Dynamics of cell surface molecules during T cell recognition.

Recognition of foreign antigens by T lymphocytes is a very important component of vertebrate immunity-vital to the clearance of pathogenic organisms and particular viruses and necessary, indirectly, for the production of high affinity antibodies. T cell recognition is mediated by the systematic scanning of cell surfaces by T cells, which collectively express many antigen receptors. When the appropriate antigenic peptide bound to a molecule of the major histocompatibility complex is found-even in minute quantities-a series of elaborate cell-surface molecule and internal rearrangements take place. The sequence of events and the development of techniques required to observe these events have significantly enhanced our understanding of T cell recognition and may find application in other systems of transient cell:cell interactions as well.

[1]  S. Jameson,et al.  T-cell-receptor affinity and thymocyte positive selection , 1996, Nature.

[2]  Emil R. Unanue,et al.  Quantitation of antigen-presenting cell MHC class II/peptide complexes necessary for T-cell stimulation , 1990, Nature.

[3]  D. Mason,et al.  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. , 1994, Biochemistry.

[4]  Michael Loran Dustin,et al.  Immature CD4(+)CD8(+) thymocytes form a multifocal immunological synapse with sustained tyrosine phosphorylation. , 2002, Immunity.

[5]  Jianzhu Chen,et al.  Soluble peptide–MHC monomers cause activation of CD8+ T cells through transfer of the peptide to T cell MHC molecules , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Patricia L. Widder,et al.  A Novel Adaptor Protein Orchestrates Receptor Patterning and Cytoskeletal Polarity in T-Cell Contacts , 1998, Cell.

[7]  Bernard Malissen,et al.  A T cell receptor CDR3beta loop undergoes conformational changes of unprecedented magnitude upon binding to a peptide/MHC class I complex. , 2002, Immunity.

[8]  Michael Loran Dustin,et al.  T Cell Receptor Signaling Precedes Immunological Synapse Formation , 2002, Science.

[9]  E. Bröcker,et al.  Antigen presentation in extracellular matrix: interactions of T cells with dendritic cells are dynamic, short lived, and sequential. , 2000, Immunity.

[10]  G. Gao,et al.  Killer Cell Immunoglobulin Receptors and T Cell Receptors Bind Peptide-Major Histocompatibility Complex Class I with Distinct Thermodynamic and Kinetic Properties* , 1999, The Journal of Biological Chemistry.

[11]  Jan Cerny,et al.  T-cell engagement of dendritic cells rapidly rearranges MHC class II transport , 2002, Nature.

[12]  S. Bromley,et al.  Stimulation of naïve T‐cell adhesion and immunological synapse formation by chemokine‐dependent and ‐independent mechanisms , 2002, Immunology.

[13]  D. Toomre,et al.  Dendritic cell maturation triggers retrograde MHC class II transport from lysosomes to the plasma membrane , 2002, Nature.

[14]  D. Wiley,et al.  Conversion of a T cell antagonist into an agonist by repairing a defect in the TCR/peptide/MHC interface: implications for TCR signaling. , 2000, Immunity.

[15]  Gerhard Wagner,et al.  Structure, specificity and CDR mobility of a class II restricted single-chain T-cell receptor , 1999, Nature Structural Biology.

[16]  P. Cresswell,et al.  Assembly, transport, and function of MHC class II molecules. , 1994, Annual review of immunology.

[17]  H. Ploegh,et al.  Peptide antagonism and T cell receptor interactions with peptide-MHC complexes. , 1998, Immunity.

[18]  J. Egen,et al.  Cytotoxic T lymphocyte antigen-4 accumulation in the immunological synapse is regulated by TCR signal strength. , 2002, Immunity.

[19]  Mark M. Davis,et al.  Direct observation of ligand recognition by T cells , 2002, Nature.

[20]  C. Monks,et al.  Selective modulation of protein kinase C-Θ during T-cell activation , 1997, Nature.

[21]  L R Pease,et al.  Alphabeta T cell receptor interactions with syngeneic and allogeneic ligands: affinity measurements and crystallization. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[22]  M. Davis,et al.  Visualizing the dynamics of T cell activation: intracellular adhesion molecule 1 migrates rapidly to the T cell/B cell interface and acts to sustain calcium levels. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[23]  A. Barclay,et al.  Transient intercellular adhesion: the importance of weak protein-protein interactions. , 1994, Trends in biochemical sciences.

