Analytical ultracentrifugation as a tool for studying protein interactions

Biophysical Reviews

Volumn 5, Issue 2, 2013, Pages 159-171

  Schuck, Peter ^a  

^a NATIONAL INSTITUTE OF BIOMEDICAL IMAGING AND BIOENGINEERING   (United States)

Author keywords

Effective particle theory; Global analysis; Multi protein complexes; Multi signal analysis; Sedimentation equilibrium; Sedimentation velocity

Indexed keywords

EID: 84877044364     PISSN: 18672450     EISSN: 18672469     Source Type: Journal    
DOI: 10.1007/s12551-013-0106-2     Document Type: Review

References (91)

1. Alami M, Dalal K, Lelj-Garolla B, Sligar SG, Duong F (2007) Nanodiscs unravel the interaction between the SecYEG channel and its cytosolic partner SecA. EMBO J 26(8): 1995-2004. doi: 10. 1038/sj. emboj. 7601661.
2. Ang S, Rowe AJ (2010) Evaluation of the information content of sedimentation equilibrium data in self-interacting systems. Macromol Biosci 10(7): 798-807. doi: 10. 1002/mabi. 201000065.
3. Aragon SR (2011) Recent advances in macromolecular hydrodynamic modeling. Methods 54(1): 101-114. doi: 10. 1016/j. ymeth. 2010. 10. 005.
4. Balbo A, Minor KH, Velikovsky CA, Mariuzza R, Peterson CB, Schuck P (2005) Studying multi-protein complexes by multi-signal sedimentation velocity analytical ultracentrifugation. Proc Natl Acad Sci USA 102: 81-86.
5. Balbo A, Brown P, Braswell E, Schuck P (2007) Measuring protein-protein interactions by equilibrium sedimentation. Curr Protoc Immunol 18: 18. 8.
6. Brautigam CA (2011) Using Lamm-Equation modeling of sedimentation velocity data to determine the kinetic and thermodynamic properties of macromolecular interactions. Methods 54(1): 4-15. doi: 10. 1016/j. ymeth. 2010. 12. 029.
7. Brookes E, Cao W, Demeler B (2010) A two-dimensional spectrum analysis for sedimentation velocity experiments of mixtures with heterogeneity in molecular weight and shape. Eur Biophys J 39(3): 405-414. doi: 10. 1007/s00249-009-0413-5.
8. Brown PH, Schuck P (2006) Macromolecular size-and-shape distributions by sedimentation velocity analytical ultracentrifugation. Biophys J 90(12): 4651-4661. doi: 10. 1529/biophysj. 106. 081372.
9. Brown PH, Schuck P (2007) A new adaptive grid-size algorithm for the simulation of sedimentation velocity profiles in analytical ultracentrifugation. Comput Phys Commun 178: 105-120.
10. Brown PH, Balbo A, Schuck P (2007) Using prior knowledge in the determination of macromolecular size-distributions by analytical ultracentrifugation. Biomacromolecules 8: 2011-2024.
11. Brown PH, Balbo A, Schuck P (2008) Characterizing protein-protein interactions by sedimentation velocity analytical ultracentrifugation. Curr Protoc Immunol 18: 18. 15.
12. Brown PH, Balbo A, Schuck P (2009) On the analysis of sedimentation velocity in the study of protein complexes. Eur Biophys J 38: 1079-1099.
13. Brown PH, Balbo A, Zhao H, Ebel C, Schuck P (2011) Density contrast sedimentation velocity for the determination of protein partial-specific volumes. PLoS One 6(10): e26221. doi: 10. 1371/journal. pone. 0026221.
14. Cann JR (1986) Effects of microheterogeneity on sedimentation patterns of interacting proteins and the sedimentation behavior of systems involving two ligands. Methods Enzymol 130(1964): 19-35. doi: 10. 1016/0076-6879(86)30005-3.
15. Cann JR (1994) Computer simulation of the sedimentation of ligand-mediated and kinetically controlled macromolecular interactions. In: Schuster TM, Laue TM (eds) Modern analytical ultracentrifugation. Birkhauser, Boston, pp 171-188.
