On the use of size exclusion chromatography for the resolution of mixed amyloid aggregate distributions: I. Equilibrium partition models

Analytical Biochemistry

Volumn 426, Issue 1, 2012, Pages 69-85

  Hall, Damien ^a   Huang, Li ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Amyloid; Amyloid size distribution; Macromolecular crowding; Purification; Size exclusion chromatography

Indexed keywords

AGGREGATES; GLYCOPROTEINS; MAMMALS; PROTEINS; PURIFICATION; SOLUTE TRANSPORT;

AGGREGATE DISTRIBUTION; AMYLOID; EQUILIBRIUM PARTITION; MACROMOLECULAR CROWDING; MOLECULAR DIMENSIONS; PARTITION COEFFICIENT; PHYSICOCHEMICAL FEATURES; PROTEIN AGGREGATES;

SIZE EXCLUSION CHROMATOGRAPHY;

AMYLOID; BOVINE INSULIN;

ARTICLE; ELUTION; GEL PERMEATION CHROMATOGRAPHY; MATHEMATICAL MODEL; MOLECULAR SIZE; PARTITION COEFFICIENT; PHYSICAL CHEMISTRY; PREDICTION; PRIORITY JOURNAL;

BOVINAE;

EID: 84860788280     PISSN: 00032697     EISSN: 10960309     Source Type: Journal    
DOI: 10.1016/j.ab.2012.04.001     Document Type: Article

References (107)

