Combined affinity and rate constant distributions of ligand populations from experimental surface binding kinetics and equilibria

Biophysical Journal

Volumn 84, Issue 6, 2003, Pages 4062-4077

  Svitel, Juraj ^a   Balbo, Andrea ^a   Mariuzza, Roy A ^b   Gonzales, Noreen R ^c   Schuck, Peter ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIGAND;

ARTICLE; BINDING AFFINITY; BINDING KINETICS; BIOSENSOR; CALCULATION; ENTROPY; LIGAND BINDING; MATHEMATICAL ANALYSIS; POLARIMETRY; PROBLEM SOLVING; PROTEIN TRANSPORT; THERMAL ANALYSIS;

EID: 0038778441     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)75132-7     Document Type: Article

References (91)

1. Abrantes, M., M. T. Magone, L. F. Boyd, and P. Schuck. 2001. Adaptation of the BIAcore X surface plasmon resonance biosensor for use with small sample volumes and long contact times. Anal. Chem. 73:2828-2835.
2. Amato, U., and W. Hughes. 1991. Maximum entropy regularization of Fredholm integral equations of the first kind. Inv. Prob. 7:793-808.
3. Andersen, P. S., P. Schuck, E. J. Sundberg, C. Geisler, K. Karjalainen, and R. A. Mariuzza. 2002. Quantifying the energetics of cooperativity in a ternary protein complex. Biochemistry. 41:5177-5184.
4. Anderson, G. P., M. A. Jacoby, F. S. Ligler, and K. D. King. 1997. Effectiveness of protein A for antibody immobilization for a fiber optic biosensor. Biosens. Bioelectron. 12:329-336.
5. Brochon, J. C. 1994. Maximum entropy method of data analysis in timeresolved spectroscopy. Methods Enzymol. 240:262-311.
6. Cooper, M. A. 2002. Optical biosensors in drug discovery. Nat. Rev. Drug Discov. 1:515-528.
7. Davis, S. J., S. Ikemizu, M. K. Wild, and P. A. van der Merwe. 1998. CD2 and the nature of protein interactions mediating cell-cell recognition. Immunol. Rev. 163:217-236.
8. Fägerstam, L. G., Å. Frostell, R. Karlsson, M. Kullman, A. Larsson, M. Malmqvist, and H. Butt. 1990. Detection of antigen-antibody interactions by surface plasmon resonance. Application to epitope mapping. J. Mol. Recognit. 3:208-214.
9. Freeland, A. C., and R. T. Bonnecaze. 1999. Inference of blood glucose concentrations from subcutaneous glucose concentrations: applications to glucose biosensors. Ann. Biomed. Eng. 27:525-537.
10. Garcia, K. C., C. G. Radu, J. Ho, R. J. Ober, and E. S. Ward. 2001. Kinetics and thermodynamics of T cell receptor-autoantigen interactions in murine experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA. 98:6818-6823.
11. Gilligan, J. J., P. Schuck, and A. L. Yergey. 2002. Mass spectrometry after capture and small-volume elution of analyte from a surface plasmon resonance biosensor. Anal. Chem. 74:2041-2047.
12. Glaser, R. W. 1993. Antigen-antibody binding and mass transport by convection and diffusion to a surface: a two-dimensional computer model of binding and dissociation kinetics. Anal. Biochem. 213:152-161.
13. Glaser, R. W., and G. Hausdorf. 1996. Binding kinetics of an antibody against HIV p24 core protein measured with real-time biomolecular interaction analysis suggest a slow conformational change in antigen p24. J. Immunol. Methods. 189:1-14.
14. Gonzales, N. R., P. Schuck, J. Schlom, and S. V. Kashmiri. 2002. Surface plasmon resonance-based competition assay to assess the sera reactivity of variants of humanized antibodies. J. Immunol. Methods. 268:197-210.
15. Gun'ko, V. M., R. Leboda, V. V. Turov, F. Villieras, J. Skubiszewska-Zieba, S. Chodorowski, and M. Marciniak. 2001. Structural and energetic nonuniformities of pyrocarbon-mineral adsorbents. J. Colloid Interface Sci. 238:340-356.