16. Chaudhry C, Weston MC, Schuck P, Rosenmund C, Mayer ML (2009) Stability of ligand-binding domain dimer assembly controls kainate receptor desensitization. EMBO J 28(10): 1518-1530. doi: 10. 1038/emboj. 2009. 86.
17. Chou CY, Jen WP, Hsieh YH, Shiao MS, Chang GG (2006) Structural and functional variations in human apolipoprotein E3 and E4. J Biol Chem 281(19): 13333-13344.
18. Claverie JMJ-M, Dreux H, Cohen R (1975) Sedimentation of generalized systems of interacting particles. I. Solution of systems of complete Lamm equations. Biopolymers 14(8): 1685-1700. doi: 10. 1002/bip. 1975. 360140811.
19. Correia JJ, Stafford WF (2009) Extracting equilibrium constants from kinetically limited reacting systems. Methods Enzymol 455: 419-446.
20. Cox DJ (1965) Computer simulation of sedimentation in the ultracentrifuge I. Diffus Arch Biochem Biophys 112(2): 249-258. doi: 10. 1016/0003-9861(65)90043-3.
21. Dam J, Schuck P (2004) Calculating sedimentation coefficient distributions by direct modeling of sedimentation velocity concentration profiles. Methods Enzymol 384(301): 185-212. doi: 10. 1016/S0076-6879(04)84012-6.
22. Dam J, Velikovsky CA, Mariuzza R, Urbanke C, Schuck P (2005) Sedimentation velocity analysis of protein-protein interactions: lamm equation modeling and sedimentation coefficient distributions c(s). Biophys J 89: 619-634. doi: doi: 10. 1529/biophysj. 105. 059568.
23. Dam J, Baber J, Grishaev A, Malchiodi EL, Schuck P, Bax A, Mariuzza RA (2006) Variable dimerization of the Ly49A natural killer cell receptor results in differential engagement of its MHC class I ligand. J Mol Biol 362(1): 102-113.
24. Darawshe S, Minton AP (1994) Quantitative characterization of macromolecular associations in solution via real-time and postcentrifugation measurements of sedimentation equilibrium: a comparison. Anal Biochem 220: 1-4.
25. Demeler B, van Holde KE (2004) Sedimentation velocity analysis of highly heterogeneous systems. Anal Biochem 335(2): 279-288. doi: 10. 1016/j. ab. 2004. 08. 039.
26. Demeler B, Behlke J, Ristau O (2000) Molecular parameters from sedimentation velocity experiments: whole boundary fitting using approximate and numerical solutions of Lamm equation. Methods Enzymol 321(1998): 38-66. doi: 10. 1016/S0076-6879(00)21186-5.
27. Dishon M, Weiss GHH, Yphantis DAA (1966) Numerical solutions of the Lamm equation. I. Numerical procedure. Biopolymers 4(4): 449-455. doi: 10. 1002/bip. 1966. 360040406.
28. Ebel C (2011) Sedimentation velocity to characterize surfactants and solubilized membrane proteins. Methods 54(1): 56-66. doi: 10. 1016/j. ymeth. 2010. 11. 003.
29. Fujita H (1975) Foundations of ultracentrifugal analysis. John Wiley & Sons, New York.
30. Gabrielson JP, Arthur KK (2011) Measuring low levels of protein aggregation by sedimentation velocity. Methods 54(1): 83-91. doi: 10. 1016/j. ymeth. 2010. 12. 030.
31. García De La Torre J, Huertas ML, Carrasco B (2000) Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. Biophys J 78(2): 719-730. doi: 10. 1016/S0006-3495(00)76630-6.
32. Ghirlando R (2011) The analysis of macromolecular interactions by sedimentation equilibrium. Methods 54(1): 145-156. doi: 10. 1016/j. ymeth. 2010. 12. 005.
33. Gilbert GA, Gilbert LM (1980a) Ultracentrifuge studies of interactions and equilibria: impact of interactive computer modelling. Biochem Soc Trans 8: 520-522. doi: 10. 1042/bst0080520.
34. Gilbert GA, Gilbert LM (1980b) Detection in the ultracentrifuge of protein heterogeneity by computer modelling, illustrated by pyruvate dehydrogenase multienzyme complex. J Mol Biol 144(3): 405-408. doi: 10. 1016/0022-2836(80)90099-6.