1. G.G. Glenner, E.D. Eanes, H.A. Bladen, R.P. Linke, and J.D. Termine β-Pleated sheet fibrils: a comparison of native amyloid with synthetic protein fibrils J. Histochem. Cytochem. 22 1974 1141 1158
2. C.M. Dobson The structural basis of protein folding and its links with human disease Philos. Trans. R Soc. Lond. B 356 2001 133 145
3. J. Inaki Guijarro, M. Sunde, J.A. Jones, I.D. Campbell, and C.M. Dobson Amyloid fibril formation by an SH3 domain Proc. Natl. Acad. Sci. USA 95 1998 4224 4228
4. S.K. Maji, L. Wang, J. Greenwald, and R. Riek Structure-activity relationship of amyloid fibrils FEBS Lett. 583 2009 2610 2617
5. E. Norrby Prions and protein-folding diseases J. Intern. Med. 270 2011 1 14
6. M.B. Pepys Amyloidosis Annu. Rev. Med. 57 2006 223 241
7. D.J. Selkoe Resolving controversies on the path to Alzheimer's therapeutics Nat. Med. 17 2011 1060 1065
8. D. Hall, and H. Edskes A model of amyloid's role in disease based on fibril fracture Biophys. Chem. 145 2009 17 28
9. T.P.J. Knowles, and M.J. Buehler Nanomechanics of functional and pathological amyloid materials Nat. Nanotechnol. 6 2011 469 479
10. W.H. Suh, K.S. Suslick, G.D. Stucky, and Y.H. Suh Nanotechnology, nanotoxicology, and neuroscience Prog. Neurobiol. 87 2009 133 170
11. D. Hall Semi-automated methods for simulation and measurement of amyloid fiber distributions obtained from transmission electron microscopy experiments Anal. Biochem. 421 2012 262 277
12. D.L. Cox, H. Lashuel, K.Y.C. Lee, and R.R.P. Singh The materials science of protein aggregation MRS Bull. 30 2005 452 457
13. E. Kasotakis, E. Mossou, L. Adler-Abramovich, E.P. Mitchell, V. Trevor-Forsyth, E. Gazit, and A. Mitraki Design of metal-binding sites onto self-assembled peptide fibrils Biopolymers 92 2009 164 172
14. M.D. Sipe, J.N. Benson, S. Buxbaum, G. Ikeda, M.J. Merlini, M.J. Saraiva, and P. Westermark Amyloid fibril protein nomenclature: 2010. Recommendations from the nomenclature committee of the International Society of Amyloidosis Amyloid 17 2010 2010 101 104
15. U. Baxa Structural basis of infectious and non-infectious amyloids Curr. Alzheim. Res. 5 2008 308 318
16. F. Shewmaker, R.P. McGlinchey, and R.B. Wickner Structural insights into functional and pathological amyloid J. Biol. Chem. 286 2011 16533 16540
17. K.N. Hu, R.P. McGlinchey, R.B. Wickner, and R. Tycko Segmental polymorphism in a functional amyloid Biophys. J. 101 2011 2242 2250
18. A.K. Chamberlain, C.E. MacPhee, J. Zurdo, L.A. Morozova-Roche, H.A. Hill, C.M. Dobson, and J.J. Davis Ultrastructural organization of amyloid fibrils by atomic force microscopy Biophys. J. 79 2000 3282 3293
19. M. Fändrich On the structural definition of amyloid fibrils and other polypeptide aggregates Cell. Mol. Life Sci. 64 2007 2066 2078
20. J. Adamcik, J. Jung, J. Flakowski, P. De Los Rios, G. Dietler, and R. Mezzenga Understanding amyloid aggregation by statistical analysis of atomic force microscopy Nat. Nanotechnol. 5 2010 423 428
21. S.S. Rogers, P. Venema, L.M.C. Sagis, E. van der Linden, and A.M. Donald Measuring the length distribution of a fibril system: a flow birefringence technique applied to amyloid fibrils Macromolecules 38 2005 2948 2958
22. M.R.H. Krebs, K.R. Domike, and A.M. Donald Protein aggregation: more than just fibrils Biochem. Soc. Trans. 37 2009 682 686
23. M.R.H. Krebs, G.L. Devlin, and A.M. Donald Protein particulates: another generic form of protein aggregation Biophys. J. 92 2007 1336 1342
24. K.J. Binger, C.L. Pham, L.M. Wilson, M.F. Bailey, L.J. Lawrence, P. Schuck, and G.J. Howlett Apolipoprotein C-II amyloid fibrils assemble via a reversible pathway that includes fibril breaking and rejoining J. Mol. Biol. 376 2008 1116 1129
25. S. Tzaban, G. Friedlander, O. Schonberger, L. Horonchik, Y. Yedidia, G. Shaked, R. Gabizon, and A. Taraboulos Protease-sensitive scrapie prion protein in aggregates of heterogeneous sizes Biochemistry 41 2002 12868 12875
26. D.M. Walsh, A. Lomakin, G.B. Benedek, M.M. Condron, and D.B. Teplow Amyloid β-protein fibrillogenesis: detection of a protofibrillar intermediate J. Biol. Chem. 272 1997 22364 22372
27. D.M. Hartley, D.W. Walsh, C.P. Ye, T. Diehl, S. Vasquez, P.M. Vassilev, D.B. Teplow, and D.J. Selkoe Protofibrillar intermediates of amyloid β-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons J. Neurosci. 19 1999 8876 8884
