Modeling bispecific monoclonal antibody interaction with two cell membrane targets indicates the importance of surface diffusion

mAbs

Volumn 8, Issue 5, 2016, Pages 905-915

  Sengers, Bram G ^a   McGinty, Sean ^b   Nouri, Fatma Z ^c   Argungu, Maryam ^d   Hawkins, Emma ^e   Hadji, Aymen ^c   Weber, Andrew ^f   Taylor, Adam ^g   Sepp, Armin ^g  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c BADJI MOKHTAR UNIVERSITY   (Algeria)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF SURREY   (United Kingdom)

^f GLAXOSMITHKLINE   (United States)

^g GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Affinity; avidity; bispecific antibody; diffusion; modeling; Monte Carlo; simulation; specificity; therapeutic

Indexed keywords

CD4 ANTIGEN; CD70 ANTIGEN; MONOCLONAL ANTIBODY; BISPECIFIC ANTIBODY;

ARTICLE; BINDING AFFINITY; CELL MEMBRANE; CONCEPTUAL FRAMEWORK; DIFFUSION; ENZYME LINKED IMMUNOSORBENT ASSAY; EQUILIBRIUM DIALYSIS; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; KINETICS; MATHEMATICAL ANALYSIS; MONTE CARLO METHOD; OLIGOMERIZATION; PROTEIN INTERACTION; ANIMAL; ANTIBODY AFFINITY; HUMAN; IMMUNOLOGY; THEORETICAL MODEL;

ANIMALS; ANTIBODIES, BISPECIFIC; ANTIBODIES, MONOCLONAL; ANTIBODY AFFINITY; DIFFUSION; HUMANS; MODELS, THEORETICAL; MONTE CARLO METHOD;

EID: 84969820388     PISSN: 19420862     EISSN: 19420870     Source Type: Journal    
DOI: 10.1080/19420862.2016.1178437     Document Type: Article

References (45)

