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Perspective

Early T‐cell activation biophysics

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Pages 401-411 | Received 07 Aug 2009, Accepted 05 Oct 2009, Published online: 07 Sep 2010

References

  • Abastado , JP , Lone , YC , Casrouge , A , Boulot , G and Kourilsky , P . 1995 . “Dimerization of soluble major histocompatibility complex‐peptide complexes is sufficient for activation of T‐cell hybridoma and induction of unresponsiveness.” . J. Exp. Med. , 182 : 439 – 447 .
  • Abbott , NL , Folkers , JP and Whitesides , GM . 1992 . “Manipulation of the wettability of surfaces on the 0.1‐ to 1‐micrometer scale through micromachining and molecular self‐assembly.” . Science , 257 : 1380 – 1382 .
  • Aivazian , D and Stern , LJ . 2000 . “Phosphorylation of T‐cell receptor zeta is regulated by a lipid dependent folding transition.” . Nat. Struct. Biol. , 7 : 1023 – 1026 .
  • Allenspach , EJ , Cullinan , P , Tong , J , Tang , Q , Tesciuba , AG , Cannon , JL , Takahashi , SM , Morgan , R , Burkhardt , JK and Sperling , AI . 2001 . “ERM‐dependent movement of CD43 defines a novel protein complex distal to the immunological synapse.” . Immunity , 15 : 739 – 750 .
  • Beddoe , T . 2009 . “Antigen ligation triggers a conformational change within the constant domain of the alphabeta T‐cell receptor.” . Immunity , 30 : 777 – 788 .
  • Betzig , E , Patterson , GH , Sougrat , R , Lindwasser , OW , Olenych , S , Bonifacino , JS , Davidson , MW , Lippincott‐Schwartz , J and Hess , HF . 2006 . “Imaging intracellular fluorescent proteins at nanometer resolution.” . Science , 313 : 1642 – 1645 .
  • Blanchard , N , Decraene , M , Yang , K , Miro‐Mur , F , Amigorena , S and Hivroz , C . 2004 . “Strong and durable TCR clustering at the T/dendritic cell immune synapse is not required for NFAT activation and IFN‐gamma production in human CD4+ T cells.” . J. Immunol. , 173 : 3062 – 3072 .
  • Boniface , JJ , Rabinowitz , JD , Wulfing , C , Hampl , J , Reich , Z , Altman , JD , Kantor , RM , Beeson , C , McConnell , HM and Davis , MM . 1998 . “Initiation of signal transduction through the T‐cell receptor requires the multivalent engagement of peptide/MHC ligands.” . Immunity , 9 : 459 – 466 .
  • Bromley , SK , Burack , WR , Johnson , KG , Somersalo , K , Sims , TN , Sumen , C , Davis , MM , Shaw , AS , Allen , PM and Dustin , ML . 2001 . “The immunological synapse.” . Annu. Rev. Immunol. , 19 : 375 – 396 .
  • Brossard , C , Feuillet , V , Schmitt , A , Randriamampita , C , Romao , M , Raposo , G and Trautmann , A . 2005 . “Multifocal structure of the T‐cell—dendritic cell synapse.” . Eur. J. Immunol. , 35 : 1741 – 1753 .
  • Burroughs , NJ and van der Merwe , PA . 2007 . “Stochasticity and spatial heterogeneity in T‐cell activation.” . Immunol. Rev. , 216 : 69 – 80 .
  • Carpentier , B , Hivroz , C and Henry , N . 2009a . “Mechanical forces in T‐cell triggering.” . Biophys. J. , 96 : 368a
  • Carpentier , B , Pierobon , P , Hivroz , C and Henry , N . 2009b . “T‐cell artificial focal triggering tools: linking surface interactions with cell response.” . PLoS ONE , 4 : e4784
  • Choudhuri , K and van der Merwe , PA . 2007 . “Molecular mechanisms involved in T‐cell receptor triggering.” . Semin. Immunol. , 19 : 255 – 261 .
  • Choudhuri , K , Wiseman , D , Brown , MH , Gould , K and van der Merwe , PA . 2005 . “T‐cell receptor triggering is critically dependent on the dimensions of its peptide‐MHC ligand.” . Nature (London) , 436 : 578 – 582 .