16. 2+ at Na-montmorillonite: analysis of heterogeneity by means of the regularization technique CONTIN. J. Colloid Interface Sci. 188:377-386.
17. Hall, D. 2001. Use of optical biosensors for the study of mechanistically concerted surface adsorption processes. Anal. Biochem. 288:109-125.
18. Hanisch, F. G., G. Uhlenbruck, H. Egge, and J. Peter-Katalinic. 1989. A B72.3 second-generation-monoclonal antibody (CC49) defines the mucin-carried carbohydrate epitope Gal beta(1-3) [NeuAc alpha(2-6)] GalNAc. Biol. Chem. Hoppe Seyler. 370:21-26.
19. Hansen, P. C. 1998. Rank-Deficient and Discrete III-Posed Problems. SIAM, Philadelphia, Pennsylvania.
20. Hodneland, C. D., Y. S. Lee, D. H. Min, and M. Mrksich. 2002. Selective immobilization of proteins to self-assembled monolayers presenting active site-directed capture ligands. Proc. Natl. Acad. Sci. USA. 99:5048-5052.
21. Jagiello, J. 1994. Stable numerical solution of the adsorption integral equation using splines. Langmuir. 10:2778-2785.
22. Karlsson, R., and A. Fält. 1997. Experimental design for kinetic analysis of protein-protein interactions with surface plasmon resonance biosensors. J. Immunol. Methods. 200:121-133.
23. Karlsson, R., H. Roos, L. Fägerstam, and B. Persson. 1994. Kinetic and concentration analysis using BIA technology. Methods Enzymol. 6: 99-110.
24. Kelley, R. F., and M. P. O'Connell. 1993. Thermodynamic analysis of an antibody functional epitope. Biochemistry. 32:6828-6835.
25. Khilko, S. N., M. T. Jelonek, M. Corr, L. F. Boyd, A. L. M. Bothwell, and D. H. Margulies. 1995. Measuring interactions of MHC class I molecules using surface plasmon resonance. J. Immunol. Methods. 183:77-94.
26. Koopal, L. K., and C. H. W. Vos. 1993. Adsorption on heterogeneous surfaces. Calculation of the adsorption energy distribution function or the affinity spectrum. Langmuir. 9:2593-2605.
27. Lakey, J. H., and E. M. Raggett. 1998. Measuring protein-protein interactions. Curr. Opin. Struct. Biol. 8:119-123.
28. Langmuir, I. 1918. The adsorption of gases on plane surfaces of glass, mica and platinum. J. Am. Chem. Soc. 40:1361-1403.
29. Lawson, C. L., and R. J. Hanson. 1974. Solving Least Squares Problems. Prentice-Hall, Englewood Cliffs, New Jersey.
30. Livesey, A. K., P. Licinio, and M. Delaye. 1986. Maximum entropy analysis of quasielastic light scattering from colloidal dispersions. J. Chem. Phys. 84:5102-5107.
31. Malmborg, A. C., and C. A. Borrebaeck. 1995. BIAcore as a tool in antibody engineering. J. Immunol. Methods. 183:7-13.
32. Mamleev, V. S., and E. A. Bekturov. 1996. Numerical method for analysis of surface heterogeneity in a case of finite diversity of adsorption sites. Langmuir. 12:3630-3642.
33. McDermott, B. M., Jr., A. H. Rux, R. J. Eisenberg, G. H. Cohen, and V. R. Racaniello. 2000. Two distinct binding affinities of poliovirus for its cellular receptor. J. Biol. Chem. 275:23089-23096.
34. Muraro, R., M. Kuroki, D. Wunderlich, D. J. Poole, D. Colcher, A. Thor, J. W. Greiner, J. F. Simpson, A. Molinolo, P. Noguchi, and J. Schlom. 1988. Generation and characterization of B72.3 second generation monoclonal antibodies reactive with the tumor-associated glycoprotein 72 antigen. Cancer Res. 48:4588-4596.