35. Gilbert GA, Jenkins RC (1956) Boundary problems in the sedimentation and electrophoresis of complex systems in rapid reversible equilibrium. Nature 177: 853-854.
36. Goldberg JR (1953) Sedimentation in the ultracentrifuge. J Phys Chem 57: 194-202. doi: 10. 1021/j150503a014.
37. González JM, Rivas G, Minton AP (2003) Effect of large refractive index gradients on the performance of absorption optics in the Beckman XL-A/I analytical ultracentrifuge: an experimental study. Anal Biochem 313(1): 133-136.
38. Hall D, Minton AP (2003) Macromolecular crowding: qualitative and semiquantitative successes, quantitative challenges. Biochem Biophys Acta 1649(2): 127-139. doi: 10. 1016/S1570-9639(03)00167-5.
39. Harding SE, Schuck P, Abdelhameed AS, Adams G, Kök MS, Morris GA (2011) Extended Fujita approach to the molecular weight distribution of polysaccharides and other polymeric systems. Methods 54(1): 136-144. doi: 10. 1016/j. ymeth. 2011. 01. 009.
40. Hernández-Rocamora VM, Reija B, García C, Natale P, Alfonso C, Minton AP, Zorrilla S et al (2012) Dynamic interaction of the Escherichia coli cell division ZipA and FtsZ proteins evidenced in nanodiscs. J Biol Chem 287(36): 30097-30104. doi: 10. 1074/jbc. M112. 388959.
41. Holladay LAA (1979) An approximate solution to the Lamm equation. Biophys Chem 10(2): 187-190. doi: 10. 1016/0301-4622(79)85039-5.
42. Hsu CS, Minton AP (1991) A strategy for efficient characterization of macromolecular heteroassociations via measurement of sedimentation equilibrium. J Mol Recognit 4(2-3): 93-104. doi: 10. 1002/jmr. 300040208.
43. Inagaki S, Ghirlando R, Grisshammer R (2012) Biophysical characterization of membrane proteins in nanodiscs. Methods. doi: 10. 1016/j. ymeth. 2012. 11. 006.
44. Lamm O (1929) Die differentialgleichung der ultrazentrifugierung. Ark Mat Astr Fys 21B(2): 1-4.
45. Lebowitz J, Lewis MS, Schuck P (2002) Modern analytical ultracentrifugation in protein science: a tutorial review. Protein Sci 11(9): 2067-2079.
46. Lewis MS, Shrager RI, Kim S-J (1993) Analysis of protein-nucleic acid and protein-protein interactions using multi-wavelength scans from the XL-A analytical ultracentrifuge. In: Schuster TM, Laue TM (eds) Modern analytical ultracentrifugation. Birkhäuser, Boston, pp 94-115.
47. Minton AP (1998) Molecular crowding: analysis of effects of high concentrations of inert cosolutes on biochemical equilibria and rates in terms of volume exclusion. Method Enzymol 295: 127-149.
48. Noy D, Discher BM, Rubtsov IV, Hochstrasser RM, Dutton PL (2005) Design of amphiphilic protein maquettes: enhancing maquette functionality through binding of extremely hydrophobic cofactors to lipophilic domains. Biochemistry 44(37): 12344-12354.
49. Padrick SB, Brautigam CA (2011) Evaluating the stoichiometry of macromolecular complexes using multisignal sedimentation velocity. Methods 54(1): 39-55. doi: 10. 1016/j. ymeth. 2011. 01. 002.
50. Padrick SB, Deka RK, Chuang JL, Wynn RM, Chuang DT, Norgard MV, Rosen MK et al (2010) Determination of protein complex stoichiometry through multisignal sedimentation velocity experiments. Anal Biochem 407(1): 89-103.
51. Patel TR, Harding SE, Ebringerova A, Deszczynski M, Hromadkova Z, Togola A, Paulsen BS et al (2007) Weak self-association in a carbohydrate system. Biophys J 93(3): 741-749.
52. Philo JS (1996) An improved function for fitting sedimentation velocity data for low-molecular-weight solutes. Biophys J 72(January): 435-444.
53. Philo JS (2000) Sedimentation equilibrium analysis of mixed associations using numerical constraints to impose mass or signal conservation. Method Enzymol 321: 100-120. doi: 10. 1124/mol. 109. 056598.