  • del Rio , A , Perez‐Jimenez , R , Liu , R , Roca‐Cusachs , P , Fernandez , JM and Sheetz , MP . 2009 . “Stretching single talin rod molecules activates vinculin binding.” . Science , 323 : 638 – 641 .
  • Delon , J and Germain , RN . 2000 . “Information transfer at the immunological synapse.” . Curr. Biol. , 10 : R923 – 933 .
  • Delon , J , Kaibuchi , K and Germain , RN . 2001 . “Exclusion of CD43 from the immunological synapse is mediated by phosphorylation‐regulated relocation of the cytoskeletal adaptor moesin.” . Immunity , 15 : 691 – 701 .
  • DeMond , AL , Mossman , KD , Starr , T , Dustin , ML and Groves , JT . 2008 . “T‐cell receptor microcluster transport through molecular mazes reveals mechanism of translocation.” . Biophys. J. , 94 : 3286 – 3292 .
  • DeMond , AL , Starr , T , Dustin , ML and Groves , JT . 2006 . “Control of antigen presentation with a photoreleasable agonist peptide.” . J. Am. Chem. Soc. , 128 : 15354 – 15355 .
  • Dustin , ML . 2008 . “T‐cell activation through immunological synapses and kinapses.” . Immunol. Rev. , 221 : 77 – 89 .
  • Dustin , ML and Zhu , C . 2006 . “T cells like a firm molecular handshake.” . Proc. Natl. Acad. Sci. U.S.A. , 103 : 4335 – 4336 .
  • Eisen , HN , Sykulev , Y and Tsomides , TJ . 1996 . “Antigen‐specific T‐cell receptors and their reactions with complexes formed by peptides with major histocompatibility complex proteins.” . Adv. Protein Chem. , 49 : 1 – 56 .
  • Evans , E . 2001 . “Probing the relation between force—lifetime—and chemistry in single molecular bonds.” . Annu. Rev. Biophys. Biomol. Struct. , 30 : 105 – 128 .
  • Evans , E and Kinoshita , K . 2007 . “Using force to probe single‐molecule receptor‐cytoskeletal anchoring beneath the surface of a living cell.” . Methods Cell Biol. , 83 : 373 – 396 .
  • Evans , E and Ritchie , K . 1997 . “Dynamic strength of molecular adhesion bonds.” . Biophys. J. , 72 : 1541 – 1555 .
  • Evans , E , Ritchie , K and Merkel , R . 1995 . “Sensitive force technique to probe molecular adhesion and structural linkages at biological interfaces.” . Biophys. J. , 68 : 2580 – 2587 .
  • Evans , EA and Calderwood , DA . 2007 . “Forces and bond dynamics in cell adhesion.” . Science , 316 : 1148 – 1153 .
  • Falconnet , D , Csucs , G , Grandin , HM and Textor , M . 2006 . “Surface engineering approaches to micropattern surfaces for cell‐based assays.” . Biomaterials , 27 : 3044 – 3063 .
  • Fernandez‐Miguel , G , Alarcon , B , Iglesias , A , Bluethmann , H , Alvarez‐Mon , M , Sanz , E and de la Hera , A . 1999 . “Multivalent structure of an alphabeta T‐cell receptor.” . Proc. Natl. Acad. Sci. U.S.A. , 96 : 1547 – 1552 .
  • Förster , T . 1946 . “Energiewanderung und fluoreszenz.” . Naturwiss. , 33 : 166 – 175 .
  • Förster , T . 1960 . “Transfer mechanisms of electronic excitation energy.” . Radiat. Res. Suppl. , 2 : 326 – 339 .
  • Giepmans , BN , Adams , SR , Ellisman , MH and Tsien , RY . 2006 . “The fluorescent toolbox for assessing protein location and function.” . Science , 312 : 217 – 224 .
  • Gil , D , Schamel , WW , Montoya , M , Sanchez‐Madrid , F and Alarcon , B . 2002 . “Recruitment of Nck by CD3 epsilon reveals a ligand‐induced conformational change essential for T‐cell receptor signaling and synapse formation.” . Cell , 109 : 901 – 912 .
  • Gil , D , Schrum , AG , Alarcon , B and Palmer , E . 2005 . “T‐cell receptor engagement by peptide‐MHC ligands induces a conformational change in the CD3 complex of thymocytes.” . J. Exp. Med. , 201 : 517 – 522 .