35. Myszka, D. G., X. He, M. Dembo, T. A. Morton, and B. Goldstein. 1998. Extending the range of rate constants available from BIACORE: interpreting mass transport influenced binding data. Biophys. J. 75: 583-594.
36. Myszka, D. G., R. W. Sweet, P. Hensley, M. Brigham-Burke, P. D. Kwong, W. A. Hendrickson, R. Wyatt, J. Sodroski, and M. L. Doyle. 2000. Energetics of the HIV gp120-CD4 binding reaction. Proc. Natl. Acad. Sci. USA. 97:9026-9031.
37. Narang, U., G. P. Anderson, F. S. Ligler, and J. Burans. 1997. Fiber optic-based biosensor for ricin. Biosens. Bioelectron. 12:937-945.
38. Natarajan, K., L. F. Boyd, P. Schuck, W. M. Yokoyama, D. Eliat, and D. H. Margulies. 1999. Interaction of the NK cell inhibitory receptor Ly49A with H-2Dd: identification of a site distinct from the TCR site. Immunity. 11:591-601.
39. Natsume, T., H. Nakayama, O. Jansson, T, Isobe, K. Takio, and K. Mikoshiba. 2000. Combination of biomolecular interaction analysis and mass spectrometric amino acid sequencing. Anal. Chem. 72:4193-4198.
40. Nedelkov, D., and R. W. Nelson. 2000. Practical considerations in BIA/ MS: optimizing the biosensor-mass spectrometry interface. J. Mol. Recog. 13:140-145.
41. Nieba, L., A. Krebber, and A. Pluckthun. 1996. Competition BIAcore for measuring true affinities: large differences from values determined from binding kinetics. Anal. Biochem. 234:155-165.
42. Nisonoff, A., and D. Pressman. 1958. Heterogeneity and average combining constants of antibodies from individual rabbits. J. Immunol. 80: 417-428.
43. O'Shannessy, D. J. 1994. Determination of kinetic rate and equilibrium binding constants for macromolecular interactions: a critique of the surface plasmon resonance literature. Curr. Opin. Biotechnol. 5:65-71.
44. O'Shannessy, D. J., and D. J. Winzor. 1996. Interpretation of deviations from pseudo-first-order kinetic behavior in the characterization of ligand binding by biosensor technology. Anal. Biochem. 236:275-283.
45. Ober, R. J., C. G. Radu, V. Ghetie, and E. S. Ward. 2001. Differences in promiscuity for antibody-FcRn interactions across species: implications for therapeutic antibodies. Int. Immunol. 13:1551-1559.
46. Ober, R. J., and E. S. Ward. 1999. The choice of reference cell in the analysis of kinetic data using BIAcore. Anal. Biochem. 271:70-80.
47. Ober, R. J., and E. S. Ward. 2002. Compensation for loss of ligand activity in surface plasmon resonance experiments. Anal. Biochem. 306:228-236.
48. Phillips, D. L. 1962. A technique for the numerical solution of certain integral equations of the first kind. J. Ass. Comp. Mach. 9:84-97.
49. Piehler, J., A. Brecht, K. Hehl, and G. Gauglitz. 1999. Protein interactions in covalently attached dextran layers. Colloids Surf. B Biointerface. 13:325-336.
50. Poland, D. 2001a. Enthalpy distributions in proteins. Biopolymers. 58: 89-105.
51. Poland, D. 2001b. Ligand binding distributions in nucleic acids. Biopolymers. 58:477-490.
52. Press, W. H., S. A. Teukolsky, W. T. Vetterling, and B. P. Flannery. 1992. Numerical Recipes in C. University Press, Cambridge.
53. Provencher, S. W. 1979. Inverse problems in polymer characterization: direct analysis of polydispersity with photon correlation spectroscopy. Macromol. Chem. 180:201-209.
54. Provencher, S. W. 1982a. A constrained regularization method for inverting data represented by linear algebraic or integral equations. Comp. Phys. Comm. 27:213-227.