28. A. Jan, D.M. Hartley, and H.A. Lashuel Preparation and characterization of toxic Aβ aggregates for structural and functional studies in Alzheimer's disease research Nat. Protoc. 5 2010 1186 1209
29. H. Fukumoto, T. Tokuda, T. Kasai, N. Ishigami, H. Hidaka, M. Kondo, D. Allsop, and M. Nakagawa High-molecular-weight β-amyloid oligomers are elevated in cerebrospinal fluid of Alzheimer patients FASEB J. 24 2010 2716 2726
30. J. Porath, and P. Flodin Gel filtration: a method for desalting and group separation Nature 183 1959 1657 1659
31. D.J. Winzor Analytical exclusion chromatography J. Biochem. Biophys. Methods 56 2004 15 52
32. H. Barth, B.E. Boyes, and C. Jackson Size exclusion chromatography and related separation techniques Anal. Chem. 70 1998 251R 278R
33. A.M. Striegel, W.W. Yau, J.J. Kirkland, and D.D. Bly Modern Size-Exclusion Liquid Chromatography: Practice of Gel Permeation and Gel Filtration Chromatography second ed. 2009 John Wiley New York
34. J.S. Philo A critical review of methods for size characterization of non-particulate protein aggregates Curr. Pharm. Biotechnol. 10 2009 359 372
35. J.C. Giddings, E. Kucera, C.R. Russell, and M.N. Myers Statistical theory for the equilibrium distribution of rigid molecules in inert porous networks: exclusion chromatography J. Phys. Chem. 72 1968 4397 4408
36. M.A. Kuntz, P.L. Dubin, J.I. Kaplan, and M.S. Mehta Evaluation of models for size exclusion chromatography of asymmetric solutes J. Phys. Chem. 98 1994 7063 7067
37. T.C. Laurent, and J. Killander A theory of gel filtration and its experimental verification J. Chromatogr. 14 1964 317 330
38. Y. Wang, I. Teraoka, F.Y. Hansen, G.H. Peters, and O. Hassager A theoretical study of the separation principle in size exclusion chromatography Macromolecules 43 2010 1651 1659
39. S. Ceru, S.J. Kokalj, S. Rabzelj, M. Skarabot, I. Gutierrez-Aguirre, N. Kopitar-Jerala, G. Anderluh, D. Turk, V. Turk, and E. Zerovnik Size and morphology of toxic oligomers of amyloidogenic proteins: a case study of human stefin B Amyloid 15 2008 147 159
40. G.W. Bushnell, G.V. Louie, and G.D. Brayer High-resolution three-dimensional structure of horse heart cytochrome c J. Mol. Biol. 214 1990 585 596
41. O. Kasyutich, A. Ilari, A. Fiorillo, D. Tatchev, A. Hoell, and P. Ceci Silver ion incorporation and nanoparticle formation inside the cavity of Pyrococcus furiosus Ferritin: structural and size distribution analyses J. Am. Chem. Soc. 132 2010 3621 3628
42. S. Sugio, A. Kashima, S. Mochizuki, M. Noda, and K. Kobayashi Crystal structure of human serum albumin at 2.5 Å resolution Prot. Eng. 12 1999 439 449
43. H.K. Song, and S.W. Suh Kunitz-type soybean trypsin inhibitor revisited: refined structure of its complex with porcine trypsin reveals an insight into the interaction between a homologous inhibitor from Erythrina caffra and tissue-type plasminogen activator J. Mol. Biol. 275 1998 347 357
44. H. Uchikoba, S. Fushinobu, T. Wakagi, M. Konno, H. Taguchi, and H. Matsuzawa Crystal structure of non-allosteric l-lactate dehydrogenase from Lactobacillus pentosus at 2.3 Å resolution: specific interactions at subunit interfaces Proteins 46 2002 206 216
45. R. Berisio, F. Sica, V.S. Lamzin, K.S. Wilson, A. Zagari, and L. Mazzarella Atomic resolution structures of ribonuclease A at six pH values Acta Crystallogr. D 58 2002 441 451
46. P.E. Stein, A.G. Leslie, J.T. Finch, and R.W. Carrell Crystal structure of uncleaved ovalbumin at 1.95 Å resolution J. Mol. Biol. 221 1991 941 949
47. J.L. White, M.L. Hackert, T.M. Buehner, M.J. Adams, G.C. Ford, P.J. Lentz, I.E. Smiley, S.J. Steindell, and M.G. Rossmann A comparison of the structures of apo-dogfish M4 lactate dehydrogenase and its ternary complexes J. Mol. Biol. 102 1976 759 766
48. J. Jiracek, L. Zakova, E. Antolikova, C.J. Watson, J.P. Turkenburg, G.G. Dodson, and A.M. Brzozowski Implications for the active form of human insulin based on the structural convergence of highly active hormone analogues Proc. Natl. Acad. Sci. USA 107 2010 1966 1971
49. GE Healthcare, technical document 71-7000-00-AG-Superose 6 PC 3.2/30 1.
50. H.M. Jaeger, and S.R. Nagel Physics of the granular state Science 235 1992 1523 1531
51. S. Torquato, T.M. Truskett, and P.G. Debenedetti Is random close packing of spheres well defined? Phys. Rev. Lett. 84 2000 2064 2067
52. R. Kurita, and E.R. Weeks Experimental study of random-close-packed colloidal particles Phys. Rev. E 82 2010 011403
