Boltzmann energy-based image analysis demonstrates that extracellular domain size differences explain protein segregation at immune synapses

PLoS Computational Biology

Volumn 7, Issue 8, 2011, Pages

  Burroughs, Nigel J ^a   Köhler, Karsten ^b   Miloserdov, Vladimir ^a   Dustin, Michael L ^c   van der Merwe, P Anton ^d   Davis, Daniel M ^e  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b ADDENBROOKE S HOSPITAL   (United Kingdom)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SIGNALING; CYTOLOGY; DIGITAL STORAGE; FLUOROPHORES; IMAGE ANALYSIS; T-CELLS;

BOLTZMANN; DOMAIN SIZE; ENERGY-BASED; EXTRACELLULAR DOMAINS; IMAGE-ANALYSIS; IMMUNE SYNAPSE; INTEGRINS; NK CELLS; PROTEIN SIZE; SIZE DIFFERENCE;

PROTEINS;

ARTICLE; BINDING KINETICS; BIOPHYSICS; CONTROLLED STUDY; CYTOSKELETON; ENERGY YIELD; EXTRACELLULAR SPACE; FLUORESCENCE ANALYSIS; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IMAGE PROCESSING; IMMUNOLOGICAL SYNAPSE; LIGAND BINDING; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; MOLECULAR IMAGING; MOLECULAR SIZE; PREDICTION; PROCESS DEVELOPMENT; PROTEIN DOMAIN; PROTEIN LOCALIZATION; THREE DIMENSIONAL IMAGING; AUTOMATED PATTERN RECOGNITION; BIOLOGY; CELL COMMUNICATION; CELL LINE; CHEMISTRY; COMPUTER SIMULATION; KINETICS; METABOLISM; METHODOLOGY; NATURAL KILLER CELL; PARTICLE SIZE; PHYSIOLOGY; POISSON DISTRIBUTION; PROTEIN TERTIARY STRUCTURE; T LYMPHOCYTE; THERMODYNAMICS;

INTERCELLULAR ADHESION MOLECULE 1; MEMBRANE PROTEIN;

CELL COMMUNICATION; CELL LINE, TRANSFORMED; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; EXTRACELLULAR SPACE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOLOGICAL SYNAPSES; INTERCELLULAR ADHESION MOLECULE-1; KILLER CELLS, NATURAL; KINETICS; MEMBRANE PROTEINS; PARTICLE SIZE; PATTERN RECOGNITION, AUTOMATED; POISSON DISTRIBUTION; PROTEIN STRUCTURE, TERTIARY; T-LYMPHOCYTES; THERMODYNAMICS;

EID: 80052314133     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002076     Document Type: Article

References (36)