55. Provencher, S. W. 1982b. CONTIN: A general purpose constrained regularization program for inverting noisy linear algebraic and integral equations. Comp. Phys. Comm. 27:229-242.
56. Provencher, S. W. 1992. Low-bias macroscopic analysis of polydispersity. In Laser Light Scattering in Biochemistry. S. E. Harding, D. B. Satelle, and V. A. Bloomfield, editors. The Royal Society of Chemistry, Cambridge, UK. pp. 92-111.
57. Puziy, A. M. 1999. Use of CONTIN for calculation of adsorption energy distributions. Langmuir. 15:6016-6025.
58. Rabbany, S. Y., R. Piervincenzi, L. Judd, A. W. Kusterbeck, R. Bredehorst, K. Hakansson, and F. S. Ligler. 1997. Assessment of heterogeneity in antibody-antigen displacement reactions. Anal. Chem. 69:175-182.
59. Rebois, R. V., P. Schuck, and J. K. Northup. 2002. Elucidating kinetic and thermodynamic constants for interaction of G protein subunits and receptors by surface plasmon resonance spectroscopy. Methods Enzymol. 344:15-42.
60. Reddish, M. A., L. Jackson, R. R. Koganty, D. Qiu, W. Hong, and B. M. Longenecker. 1997. Specificities of anti-sialyl-Tn and anti-Tn monoclonal antibodies generated using novel clustered synthetic glycopeptide epitopes. Glycoconj. J. 14:549-560.
61. Rich, R. L., and D. G. Myszka. 2001. Survey of the year 2000 commercial optical biosensor literature. J. Mol. Recognit. 14:273-294.
62. Roden, L. D., and D. G. Myszka. 1996. Global analysis of a macromolecular interaction measured on BIAcore. Biochem. Biophys. Res. Commun. 225:1073-1077.
63. Rudolph, M. G., J. G. Luz, and I. A. Wilson. 2002. Structural and thermodynamic correlates of T-cell signaling. Annu. Rev. Biophys. Biomol. Struct. 31:121-149.
64. Rusch, U., M. Borkovec, J. Daicic, and W. H. van Riemsdijk. 1997. Interpretation of competitive adsorption isotherms in terms of affinity distributions. J. Colloid Interface Sci. 191:247-255.
65. Schuck, P. 1996. Kinetics of ligand binding to receptor immobilized in a polymer matrix, as detected with an evanescent wave biosensor. I. A computer simulation of the influence of mass transport. Biophys. J. 70: 1230-1249.
66. Schuck, P. 1997a. Reliable determination of binding affinity and kinetics using surface plasmon resonance biosensors. Curr. Opin. Biotechnol. 8:498-502.
67. Schuck, P. 1997b. Use of surface plasmon resonance to probe the equilibrium and dynamic aspects of interactions between biological macromolecules. Annu. Rev. Biophys. Biomol. Struct. 26:541-566.
68. Schuck, P. 2000. Size distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys. J. 78:1606-1619.
69. Schuck, P., L. F. Boyd, and P. S. Andersen. 1999. Measuring protein interactions by optical biosensors. In Current Protocols in Protein Science. J. E. Coligan, B. M. Dunn, H. L. Ploegh, D. W. Speicher, and P. T. Wingfield, editors. John Wiley & Sons, New York. pp. 20.2.1-20.2. 21.
70. Schuck, P., D. B. Millar, and A. A. Kortt. 1998. Determination of binding constants by equilibrium titration with circulating sample in a surface plasmon resonance biosensor. Anal. Biochem. 265:79-91.
71. Schuck, P., and A. P. Minton. 1996a. Analysis of mass transport limited binding kinetics in evanescent wave biosensors. Anal. Biochem. 240:262-272.
72. Schuck, P., and A. P. Minton. 1996b. Minimal requirements for internal consistency of the analysis of surface plasmon resonance biosensor data. Trends Biochem. Sci. 252:458-460.