54. Rivas G, Minton AP (2011) Beyond the second virial coefficient: sedimentation equilibrium in highly non-ideal solutions. Methods 54(1): 167-174. doi: 10. 1016/j. ymeth. 2010. 11. 004.
55. Rivas G, Fernandez JAA, Minton AP (1999) Direct observation of the self-association of dilute proteins in the presence of inert macromolecules at high concentration via tracer sedimentation equilibrium: theory, experiment, and biological significance. Biochemistry 38(29): 9379-9388. doi: 10. 1021/bi990355z.
56. Rivas G, Fernández JA, Minton AP (2001) Direct observation of the enhancement of noncooperative protein self-assembly by macromolecular crowding: indefinite linear self-association of bacterial cell division protein FtsZ. Proc Natl Acad Sci USA 98(6): 3150-3155. doi: 10. 1073/pnas. 051634398.
57. Rowe AJ (2005) Weak interactions: Optimal algorithms for their study in the AUC. In: Scott DJ, Harding SE, Rowe AJ (eds) Analytical ultracentrifugation. Techniques and methods. RSC Publishing, Cambridge, pp 484-500.
58. Rowe AJ (2011) Ultra-weak reversible protein-protein interactions. Methods 54(1): 157-166. doi: 10. 1016/j. ymeth. 2011. 02. 006.
59. Schachman HK (1959) Ultracentrifugation in biochemistry. Academic, New York.
60. Schachman HK (1989) Analytical ultracentrifugation reborn. Nature 341(21): 259-260.
61. Schuck P (1994) Simultaneous radial and wavelength analysis with the Optima XL-A analytical ultracentrifuge. Progr Colloid Polym Sci 94: 1-13.
62. Schuck P (1998) Sedimentation analysis of noninteracting and self-associating solutes using numerical solutions to the Lamm equation. Biophys J 75(3): 1503-1512. doi: 10. 1016/S0006-3495(98)74069-X.
63. Schuck P (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J 78(3): 1606-1619. doi: 10. 1016/S0006-3495(00)76713-0.
64. Schuck P (2003) On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation. Anal Biochem 320: 104-124. doi: 10. 1016/S0003-2697(03)00289-6.
65. Schuck P (2004a) A model for sedimentation in inhomogeneous media. I. Dynamic density gradients from sedimenting co-solutes. Biophys Chem 108: 187-200.
66. Schuck P (2004b) A model for sedimentation in inhomogeneous media. II. Compressibility of aqueous and organic solvents. Biophys Chem 187: 201-214.
67. Schuck P (2009) On computational approaches for size-and-shape distributions from sedimentation velocity analytical ultracentrifugation. Eur Biophys J 39: 1261-1275.
68. Schuck P (2010a) Some statistical properties of differencing schemes for baseline correction of sedimentation velocity data. Anal Biochem 401(2): 280-287.
69. Schuck P (2010b) Sedimentation patterns of rapidly reversible protein interactions. Biophys J 98(9): 2005-2013.
70. Schuck P (2010c) Diffusion of the reaction boundary of rapidly interacting macromolecules in sedimentation velocity. Biophys J 98(11): 2741-2751. doi: 10. 1016/j. bpj. 2010. 03. 004.
71. Schuck P, Demeler B (1999) Direct sedimentation analysis of interference optical data in analytical ultracentrifugation. Biophys J 76: 2288-2296.
72. Schuck P, Rossmanith P (2000) Determination of the sedimentation coefficient distribution by least-squares boundary modeling. Biopolymers 54: 328-341.
73. Schuck P, MacPhee CE, Howlett GJ (1998) Determination of sedimentation coefficients for small peptides. Biophys J 74: 466-474.
74. Schuck P, Taraporewala ZF, McPhie P, Patton JT (2001) Rotavirus nonstructural protein NSP2 self-assembles into octamers that undergo ligand-induced conformational changes. J Biol Chem 276(13): 9679-9687. doi: 10. 1074/jbc. M009398200.