1. R.E.Kontermann. Dual targeting strategies with bispecific antibodies. MAbs 2012; 4:182-97; PMID:22453100; http://dx.doi.org/10.4161/mabs.4.2.19000
2. K.Garber. Bispecific antibodies rise again. Nat Rev Drug Discov 2014; 13:799-801; PMID:25359367; http://dx.doi.org/10.1038/nrd4478
3. C.Grandjenette, M.Dicato, M.Diederich. Bispecific antibodies: an innovative arsenal to hunt, grab and destroy cancer cells. Curr Pharm Biotechnol 2015; 16:670-83; PMID:25941884; http://dx.doi.org/10.2174/1389201016666150505124037
4. C.Spiess, Q.Zhai, P.J.Carter. Alternative molecular formats and therapeutic applications for bispecific antibodies. Mol Immunol 2015; 67:95-106; PMID:25637431; http://dx.doi.org/10.1016/j.molimm.2015.01.003
5. Y.Mazor, V.Oganesyan, C.Yang, A.Hansen, J.Wang, H.Liu, K.Sachsenmeier, M.Carlson, D.V.Gadre, M.J.Borrok, et al. Improving target cell specificity using a novel monovalent bispecific IgG design. mAbs 2015; 7:377-89; PMID:25621507; http://dx.doi.org/10.1080/19420862.2015.1007816
6. Y.Mazor, A.Hansen, C.Yang, P.S.Chowdhury, J.Wang, G.Stephens, H.Wu, W.F.Dall'Acqua. Insights into the molecular basis of a bispecific antibody's target selectivity. mAbs 2015; 7:461-9; PMID:25730144; http://dx.doi.org/10.1080/19420862.2015.1022695
7. J.B.Ridgway, L.G.Presta, P.Carter. 'Knobs-into-holes' engineering of antibody CH3 domains for heavy chain heterodimerization. Protein Eng 1996; 9:617-21; PMID:8844834; http://dx.doi.org/10.1093/protein/9.7.617
8. N.Fischer, G.Elson, G.Magistrelli, E.Dheilly, N.Fouque, A.Laurendon, F.Gueneau, U.Ravn, J.F.Depoisier, V.Moine, et al. Exploiting light chains for the scalable generation and platform purification of native human bispecific IgG. Nat Commun 2015; 6:6113; PMID:25672245; http://dx.doi.org/10.1038/ncomms7113
9. C.Klein, C.Sustmann, M.Thomas, K.Stubenrauch, R.Croasdale, J.Schanzer, U.Brinkmann, H.Kettenberger, J.T.Regula, W.Schaefer. Progress in overcoming the chain association issue in bispecific heterodimeric IgG antibodies. mAbs 2012; 4:653-63; PMID:22925968; http://dx.doi.org/10.4161/mabs.21379
10. M.A.McCloskey, M.M.Poo. Rates of membrane-associated reactions: reduction of dimensionality revisited. J Cell Biol 1986; 102:88-96; PMID:3001105; http://dx.doi.org/10.1083/jcb.102.1.88
11. T.Kihara, J.Ito, J.Miyake. Measurement of Biomolecular Diffusion in Extracellular Matrix Condensed by Fibroblasts Using Fluorescence Correlation Spectroscopy. PLoS One 2013; 8:e82382; PMID:24312418; http://dx.doi.org/10.1371/journal.pone.0082382
12. A.Einstein. Investigations on the theory of the brownian movement. Dover Publications, 1956.
13. M.Gavutis, E.Jaks, P.Lamken, J.Piehler. Determination of the two-dimensional interaction rate constants of a cytokine receptor complex. Biophys J 2006; 90:3345-55; PMID:16473899; http://dx.doi.org/10.1529/biophysj.105.072546
14. H.Nygren, C.Czerkinsky, M.Stenberg. Dissociation of antibodies bound to surface-immobilized antigen. J Immunol Methods 1985; 85:87-95; PMID:3908564; http://dx.doi.org/10.1016/0022-1759(85)90276-5
15. J.M.Burke. Using systms pharmacology modeling approaches to guide preclinical animal studies. 2015.
16. T.J.van Steeg, K.R.Bergmann, N.Dimasi, K.F.Sachsenmeier, B.Agoram. The application of mathematical modelling to the design of bispecific monoclonal antibodies. mAbs 2016; 8(3):585-92; PMID:26910134; http://dx.doi.org/10.1080/19420862.2016.1141160
17. E.N.Kaufman, R.K.Jain. Effect of bivalent interaction upon apparent antibody affinity: experimental confirmation of theory using fluorescence photobleaching and implications for antibody binding assays. Cancer Res 1992; 52:4157-67; PMID:1638531
18. K.M.Muller, K.M.Arndt, A.Pluckthun. Model and simulation of multivalent binding to fixed ligands. Anal Biochem 1998; 261:149-58; PMID:9716417; http://dx.doi.org/10.1006/abio.1998.2725
19. L.D.Shea, G.M.Omann, J.J.Linderman. Calculation of diffusion-limited kinetics for the reactions in collision coupling and receptor cross-linking. Biophys J 1997; 73:2949-59; PMID:9414209; http://dx.doi.org/10.1016/S0006-3495(97)78323-1
20. F.F.Heilemann, B.Joel, E.Roland, Mike. One, two or three? Probing the stoichiometry of membrane proteins by single-molecule localization microscopy. Sci Rep 2015; 5:14072; PMID:26358640; http://dx.doi.org/10.1038/srep14072
21. S.Zheng, S.Moores, S.Jarantow, J.Pardinas, M.Chiu, H.Zhou, W.Wang. Cross-arm binding efficiency of an EGFR x c-Met bispecific antibody. mAbs 2016; 8(3):551-61; PMID:26761634; http://dx.doi.org/10.1080/19420862.2015.1136762
22. R.W.Johnstone, S.M.Andrew, M.P.Hogarth, G.A.Pietersz, I.F.C.McKenzie. The effect of temperature on the binding kinetics and equilibrium constants of monoclonal antibodies to cell surface antigens. Mol Immunol 1990; 27:327-33; PMID:2359411; http://dx.doi.org/10.1016/0161-5890(90)90045-2
23. K.R.Page, E.Mezzalana, A.J.MacDonald, S.Zamuner, G.De Nicolao, A.van Maurik. Temporal pharmacokinetic/pharmacodynamic interaction between human CD3ϵ antigen–targeted monoclonal antibody otelixizumab and CD3ϵ binding and expression in human peripheral blood mononuclear cell static culture. J Pharmacol Exp Ther 2015; 355:199-205; PMID:26341624; http://dx.doi.org/10.1124/jpet.115.224899