73. Schuck, P., M. A. Perugini, N. R. Gonzales, G. J. Howlett, and D. Schubert. 2002. Size-distribution analysis of proteins by analytical ultracentrifugation: strategies and application to model systems. Biophys. J. 82:1096-1111.
74. Selinger, J. V., and S. Y. Rabbany. 1997. Theory of heterogeneity in displacement reactions. Anal. Chem. 69:170-174.
75. Sips, R. 1948. On the structure of a catalyst surface. J. Chem. Phys. 16:490-495.
76. Smith, C. R., and W. T. Grandy. 1985. Maximum-Entropy and Bayesian Methods in Inverse Problems. Reidel, Dordrecht, The Netherlands.
77. Stanley, B. J., K. Topper, and D. B. Marshall. 1994. Analysis of the heterogeneous rate of dissociation of Cu(II) from humic and fulvic acids by statistical deconvolution. Anal. Chim. Acta. 287:25-34.
78. Steinbach, P. J. 1996. Two-dimensional distributions of activation enthalpy and entropy from kinetics by the maximum entropy method. Biophys. J. 70:1521-1528.
79. Steinbach, P. J., R. Ionescu, and C. R. Matthews. 2002. Analysis of kinetics using a hybrid maximum-entropy/nonlinear-least-squares method: application to protein folding. Biophys. J. 82:2244-2255.
80. Sundberg, E. J., and R. A. Mariuzza. 2002. Molecular recognition in antigen-antibody complexes. Adv. Protein Chem. 61:119-160.
81. van der Heide, U. A., S. C. Hopkins, and Y. E. Goldman. 2000. A maximum entropy analysis of protein orientations using fluorescence polarization data from multiple probes. Biophys. J. 78:2138-2150.
82. van der Merwe, P. A., and A. N. Barclay. 1996. Analysis of cell-adhesion molecule interactions using surface plasmon resonance. Curr. Opin. Immunol. 8:257-261.
83. van der Merwe, P. A., A. N. Barclay, D. W. Mason, E. A. Davies, B. P. Morgan, M. Tone, A. K. C. Krishnam, C. Ianelli, and S. J. Davis. 1994. Human cell-adhesion molecule CD2 binds CD58 (LFA-3) with a very low affinity and an extremely fast dissociation rate but does not bind CD48 or CD59. Biochemistry. 33:10149-10160.
84. Vijayendran, R. A., and D. E. Leckband. 2001. A quantitative assessment of heterogeneity for surface-immobilized proteins. Anal. Chem. 73: 471-480.
85. Vijayendran, R. A., F. S. Ligler, and D. E. Leckband. 1999. A computational reaction-diffusion model for the analysis of transport limited kinetics. Anal. Chem. 71:5405-5412.
86. Ward, E. S., D. Gussow, A. D. Griffiths, P. T. Jones, and G. Winter. 1989. Binding activities of a repertoire of single immunoglobulin variable domains secreted from Escherichia coli. Nature. 341:544-546.
87. Williams, C., and T. A. Addona. 2000. The integration of SPR biosensors with mass spectrometry: possible applications for proteome analysis. Trends Biotechnol. 18:45-48.
88. Wofsy, C., and B. Goldstein. 2002. Effective rate models for receptors distributed in a layer above a surface: application to cells and Biacore. Biophys. J. 82:1743-1755.
89. Xing, L., K. Tjarnlund, B. Lindqvist, G. G. Kaplan, D. Feigelstock, R. H. Cheng, and J. M. Casasnovas. 2000. Distinct cellular receptor interactions in poliovirus and rhinoviruses. EMBO J. 19: 1207-1216.
90. Yarmush, M. L., D. B. Patankar, and D. M. Yarmush. 1996. An analysis of transport resistances in the operation of BIAcore; implications for kinetic studies of biospecific interactions. Mol. Immunol. 33:1203-1214.
91. Zacher, T., and E. Wischerhoff. 2002. Real-time two-wavelength surface plasmon resonance as a tool for the vertical resolution of binding processes in biosensing hydrogels. Langmuir. 18:1748-1759.