53. M.J. Lu Preparation of beaded organic polymers and their use in size exclusion chromatography C. San-Wu, Column Handbook for Size-Exclusion Chromatography 1999 Academic Press San Diego
54. T. Andersson, M. Carlsson, L. Hagel, P. Pernemalm, and J. Jansson Agarose-based media for high resolution gel filtration of biopolymers J. Chromatogr. A 326 1985 33 44
55. M. Eisentein A look back: adventures in the matrix Nat. Methods 3 2006 410 411
56. K.E. Thompson, and H.S. Fogler Modelling flow in disordered packed beds from pore-scale fluid mechanics AIChE J. 43 1997 1377 1389
57. X. Subagyo, N. Standish, and N.A. Brooks A new model of velocity distribution of a single-phase fluid flowing in packed beds Chem. Eng. Sci. 53 1998 1375 1385
58. T. Dumas, F. Lesage, and M.A. Latifi Modelling and measurements of the velocity gradient and local flow direction at the pore scale of a packed bed Chem. Eng. Res. Des. 88 2010 379 384
59. T. Takeuchi, X. Siswoyo, Z. Aspanut, and L.W. Lim Hydrodynamic chromatography of silica colloids on small spherical nonporous silica particles Anal. Sci. 25 2009 301 306
60. R. Edam, S. Eeltink, D.J.D. Vanhoutte, W.T. Kok, and P.J. Schoenmakers Hydrodynamic chromatography of macromolecules using polymer monolithic columns J. Chromatogr. A 1218 2011 8638 8645
61. J.C. Giddings, F.J.F. Yang, and M.N. Myers Field flow fractionation: a versatile new separation method Science 193 1976 1244 1245
62. G. Yohannes, M. Jussila, K. Hartonen, and M.L. Riekkola Asymmetrical flow-field fractionation technique for separation and characterization of biopolymers and bioparticles J. Chromatogr. A 1218 2011 4104 4116
63. T. Atmakidis, and E.Y. Kenig CFD-based analysis of the wall effect on the pressure drop in packed beds with moderate tube/particle diameter ratios in the laminar flow regime Chem. Eng. J. 155 2009 404 410
64. R.B. Bird, W.E. Stewart, and N.E. Lightfoot Transport Phenomena 2002 John Wiley New York
65. R. Bowley, and M. Sanchez Introductory Statistical Mechanics second ed. 1996 Clarendon Oxford, UK
66. J. Schnitzer Analysis of steric partition behavior of molecules in membranes using statistical physics Biophys. J. 54 1988 1065 1076
67. A.G. Ogston The spaces in a uniform random suspension of fibres Trans. Faraday Soc. 54 1958 1754 1757
68. J.P. Hansen, and I.D. McDonald Theory of Simple Liquids third ed. 2006 Academic Press San Diego
69. Z.D. Li, D.P. Cao, and J.Z. Wu Density-functional theory and Monte Carlo simulation for the surface structure and correlation functions of freely jointed Lennard-Jones polymeric fluids J. Chem. Phys. 122 2004 174708
70. S. Asakura, and F. Oosawa On interaction between two bodies immersed in a solution of macromolecules J. Chem. Phys. 22 1954 1255 1256
71. S. Asakura, and F. Oosawa Interaction between particles suspended in solutions of macromolecules J. Polym. Sci. 33 1958 183 192
72. T.C. Laurent The interaction between polysaccharides and other macromolecules: 9. The exclusion of molecules from hyaluronic acid gels and solutions Biochem. J. 93 1964 106 112
73. A.P. Minton, and J. Wilf Effect of macromolecular crowding upon the structure and function of an enzyme: glyceraldehyde-3-phosphate dehydrogenase Biochemistry 20 1981 4821 4826
74. S.J. Harris, and D.J. Winzor Effect of thermodynamic nonideality on the subcellular distribution of enzyme adsorption of aldolase to muscle myofibrils Arch. Biochem. Biophys. 243 1985 598 604
75. S.B. Zimmerman, and A.P. Minton Macromolecular crowding: biochemical, biophysical, and physiological consequences Annu. Rev. Biophys. Biomol. Struct. 22 1992 27 65
76. D. Hall, and A.P. Minton Macromolecular crowding: qualitative and semi-quantitative successes, quantitative challenges Biochim. Biophys. Acta 1649 2003 127 139
77. S.M. Oversteegen, and R. Roth General methods for free-volume theory J. Chem. Phys. 122 2005 214502
78. H.X. Zhou, G. Rivas, and A.P. Minton Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences Annu. Rev. Biophys. 37 2008 375 397
79. D. Hall, and A.P. Minton Effects of inert volume-excluding macromolecules on protein fiber formation: I. Equilibrium models Biophys. Chem. 98 2002 93 104
80. B. Solomon, R. Koppel, D. Frankel, and E. Hanan-Aharon Disaggregation of Alzheimer β-amyloid by site-directed mAb Proc. Natl. Acad. Sci. USA 94 1997 4109 4112
81. R. Kayed, Y. Sokolov, B. Edmonds, T.M. McIntire, S.C. Milton, J.E. Hall, and C.G. Glabe Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases J. Biol. Chem. 279 2004 46363 46366
