 101-&
105. Chronopoulos S., Laird D.W., and Alikhan Z. Immunolocalization of serum Amyloid-A and Aa-Amyloid in lysosomes in murine monocytoid cells-confocal and immunogold electron-microscopic studies. J. Pathol. 173 (1994) 361-369
106. Kluve-Beckerman B., Manaloor J.J., and Liepnieks J.J. A pulse-chase study tracking the conversion of macrophage-endocytosed serum amyloid A into extracellular amyloid. Arthrithis Rheum. 46 (2002) 1905-1913
107. Kluve-Beckerman B., Manaloor J., and Leipnieks J.J. Binding, trafficking and accumulation of serum amyloid A in peritoneal macrophages. Scand. J. Immunol. 53 (2001) 393-400
108. Alaupovic P. The concept of apolipoprotein-defined lipoprotein families and its clinical significance. Curr. Atheroscler. Rep. 5 (2003) 459-467
109. Krimbou L., Marcil M., and Genest J. New insights into the biogenesis of human high-density lipoproteins. Curr. Opin. Lipidol. 17 (2006) 258-267
110. Howlett G.J., and Moore K. Untangling the role of amyloid in atherosclerosis. Curr. Opin. Lipidol. 17 (2006) 541-547
111. Andreola A., Bellotti V., Giorgetti S., Mangione P., Obici L., Stoppini M., Torres J., Monzani E., Merlini G., and Sunde M. Conformational switching and fibrillogenesis in the amyloidogenic fragment of apolipoprotein a-I. J. Biol. Chem. 278 (2003) 2444-2451
112. Benson M.D., Liepnieks J.J., Yazaki M., Yamashita T., Hamidi A.K., Guenther B., and Kluve-Beckerman B. A new human hereditary amyloidosis: the result of a stop-codon mutation in the apolipoprotein AII gene. Genomics 72 (2001) 272-277
113. Segrest J.P., Jones M.K., De Loof H., Brouillette C.G., Venkatachalapathi Y.V., and Anantharamaiah G.M. The amphipathic helix in the exchangeable apolipoproteins: a review of secondary structure and function. J. Lipid Res. 33 (1992) 141-166
114. Maiorano J.N., Jandacek R.J., Horace E.M., and Davidson W.S. Identification and structural ramifications of a hinge domain in apolipoprotein A-I discoidal high-density lipoproteins of different size. Biochemistry 43 (2004) 11717-11726
115. Li H.H., Lyles D.S., Pan W., Alexander E., Thomas M.J., and Sorci-Thomas M.G. ApoA-I structure on discs and spheres-Variable helix registry and conformational states. J. Biol. Chem. 277 (2002) 39093-39101
116. Tricerri M.A., Agree A.K.B., Sanchez S.A., Bronski J., and Jonas A. Arrangement of apolipoprotein A-I in reconstituted high-density lipoprotein disks: an alternative model based on fluorescence resonance energy transfer experiments. Biochemistry 40 (2001) 5065-5074
117. Cooper G.J., Willis A.C., Clark A., Turner R.C., Sim R.B., and Reid K.B. Purification and characterization of a peptide from amyloid-rich pancreases of type 2 diabetic patients. Proc. Natl. Acad. Sci. U. S. A. 84 (1987) 8628-8632
118. Hoppener J.W., Oosterwijk C., van Hulst K.L., Verbeek J.S., Capel P.J., de Koning E.J., Clark A., Jansz H.S., and Lips C.J. Molecular physiology of the islet amyloid polypeptide (IAPP)/amylin gene in man, rat, and transgenic mice. J. Cell. Bioch. 55 (1994) 39-53 (Suppl.)
119. Lorenzo A., Razzaboni B., Weir G.C., and Yankner B.A. Pancreatic islet cell toxicity of amylin associated with type-2 diabetes mellitus. Nature 368 (1994) 756-760
120. Padrick S.B., and Miranker A.D. Islet amyloid polypeptide: identification of long-range contacts and local order on the fibrillogenesis pathway. J. Mol. Biol. 308 (2001) 783-794
121. Porat Y., Kolusheva S., Jelinek R., and Gazit E. The human islet amyloid polypeptide forms transient membrane-active prefibrillar assemblies. Biochemistry 42 (2003) 10971-10977
122. Demuro A., Mina E., Kayed R., Milton S.C., Parker I., and Glabe C.G. Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers. J. Biol. Chem. 280 (2005) 17294-17300