75. Schuck P, Perugini MAA, Gonzales NRR, Howlett GJJ, Schubert D (2002) Size-distribution analysis of proteins by analytical ultracentrifugation: strategies and application to model systems. Biophys J 82(2): 1096-1111. doi: 10. 1016/S0006-3495(02)75469-6.
76. Schuck P, Balbo A, Brown PH, Zhao H (2010) Analytical ultracentrifugation. In: Meyers RA (ed) Encyclopedia of analytical chemistry. John Wiley, Chichester, pp 21-52. doi: 10. 1002/9780470027318. a9091.
77. Stafford WF (1992) Boundary analysis in sedimentation transport experiments: a procedure for obtaining sedimentation coefficient distributions using the time derivative of the concentration profile. Anal Biochem 203: 295-301.
78. Stafford WF, Sherwood PJ (2004) Analysis of heterologous interacting systems by sedimentation velocity: curve fitting algorithms for estimation of sedimentation coefficients, equilibrium and kinetic constants. Biophys Chem 108(1-3): 231-243. doi: 10. 1016/j. bpc. 2003. 10. 028.
79. Svedberg T, Pedersen KO (1940) The ultracentrifuge. Oxford University Press, London.
80. Tanford C, Reynolds JAA (1976) Characterization of membrane proteins in detergent solutions. Biochim Biophys Acta 457(2): 133-170. doi: 10. 1016/0304-4157(76)90009-5.
81. Urbanke C, Ziegler B, Stieglitz K (1980) Complete evaluation of sedimentation velocity experiments in the analytical ultracentrifuge. Fresenius Z Anal Chem 301: 139-140.
82. Vistica J, Dam J, Balbo A, Yikilmaz E, Mariuzza RA, Rouault TA, Schuck P (2004) Sedimentation equilibrium analysis of protein interactions with global implicit mass conservation constraints and systematic noise decomposition. Anal Biochem 326: 234-256. doi: 10. 1016/j. ab. 2003. 12. 014.
83. Wills PR, Scott DJ, Winzor DJ (2012) Allowance for effects of thermodynamic nonideality in sedimentation equilibrium distributions reflecting protein dimerization. Anal Biochem 422(1): 28-32. doi: 10. 1016/j. ab. 2011. 12. 010.
84. Zhao H, Schuck P (2012) Global multi-method analysis of affinities and cooperativity in complex systems of macromolecular interactions. Anal Chem 84: 9513-9519. doi: 10. 1021/ac302357w.
85. Zhao H, Brown PH, Balbo A, Fernandez Alonso MC, Polishchuck N, Chaudhry C, Mayer ML et al (2010) Accounting for solvent signal offsets in the analysis of interferometric sedimentation velocity data. Macromol Biosci 10: 736-745.
86. Zhao H, Balbo A, Brown PH, Schuck P (2011) The boundary structure in the analysis of reversibly interacting systems by sedimentation velocity. Methods 54(1): 16-30. doi: 10. 1016/j. ymeth. 2011. 01. 010.
87. Zhao H, Berger AJ, Brown PH, Kumar J, Balbo A, May CA, Casillas E et al (2012) Analysis of high-affinity assembly for AMPA receptor amino-terminal domains. J Gen Physiol 139: 371-388. doi: 10. 1085/jgp. 201210770.
88. Zhao H, Brautigam CA, Ghirlando R, Schuck P (2013) Current methods in sedimentation velocity and sedimentation equilibrium analytical ultracentrifugation. Curr Protoc Protein Sci 7: 20. 12. 1.
89. Zhi L, Mans J, Paskow MJ, Brown PH, Schuck P, Jonjić S, Natarajan K et al (2010) Direct interaction of the mouse cytomegalovirus m152/gp40 immunoevasin with RAE-1 isoforms. Biochemistry 49(11): 2443-2453. doi: 10. 1021/bi902130j.
90. Zhou HX, Rivas G, Minton AP (2008) Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences. Annu Rev Biophys 37: 375-397. doi: 10. 1146/annurev. biophys. 37. 032807. 125817.
91. Zimmerman SB, Minton AP (1993) Macromolecular crowding: biochemical, biophysical, and physiological consequences. Annu Rev Biophys Biomol Struct 22: 27-65. doi: 10. 1146/annurev. bb. 22. 060193. 000331.