82. M. Bucciantini, E. Giannoni, F. Chiti, F. Baroni, L. Formigli, J. Zurdo, N. Taddei, G. Ramponi, C.M. Dobson, and M. Stefani Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases Nature 416 2002 507 511
83. C. Glabe Structural classification of toxic amyloid oligomers J. Biol. Chem. 283 2008 29639 29643
84. W.L. Klein Aβ toxicity in Alzheimer's disease: globular oligomers (ADDLs) as new vaccine and drug targets Neurochem. Int. 41 2002 345 352
85. K.A. Dill, and S.A. Bromberg Molecular Driving Forces: Statistical Thermodynamics in Chemistry and Biology 2003 Garland Science New York
86. C.R. Cantor, and P.R. Schimmel Biophysical Chemistry. Part 1. The Conformation of Biological Macromolecules 1985 W. H. Freeman New York
87. A.V. Kyrylyuk, A. Wouterse, and A.P. Philipse Percolation and jamming in random heterogeneous materials with competing length scales Progr. Colloid Polym. Sci. 137 2010 29 33
88. C.R. Cantor, and P.R. Schimmel Biophysical Chemistry. Part II. Techniques for the Study of Biological Structure and Function 1985 W. H. Freeman New York
89. R. Adachi, K. Yamaguchi, H. Yagi, K. Sakurai, H. Naiki, and Y. Goto Flow-induced alignment of amyloid protofilaments revealed by linear dichroism J. Biol. Chem. 282 2007 8978 8983
90. P. Andrews The gel-filtration behaviour of proteins related to their molecular weights over a wide range Biochem. J. 96 1965 595 606
91. Z. Grubisic, P. Rempp, and H. Benoit A universal calibration for gel permeation chromatography J. Polym. Sci. B 5 1967 753 763
92. L.K. Kostanski, D.M. Keller, and A.E. Hamielec Size-exclusion chromatography: a review of calibration methodologies J. Biochem. Biophys. Methods 58 2004 159 186
93. Y. Li, W.F. Weiss, and C.J. Roberts Characterization of high-molecular-weight non-native aggregates and aggregation kinetics by size exclusion chromatography with inline multi-angle laser light scattering J. Pharm. Sci. 98 2009 3997 4016
94. M.P. Tarazona, and E. Saiz Combination of SEC/MALS experimental procedures and theoretical analysis for studying the solution properties of macromolecules J. Biochem. Biophys. Methods 56 2003 95 116
95. J.R. Cann, and D.J. Winzor Frontal gel chromatography of interacting systems: theoretical and experimental evaluation of the shapes of elution profiles for systems of the type A + B reversible C Arch. Biochem. Biophys. 256 1987 78 89
96. Z. Li, Y. Gu, and T. Gu Mathematical modelling and scale-up of size-exclusion chromatography Biochem. Eng. J. 2 1998 145 155
97. H. Kempe, A. Axelsson, B. Nilsson, and G. Zacchi Simulation of chromatographic processes applied to separation of proteins J. Chromatogr. A 846 1999 1 12
98. B. Zelic, and B. Nesek Mathematical modelling of size exclusion chromatography Eng. Life Sci. 6 2006 163 169
99. P.L. Dubin, and J.M. Principi Failure of universal calibration for size exclusion chromatography of rodlike macromolecules versus random coils and globular proteins Macromolecules 22 1989 1891 1896
100. X. Guo, M. Condra, K. Kimura, G. Berth, H. Dautzenberg, and P.L. Dubin Determination of molecular weight of heparin by size exclusion chromatography with universal calibration Anal. Biochem. 312 2003 33 39
101. B.J. Bauer, M.L. Becker, V. Bajpai, J.A. Fagan, E.K. Hobbie, K. Migler, C.M. Guttman, and W.R. Blair Measurement of single-wall nanotube dispersion by size exclusion chromatography J. Phys. Chem. C 111 2007 17914 17918
102. D. Rodbard, and A. Chrambach Unified theory for gel electrophoresis and gel filtration Proc. Natl. Acad. Sci. USA 65 1970 970 977
103. C.J.C. Watts, A. Gray-Weale, and R.G. Gilbert Interpreting size-exclusion data for highly branched biopolymers by reverse Monte Carlo simulations Biomacromolecules 8 2007 455 463
104. L. Hagel, M. Östberg, and T. Andersson Apparent pore size distributions of chromatography media J. Chromatogr. A 743 1996 33 42
105. I. Tatárová, R. Fáber, R. Denoyel, and M. Polakovic Characterization of pore structure of a strong anion-exchange membrane adsorbent under different buffer and salt concentration conditions J. Chromatogr. A 1216 2009 941 947
106. D. Hall, and N. Hirota Multi-scale modelling of amyloid formation from unfolded proteins using a set of theory derived rate constants Biophys. Chem. 140 2008 122 128
107. K. Sasahara, D. Hall, and D. Hamada Effect of lipid type on the binding of lipid vesicles to islet amyloid polypeptide amyloid fibrils Biochemistry 49 2010 3040 3048