1. Springer TA, (1990) Adhesion receptors of the immune system. Nature 346: 425-434.
2. Zhu J, Luo BH, Xiao T, Zhang C, Nishida N, et al. (2008) Structure of a Complete Integrin Ectodomain in a Physiologic Resting State and Activation and Deactivation by Applied Forces. Mol Cell 32: 849-861.
3. Grakoui A, Bromley SK, Sumen C, Davis MM, Shaw AS, et al. (1999) The immunological synapse: a molecular machine controlling T cell activation. Science 285: 221-227.
4. Monks CR, Freiberg BA, Kupfer H, Sciaky N, Kupfer A, (1998) Three dimensional segregation of supramolecular activation clusters in t cells. Nature 395: 82-86.
5. Hailman E, Burack W, Shaw A, Dustin M, Allen P, (2002) Immature CD4+CD8+ Thymocytes Form a Multifocal Immunological Synapse with Sustained Tyrosine Phosphorylation. Immunity 16: 839-848.
6. Carlin LM, Eleme K, McCann FE, Davis DM, (2001) Intercellular transfer and supramolecular organisation of human leukocyte antigen C at the inhibitory natural killer cell synapse. J Exp Med 194: 1507-1517.
7. Campi G, Varma R, Dustin ML, (2005) Actin and agonist MHC-peptide complex-dependent T cell receptor microclusters as scaffolds for signalling. J Exp Med 202: 1031-1036.
8. Mossman K, Groves J, (2007) Micropatterned supported membranes as tools for quantitative studies of the immunological synapse. Chem Soc Rev 36: 46-54.
9. Dustin ML, Olszowy MW, Holdorf AD, Li J, Bromley S, et al. (1998) A novel adaptor protein orchestrates receptor patterning and cytoskeletal polarity in t-cell contacts. Cell 94: 667-677.
10. Simons K, Ikonen E, (1997) Functional rafts in cell membranes. Nature 387: 569-572.
11. Morone N, Fujiwara T, Murase K, Kasai RS, Ike H, et al. (2006) Three-dimensional reconstruction of the membrane skeleton at the plasma membrane interface by electron tomography. J Cell Biol 174: 851-862.
12. Tsourkas P, Raychaudhuri S, (2010) Modeling of B cell synapse formation by Monte Carlo simulation shows that directed transport of receptor molecules is a potential formation mechanism. Cell Mol Bioeng 3: 256-268.
13. Qi SY, Groves JT, Chakraborty AK, (2001) Synaptic pattern formation during cellular recognition. Proc Natl Acad Sci U S A 98: 6548-6554.
14. Burroughs NJ, Wülfing C, (2002) Differential segregation in a cell:cell contact interface- the formation of the immunological synapse. Biophys J 83: 1784-1796.
15. Coombs D, Dembo M, Wolsy C, Goldstein B, (2004) Equilibrium thermodynamics of cell:cell adhesion mediated by multiple ligand-receptor pairs. Biophys J 86: 1408-1423.
16. Weikl T, Lipowski R, (2004) Pattern formation during T-cell adhesion. Biophys J 87: 3665-3678.
17. Weikl T, Asfaw M, Krobath H, Rozycki B, Lipowski R, (2009) Adhesion of membranes via receptorligand complexes: Domain formation, binding cooperativity, and active processes. Soft Matter 5: 3213-3224.
18. Davis DM, Chiu I, Fassett M, Cohen GB, Mandelboim O, et al. (1999) The human natural killer cell immune synapse. Proc Natl Acad Sci U S A 26: 15062-15067.
19. Weikl T, Groves J, Lipowski R, (2002) Pattern formation during adhesion of multicomponent membranes. Europhys Lett 6: 916-922.
20. Burshtyn DN, Shin J, Stebbins C, Long EO, (2000) Adhesion to target cells is disrupted by the killer cell inhibitory receptor. Curr Biol 10: 777-780.
21. Culley F, Johnson M, Evans J, Kumar S, Crilly R, et al. (2009) Natural Killer Cell Signal Integration Balances Synapse Symmetry and Migration. PLoS Biol 7: e1000159 doi:10.1371/journal.pbio.1000159.
22. van der Merwe PA, McNamee PN, Davies EA, Barclay AN, Davis SJ, (1995) Topology of the CD2-CD48 cell-adhesion molecule complex: implications for antigen recognition by T cells. Curr Biol 5: 74-84.
23. Wang JH, Smolyar A, Tan K, Liu JH, Kim M, et al. (1999) Structure of a heterophilic adhesion complex between the human CD2 and CD58 (LFA-3) counterreceptors. Cell 97: 791-803.
24. Yang Y, Jun CD, Liu JH, Zhang R, Joachimiak A, et al. (2004) Structural basis for dimerization of ICAM-1 on the cell surface. Mol Cell 14: 269-276.
25. Dustin ML, Starr T, Coombs D, Majeau GR, Meier W, et al. (2007) Quantification and Modeling of Tripartite CD2-, CD58FC Chimera (Alefacept)-, and CD16-mediated Cell Adhesion. J Biol Chem 282: 34748-34757.
26. Zhu J, Dustin ML, Cairo CW, Golan DE, (2007) Analysis of Two-Dimensional Dissociation Constant of Laterally Mobile Cell Adhesion Molecules. Biophys 92: 1022-1034.
27. Milstein O, Tseng SY, Starr T, Llodra J, Nans A, et al. (2008) Nanoscale increases in CD2-CD48- mediated intermembrane spacing decrease adhesion and reorganize the immunological synapse. J Biol Chem 283: 34414-34422.
28. Chattopadhyay A, Burroughs N, (2007) Close contact fluctuations: the seeding of signalling domains in the immunological synapse. Europhys Lett 77: 48003.
29. Dustin ML, Golan DE, Zhu DM, Miller JM, Meier W, et al. (1997) Low affinity interaction of human or rat T cell adhesion molecule CD2 with its ligand aligns adhering membranes to achieve high physiological affinity. J Biol Chem 272: 30889-30898.
30. Bell GI, (1978) Models of specific adhesion of cells to cells. Science 200: 618-627.
31. Almeida CR, Davis DM, (2006) Segregation of HLA-C from ICAM-1 at NK Cell Immune Synapses Is Controlled by Its Cell Surface Density. J Immunol 177: 6904-6910.
32. Köhler K, Xiong S, Brzostek J, Mehrabi M, Eissmann P, et al. (2010) Matched Sizes of Activating and Inhibitory Receptor/Ligand Pairs Are Required for Optimal Signal Integration by Human Natural Killer Cells. PLoS ONE 5: e15374 doi:10.1371/journal.pone.0015374.
33. Shimizu Y, Geraghty DE, Koller BH, Orr HT, DeMars R, (1988) Transfer and expression of three cloned human non-HLA-A,B,C class I major histocompatibility complex genes in mutant lymphoblastoid cells. Proc Natl Acad Sci U S A 85: 227-231.
34. Barreiro O, Yez-M M, Serrador JM, Montoya MC, Vicente-Manzanares M, et al. (2002) Dynamic interaction of VCAM-1 and ICAM-1 with moesin and ezrin in a novel endothelial docking structure for adherent leukocytes. J Cell Biol 157: 1233-1245.
35. Cohen GB, Gandhi RT, Davis DM, Mandelboim O, Chen BK, et al. (1999) The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 10: 661-671.
36. Gelman A, Rubin D, (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7: 457-511.