An induced rebinding model of antigen discrimination☆

Highlights • We propose that pMHC binding to TCR can increase (induce) pMHC rebinding.• Published studies are consistent with an induced rebinding model.• Induced rebinding improves the ability of T cells to discriminate antigens.• Induced rebinding relates 3D to 2D TCR–pMHC binding parameters.

[1]  H. Zhang,et al.  Why Do Some T Cell Receptor Cytoplasmic Domains Associate with the Plasma Membrane? , 2012, Front. Immun..

[2]  Daniel Coombs,et al.  Antigen Potency and Maximal Efficacy Reveal a Mechanism of Efficient T Cell Activation , 2011, Science Signaling.

[3]  Alexis M. Kalergis,et al.  Efficient T cell activation requires an optimal dwell-time of interaction between the TCR and the pMHC complex , 2001, Nature Immunology.

[4]  William J. Fitzgerald,et al.  Single-molecule level analysis of the subunit composition of the T cell receptor on live T cells , 2007, Proceedings of the National Academy of Sciences.

[5]  T. McKeithan,et al.  Kinetic proofreading in T-cell receptor signal transduction. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Ronald N Germain,et al.  Modeling T Cell Antigen Discrimination Based on Feedback Control of Digital ERK Responses , 2005, PLoS biology.

[7]  V. Cerundolo,et al.  Kinetics and mechanics of two-dimensional interactions between T cell receptors and different activating ligands. , 2012, Biophysical journal.

[8]  Cliburn Chan,et al.  Cooperative enhancement of specificity in a lattice of T cell receptors , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[9]  S. Andrews Serial rebinding of ligands to clustered receptors as exemplified by bacterial chemotaxis , 2005, Physical biology.

[10]  Paul François,et al.  Phenotypic model for early T-cell activation displaying sensitivity, specificity, and antagonism , 2013, Proceedings of the National Academy of Sciences.

[11]  Bernhard Hemmer,et al.  TCR ligand discrimination is enforced by competing ERK positive and SHP-1 negative feedback pathways , 2003, Nature Immunology.

[12]  Mark M Davis,et al.  TCR and Lat are expressed on separate protein islands on T cell membranes and concatenate during activation , 2010, Nature Immunology.

[13]  Evan W. Newell,et al.  TCR–peptide–MHC interactions in situ show accelerated kinetics and increased affinity , 2010, Nature.

[14]  Barbara Hausmann,et al.  Thymic selection threshold defined by compartmentalization of Ras/MAPK signalling , 2006, Nature.

[15]  Ji Won Yoon,et al.  DySCo: Quantitating Associations of Membrane Proteins Using Two-Color Single-Molecule Tracking , 2009, Biophysical journal.

[16]  Raibatak Das,et al.  A Role for Rebinding in Rapid and Reliable T Cell Responses to Antigen , 2009, PLoS Comput. Biol..

[17]  David M Kranz,et al.  Quantitative analysis of the contribution of TCR/pepMHC affinity and CD8 to T cell activation. , 2003, Immunity.

[18]  B. Alarcón,et al.  Coexistence of multivalent and monovalent TCRs explains high sensitivity and wide range of response , 2005, The Journal of experimental medicine.

[19]  C. Carman,et al.  Antigen Recognition Is Facilitated by Invadosome-like Protrusions Formed by Memory/Effector T Cells , 2012, The Journal of Immunology.

[20]  Jianzhu Chen,et al.  The Impact of TCR-Binding Properties and Antigen Presentation Format on T Cell Responsiveness1 , 2009, The Journal of Immunology.

[21]  Etienne Gagnon,et al.  Regulation of T Cell Receptor Activation by Dynamic Membrane Binding of the CD3ɛ Cytoplasmic Tyrosine-Based Motif , 2008, Cell.

[22]  W. Schamel,et al.  Increased sensitivity of antigen-experienced T cells through the enrichment of oligomeric T cell receptor complexes. , 2011, Immunity.

[23]  Sudha Kumari,et al.  T cell antigen receptor activation and actin cytoskeleton remodeling. , 2014, Biochimica et biophysica acta.

[24]  Paul D. Dunne,et al.  Taking T cells beyond the diffraction limit , 2010, Nature Immunology.

[25]  Mark M. Davis,et al.  Peptide-MHC heterodimers show that thymic positive selection requires a more restricted set of self-peptides than negative selection , 2010, The Journal of experimental medicine.

[26]  Arup K. Chakraborty,et al.  Fast on-rates allow short dwell time ligands to activate T cells , 2010, Proceedings of the National Academy of Sciences.

[27]  J. Allard,et al.  Mechanical modulation of receptor-ligand interactions at cell-cell interfaces. , 2012, Biophysical journal.

[28]  Suliana Manley,et al.  Functional nanoscale organization of signaling molecules downstream of the T cell antigen receptor. , 2011, Immunity.

[29]  M. Edidin,et al.  Quantum dot fluorescence characterizes the nanoscale organization of T cell receptors for antigen. , 2011, Biophysical journal.

[30]  Omer Dushek,et al.  Basic residues in the T-cell receptor ζ cytoplasmic domain mediate membrane association and modulate signaling , 2011, Proceedings of the National Academy of Sciences.

[31]  Cheng Zhu,et al.  The kinetics of two dimensional TCR and pMHC interactions determine T cell responsiveness , 2010, Nature.

[32]  Mark M Davis,et al.  Spatial and temporal dynamics of T cell receptor signaling with a photoactivatable agonist. , 2007, Immunity.

[33]  Rajat Varma,et al.  T cell receptor-proximal signals are sustained in peripheral microclusters and terminated in the central supramolecular activation cluster. , 2006, Immunity.

[34]  Deborah Leckband,et al.  Memory in receptor–ligand-mediated cell adhesion , 2007, Proceedings of the National Academy of Sciences.

[35]  U. Täuber,et al.  Effects of receptor clustering on ligand dissociation kinetics: theory and simulations. , 2004, Biophysical journal.

[36]  Daniel Coombs,et al.  Dependence of T Cell Antigen Recognition on T Cell Receptor-Peptide MHC Confinement Time , 2010, Immunity.

[37]  B. Evavold,et al.  Two-stage cooperative T cell receptor-peptide major histocompatibility complex-CD8 trimolecular interactions amplify antigen discrimination. , 2011, Immunity.

[38]  T. Fahmy,et al.  Increased TCR avidity after T cell activation: a mechanism for sensing low-density antigen. , 2001, Immunity.

[39]  Omer Dushek,et al.  Mechanisms for T cell receptor triggering , 2011, Nature Reviews Immunology.

[40]  R. Germain,et al.  The dynamics of T cell receptor signaling: complex orchestration and the key roles of tempo and cooperation. , 1999, Annual review of immunology.

[41]  P. R. ten Wolde,et al.  Membrane clustering and the role of rebinding in biochemical signaling. , 2011, Biophysical journal.

[42]  P. A. van der Merwe,et al.  Late arrival: recruiting coreceptors to the T cell receptor complex. , 2011, Immunity.