[24]  M. Davis,et al.  Kinetics of T-cell receptor binding to peptide/I-Ek complexes: correlation of the dissociation rate with T-cell responsiveness. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[25]  V. Moy,et al.  Direct evidence for two affinity states for lymphocyte function-associated antigen 1 on activated T cells. , 1993, The Journal of biological chemistry.

[26]  P. Negulescu,et al.  Polarity of T cell shape, motility, and sensitivity to antigen. , 1996, Immunity.

[27]  S. Bromley,et al.  The immunological synapse: a molecular machine controlling T cell activation. , 1999, Science.

[28]  D. Zaller,et al.  Staging and resetting T cell activation in SMACs , 2002, Nature Immunology.

[29]  P. Anton van der Merwe,et al.  The TCR Triggering Puzzle , 2001 .

[30]  Mark M. Davis,et al.  Imaging synapse formation during thymocyte selection: inability of CD3zeta to form a stable central accumulation during negative selection. , 2002, Immunity.

[31]  K. Garcia,et al.  A functional hot spot for antigen recognition in a superagonist TCR/MHC complex. , 2000, Immunity.

[32]  Ellis L. Reinherz,et al.  T Cell Receptor Binding to a pMHCII Ligand Is Kinetically Distinct from and Independent of CD4* , 2001, The Journal of Biological Chemistry.

[33]  N. Shastri,et al.  Measurement of ligand-induced activation in single viable T cells using the lacZ reporter gene. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[34]  B M Baker,et al.  Four A6-TCR/peptide/HLA-A2 structures that generate very different T cell signals are nearly identical. , 1999, Immunity.

[35]  S. Singer,et al.  On the mechanism of unidirectional killing in mixtures of two cytotoxic T lymphocytes. Unidirectional polarization of cytoplasmic organelles and the membrane-associated cytoskeleton in the effector cell , 1986, The Journal of experimental medicine.

[36]  Michael Loran Dustin,et al.  Cutting Edge: Quantitative Imaging of Raft Accumulation in the Immunological Synapse , 2002, The Journal of Immunology.

[37]  H. Ploegh,et al.  How MHC class II molecules acquire peptide cargo: biosynthesis and trafficking through the endocytic pathway. , 1995, Annual review of cell and developmental biology.

[38]  J. Altman,et al.  Initiation of signal transduction through the T cell receptor requires the multivalent engagement of peptide/MHC ligands [corrected]. , 1998, Immunity.

[39]  L R Pease,et al.  Structural basis of plasticity in T cell receptor recognition of a self peptide-MHC antigen. , 1998, Science.

[40]  David I. Stuart,et al.  The Human Low Affinity Fcγ Receptors IIa, IIb, and III Bind IgG with Fast Kinetics and Distinct Thermodynamic Properties* , 2001, The Journal of Biological Chemistry.

[41]  Mark M. Davis,et al.  T-cell antigen receptor genes and T-cell recognition , 1988, Nature.

[42]  D. Fremont,et al.  High- and low-potency ligands with similar affinities for the TCR: the importance of kinetics in TCR signaling. , 1998, Immunity.

[43]  P. Linsley,et al.  CD80 (B7-1) Binds Both CD28 and CTLA-4 with a Low Affinity and Very Fast Kinetics , 1997, The Journal of experimental medicine.

[44]  D. Margulies Interactions of TCRs with MHC-peptide complexes: a quantitative basis for mechanistic models. , 1997, Current opinion in immunology.

[45]  Philippe Bousso,et al.  Dynamics of Thymocyte-Stromal Cell Interactions Visualized by Two-Photon Microscopy , 2002, Science.

[46]  J. Egen,et al.  CTLA-4-mediated inhibition in regulation of T cell responses: mechanisms and manipulation in tumor immunotherapy. , 2001, Annual review of immunology.

[47]  B. Freiberg,et al.  Formation of supramolecular activation clusters on fresh ex vivo CD8+ T cells after engagement of the T cell antigen receptor and CD8 by antigen-presenting cells , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Ursula Esser,et al.  Mapping T-cell receptor–peptide contacts by variant peptide immunization of single-chain transgenics , 1992, Nature.

[49]  H. Grey,et al.  The minimal number of class II MHC-antigen complexes needed for T cell activation. , 1990, Science.

[50]  A. Trautmann,et al.  CD8 expression allows T cell signaling by monomeric peptide-MHC complexes. , 1998, Immunity.

[51]  A. Barclay,et al.  Affinity and kinetic analysis of the interaction of the cell adhesion molecules rat CD2 and CD48. , 1993, The EMBO journal.