24. I.Vainshtein, L.Roskos, J.Cheng, M.Sleeman, B.Wang, M.Liang. Quantitative measurement of the target-mediated internalization kinetics of biopharmaceuticals. Pharm Res 2015; 32:286-99; PMID:25208874; http://dx.doi.org/10.1007/s11095-014-1462-8
25. K.M.Mahoney, P.D.Rennert, G.J.Freeman. Combination cancer immunotherapy and new immunomodulatory targets. Nat Rev Drug Discov 2015; 14:561-84; PMID:26228759; http://dx.doi.org/10.1038/nrd4591
26. K.D.Wittrup, G.M.Thurber, M.M.Schmidt, J.J.Rhoden. Practical theoretic guidance for the design of tumor-targeting agents. In: K.D.Wittrup, L.V.Gregory, eds. Methods in Enzymology: Academic Press, 2012:255-68; http://dx.doi.org/10.1016/B978-0-12-396962-0.00010-0
27. J.A.Huwaldt. Plot Digitizer 2.6.8. 2015; http://plotdigitizer.sourceforge.net/
28. R.A.Kerr, T.M.Bartol, B.Kaminsky, M.Dittrich, J.-C.J.Chang, S.B.Baden, T.J.Sejnowski, J.R.Stiles. Fast Monte Carlo simulation methods for biological reaction-diffusion systems in solution and on surfaces. SIAM J Sci Comput 2008; 30:3126-49; PMID:20151023; http://dx.doi.org/10.1137/070692017
29. J.R.Stiles, T.M.Bartol. Monte Carlo methods for simulating realistic synaptic microphysiology using MCell. In: E.De Schutter, ed. Computational neuroscience Realistic modeling for experimentalists. Boca Raton, FL: CRC Press, 2001; 87-127.
30. J.R.Stiles, D.Van Helden, T.M.Bartol, Jr., E.E.Salpeter, M.M.Salpeter. Miniature endplate current rise times less than 100 microseconds from improved dual recordings can be modeled with passive acetylcholine diffusion from a synaptic vesicle. Proc Natl Acad Sci USA 1996; 93:5747-52; PMID:8650164; http://dx.doi.org/10.1073/pnas.93.12.5747
31. MCell Monte Carlo Cell.
32. B.O.Community. Blender - a 3D modelling and rendering package. Blender Foundation, 2015.
33. G.Schreiber. Kinetic studies of protein–protein interactions. Curr Opin Struct Biol 2002; 12:41-7; PMID:11839488; http://dx.doi.org/10.1016/S0959-440X(02)00287-7
34. S.H.Northrup, H.P.Erickson. Kinetics of protein-protein association explained by Brownian dynamics computer simulation. Proc Natl Acad Sci USA 1992; 89:3338-42; PMID:1565624; http://dx.doi.org/10.1073/pnas.89.8.3338
35. D.C.Torney, H.M.McConnell. Diffusion-limited reaction rate theory for two-dimensional systems. Proc R Soc Lond 1983; A 387:147-70; http://dx.doi.org/10.1098/rspa.1983.0055
36. B.Goldstein, R.Griego, C.Wofsy. Diffusion-limited forward rate constants in two dimensions. Application to the trapping of cell surface receptors by coated pits. Biophys J 1984; 46:573-86; PMID:6149773; http://dx.doi.org/10.1016/S0006-3495(84)84056-4
37. D.Colquhoun, K.A.Dowsland, M.Beato, A.J.R.Plested. How to impose microscopic reversibility in complex reaction mechanisms. Biophys J 2004; 86:3510-8; PMID:15189850; http://dx.doi.org/10.1529/biophysj.103.038679
38. D.M.Zhu, M.L.Dustin, C.W.Cairo, D.E.Golan. Analysis of two-dimensional dissociation constant of laterally mobile cell adhesion molecules. Biophys J 2007; 92:1022-34; PMID:17085486; http://dx.doi.org/10.1529/biophysj.106.089649
39. P.A.van der Merwe, A.N.Barclay, D.W.Mason, E.A.Davies, B.P.Morgan, M.Tone, A.K.Krishnam, C.Ianelli, S.J.Davis. Human cell-adhesion molecule CD2 binds CD58 (LFA-3) with a very low affinity and an extremely fast dissociation rate but does not dind CD48 or CD59. Biochemistry 1994; 33:10149-60; PMID:7520278; http://dx.doi.org/10.1021/bi00199a043
40. H.Zhan, R.Stanciauskas, C.Stigloher, K.K.Dizon, M.Jospin, J.-L.Bessereau, F.Pinaud. In vivo single-molecule imaging identifies altered dynamics of calcium channels in dystrophin-mutant C. elegans. Nat Commun 2014; 5:4974; PMID:25232639; http://dx.doi.org/10.1038/ncomms5974
41. R.Pal, B.C.Nair, G.M.Hoke, M.G.Sarngadharan, M.Edidin. Lateral diffusion of CD4 on the surface of a human neoplastic T-cell line probed with a fluorescent derivative of the envelope glycoprotein (gp120) of human immunodeficiency virus type 1 (HIV-1). J Cell Physiol 1991; 147:326-32; PMID:2040664; http://dx.doi.org/10.1002/jcp.1041470219
42. S.S.Rawat, C.Zimmerman, B.T.Johnson, E.Cho, S.J.Lockett, R.Blumenthal, A.Puri. Restricted lateral mobility of plasma membrane CD4 impairs HIV-1 envelope glycoprotein mediated fusion. Mol Membr Biol 2008; 25:83-94; PMID:18097956; http://dx.doi.org/10.1080/09687680701613713
43. A.-M.Baker, A.Saulière, G.Gaibelet, B.Lagane, S.Mazères, M.Fourage, F.Bachelerie, L.Salomé, A.Lopez, F.Dumas. CD4 interacts constitutively with multiple CCR5 at the plasma membrane of living cells. J Biol Chem 2007; 282:35163-8; PMID:17855336; http://dx.doi.org/10.1074/jbc.M705617200
44. C.M.Finnegan, S.S.Rawat, E.H.Cho, D.L.Guiffre, S.Lockett, A.H.Merrill, R.Blumenthal. Sphingomyelinase testricts the lateral diffusion of CD4 and inhibits human immunodeficiency virus fusion. J Virol 2007; 81:5294-304; PMID:17344303; http://dx.doi.org/10.1128/JVI.02553-06
45. W.M.Saltzman, M.L.Radomsky, K.J.Whaley, R.A.Cone. Antibody diffusion in human cervical mucus. Biophys Jo 1994; 66:508-15; PMID:8161703; http://dx.doi.org/10.1016/S0006-3495(94)80802-1