[52]  A. Hayday [gamma][delta] cells: a right time and a right place for a conserved third way of protection. , 2000, Annual review of immunology.

[53]  Raimund J. Ober,et al.  Kinetics and thermodynamics of T cell receptor– autoantigen interactions in murine experimental autoimmune encephalomyelitis , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[54]  D. Jeanfavre,et al.  Molecular regulation of the interaction between leukocyte function-associated antigen-1 and soluble ICAM-1 by divalent metal cations. , 1998, Journal of immunology.

[55]  I. Weissman,et al.  Thymus cell migration: Quantitative aspects of cellular traffic from the thymus to the periphery in mice , 1980, European journal of immunology.

[56]  Z Reich,et al.  Thermodynamics of T cell receptor binding to peptide-MHC: evidence for a general mechanism of molecular scanning. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[57]  R. J. Cohen,et al.  Kinetics and affinity of reactions between an antigen-specific T cell receptor and peptide-MHC complexes. , 1994, Immunity.

[58]  Michael Loran Dustin,et al.  Visualization of CD2 interaction with LFA-3 and determination of the two-dimensional dissociation constant for adhesion receptors in a contact area , 1996, The Journal of cell biology.

[59]  Graça Raposo,et al.  Antigen-dependent and -independent Ca2+ Responses Triggered in T Cells by Dendritic Cells Compared with B Cells , 1998, The Journal of experimental medicine.

[60]  T. Zal,et al.  Inhibition of T cell receptor-coreceptor interactions by antagonist ligands visualized by live FRET imaging of the T-hybridoma immunological synapse. , 2002, Immunity.

[61]  S. Jameson,et al.  Qualitative and quantitative differences in T cell receptor binding of agonist and antagonist ligands. , 1999, Immunity.

[62]  A. Trautmann,et al.  Antigen recognition by helper T cells elicits a sequence of distinct changes of their shape and intracellular calcium , 1994, Current Biology.

[63]  Balbino Alarcón,et al.  Recruitment of Nck by CD3ϵ Reveals a Ligand-Induced Conformational Change Essential for T Cell Receptor Signaling and Synapse Formation , 2002, Cell.

[64]  S. Singer,et al.  The specific direct interaction of helper T cells and antigen- presenting B cells. II. Reorientation of the microtubule organizing center and reorganization of the membrane-associated cytoskeleton inside the bound helper T cells , 1987, The Journal of experimental medicine.

[65]  Y. Chien,et al.  A TCR binds to antagonist ligands with lower affinities and faster dissociation rates than to agonists. , 1996, Immunity.

[66]  F. Gounari,et al.  On the brink of becoming a T cell. , 2002, Current opinion in immunology.

[67]  A. Fersht,et al.  Rapid, electrostatically assisted association of proteins , 1996, Nature Structural Biology.

[68]  B K Jakobsen,et al.  T cell receptor and coreceptor CD8 alphaalpha bind peptide-MHC independently and with distinct kinetics. , 1999, Immunity.

[69]  P Bongrand,et al.  Determination of the lifetime and force dependence of interactions of single bonds between surface-attached CD2 and CD48 adhesion molecules. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[70]  A. Lanzavecchia,et al.  T lymphocyte costimulation mediated by reorganization of membrane microdomains. , 1999, Science.

[71]  Ash A. Alizadeh,et al.  Genomic expression programs and the integration of the CD28 costimulatory signal in T cell activation , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[72]  J. Cochran,et al.  The relationship of MHC-peptide binding and T cell activation probed using chemically defined MHC class II oligomers. , 2000, Immunity.

[73]  M. Davis,et al.  Differential clustering of CD4 and CD3zeta during T cell recognition. , 2000, Science.

[74]  G. Crabtree,et al.  NFAT Signaling Choreographing the Social Lives of Cells , 2002, Cell.

[75]  Mark M. Davis,et al.  Two-step binding mechanism for T-cell receptor recognition of peptide–MHC , 2002, Nature.

[76]  D. Margulies,et al.  Lack of strict correlation of functional sensitization with the apparent affinity of MHC/peptide complexes for the TCR. , 1995, Journal of immunology.

[77]  Boris Barbour,et al.  Functional antigen-independent synapses formed between T cells and dendritic cells , 2001, Nature Immunology.

[78]  Z Reich,et al.  Ligand recognition by alpha beta T cell receptors. , 1998, Annual review of immunology.

[79]  T. Mosmann,et al.  Polarized expression of cytokines in cell conjugates of helper T cells and splenic B cells. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[80]  B K Jakobsen,et al.  TCR binding to peptide-MHC stabilizes a flexible recognition interface. , 1999, Immunity.

[81]  A. Lanzavecchia,et al.  The duration of antigenic stimulation determines the fate of naive and effector T cells. , 1998, Immunity.

[82]  S. Singer,et al.  Cell biology of cytotoxic and helper T cell functions: immunofluorescence microscopic studies of single cells and cell couples. , 1989, Annual review of immunology.

[83]  J. Morrow,et al.  The spectrin-ankyrin skeleton controls CD45 surface display and interleukin-2 production. , 2002, Immunity.

[84]  R. Germain,et al.  Dynamic Imaging of T Cell-Dendritic Cell Interactions in Lymph Nodes , 2002, Science.

[85]  P. Merwe,et al.  The immunological synapse: required for T cell receptor signalling or directing T cell effector function? , 2001, Current Biology.

[86]  A. Weiss,et al.  Akt provides the CD28 costimulatory signal for up-regulation of IL-2 and IFN-γ but not TH2 cytokines , 2001, Nature Immunology.

[87]  J. Rast,et al.  Evolution of antigen binding receptors. , 1999, Annual review of immunology.

[88]  D E Leckband,et al.  Long-range attraction and molecular rearrangements in receptor-ligand interactions. , 1992, Science.

[89]  Matthew F. Krummel,et al.  Quantifying signaling-induced reorientation of T cell receptors during immunological synapse formation , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[90]  Mark M Davis,et al.  Dynamics of p56lck translocation to the T cell immunological synapse following agonist and antagonist stimulation. , 2002, Immunity.

[91]  I. Trowbridge,et al.  CD45: an emerging role as a protein tyrosine phosphatase required for lymphocyte activation and development. , 1994, Annual review of immunology.

[92]  Michael Loran Dustin,et al.  Role of lymphocyte adhesion receptors in transient interactions and cell locomotion. , 1991, Annual review of immunology.

[93]  A. Weiss,et al.  Signal transduction by the TCR for antigen. , 2000, Current opinion in immunology.

[94]  C. Janeway,et al.  The specificity and orientation of a TCR to its peptide-MHC class II ligands. , 1996, Immunity.

[95]  Mark J. Miller,et al.  Two-Photon Imaging of Lymphocyte Motility and Antigen Response in Intact Lymph Node , 2002, Science.

[96]  Colin R. F. Monks,et al.  Three-dimensional segregation of supramolecular activation clusters in T cells , 1998, Nature.

[97]  P. Merwe,et al.  A Subtle Role for Cd2 in T Cell Antigen Recognition , 1999 .

[98]  Andrea Iaboni,et al.  The interaction properties of costimulatory molecules revisited. , 2002, Immunity.

[99]  C. Janeway The T cell receptor as a multicomponent signalling machine: CD4/CD8 coreceptors and CD45 in T cell activation. , 1992, Annual review of immunology.

[100]  S. Bromley,et al.  Identification of self through two-dimensional chemistry and synapses. , 2001, Annual review of cell and developmental biology.

[101]  Mark M. Davis,et al.  Determination of the Relationship Between T Cell Responsiveness and the Number of MHC-Peptide Complexes Using Specific Monoclonal Antibodies1 , 2000, The Journal of Immunology.

[102]  M. Davis,et al.  A receptor/cytoskeletal movement triggered by costimulation during T cell activation. , 1998, Science.

[103]  M. Luscher,et al.  Peptide binding to class I MHC on living cells and quantitation of complexes required for CTL lysis , 1991, Nature.

[104]  A. Fersht Nucleation mechanisms in protein folding. , 1997, Current opinion in structural biology.

[105]  R C Brower,et al.  Minimal requirements for peptide mediated activation of CD8+ CTL. , 1994, Molecular immunology.

[106]  H. Eisen,et al.  Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T cell response. , 1996, Immunity.

[107]  G. Griffiths,et al.  The immunological synapse of CTL contains a secretory domain and membrane bridges. , 2001, Immunity.

[108]  E. Jaffee,et al.  Enhanced antigen-specific antitumor immunity with altered peptide ligands that stabilize the MHC-peptide-TCR complex. , 2000, Immunity.

[109]  S. Davis,et al.  The role of charged residues mediating low affinity protein-protein recognition at the cell surface by CD2. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[110]  J. Allison,et al.  Co-stimulation in T cell responses. , 1997, Current opinion in immunology.