  • Gomez , TS and Billadeau , DD . 2008 . “T‐cell activation and the cytoskeleton: you can't have one without the other.” . Adv. Immunol. , 97 : 1 – 64 .
  • Grakoui , A , Bromley , SK , Sumen , C , Davis , MM , Shaw , AS , Allen , PM and Dustin , ML . 1999a . “The immunological synapse: a molecular machine controlling T‐cell activation.” . Science , 285 : 221 – 227 .
  • Grakoui , A , Donermeyer , DL , Kanagawa , O , Murphy , KM and Allen , PM . 1999b . “TCR‐independent pathways mediate the effects of antigen dose and altered peptide ligands on T‐cell polarization.” . J. Immunol. , 162 : 1923 – 1930 .
  • Groves , JT , Ulman , N and Boxer , SG . 1997 . “Micropatterning fluid lipid bilayers on solid supports.” . Science , 275 : 651 – 653 .
  • Gustafsson , MG . 2008 . “Super‐resolution light microscopy goes live.” . Nat. Methods , 5 : 385 – 387 .
  • Gustafsson , MG , Shao , L , Carlton , PM , Wang , CJ , Golubovskaya , IN , Cande , WZ , Agard , DA and Sedat , JW . 2008 . “Three‐dimensional resolution doubling in wide‐field fluorescence microscopy by structured illumination.” . Biophys. J. , 94 : 4957 – 4970 .
  • Hess , ST , Girirajan , TP and Mason , MD . 2006 . “Ultra‐high resolution imaging by fluorescence photoactivation localization microscopy.” . Biophys. J. , 91 : 4258 – 4272 .
  • Hess , ST , Gould , TJ , Gunewardene , M , Bewersdorf , J and Mason , MD . 2009 . “Ultrahigh resolution imaging of biomolecules by fluorescence photoactivation localization microscopy.” . Methods Mol. Biol. , 544 : 483 – 522 .
  • Irles , C , Symons , A , Michel , F , Bakker , TR , van der Merwe , PA and Acuto , O . 2003 . “CD45 ectodomain controls interaction with GEMs and Lck activity for optimal TCR signaling.” . Nat. Immunol. , 4 : 189 – 197 .
  • Irvine , DJ , Doh , J and Huang , B . 2007 . “Patterned surfaces as tools to study ligand recognition and synapse formation by T cells.” . Curr. Opin. Immunol. , 19 : 463 – 469 .
  • Irvine , DJ , Purbhoo , MA , Krogsgaard , M and Davis , MM . 2002 . “Direct observation of ligand recognition by T cells.” . Nature (London) , 419 : 845 – 849 .
  • Janmey , PA and McCulloch , CA . 2007 . “Cell mechanics: integrating cell responses to mechanical stimuli.” . Annu. Rev. Biomed. Eng. , 9 : 1 – 34 .
  • Jares‐Erijman , EA and Jovin , TM . 2003 . “FRET imaging.” . Nat. Biotechnol. , 21 : 1387 – 1395 .
  • Ji , N , Shroff , H , Zhong , H and Betzig , E . 2008 . “Advances in the speed and resolution of light microscopy.” . Curr. Opin. Neurobiol. , 18 : 605 – 616 .
  • Kaizuka , Y , Douglass , AD , Varma , R , Dustin , ML and Vale , RD . 2007 . “Mechanisms for segregating T‐cell receptor and adhesion molecules during immunological synapse formation in Jurkat T cells.” . Proc. Natl. Acad. Sci. U.S.A. , 104 : 20296 – 20301 .
  • Kalergis , AM , Boucheron , N , Doucey , MA , Palmieri , E , Goyarts , EC , Vegh , Z , Luescher , IF and Nathenson , SG . 2001 . “Efficient T‐cell activation requires an optimal dwell‐time of interaction between the TCR and the pMHC complex.” . Nat. Immunol. , 2 : 229 – 234 .
  • Kerppola , TK . 2008 . “Bimolecular fluorescence complementation (BiFC) analysis as a probe of protein interactions in living cells.” . Ann. Rev. Biophys. , 37 : 465 – 487 .
  • Krogsgaard , M , Huppa , JB , Purbhoo , MA and Davis , MM . 2003 . “Linking molecular and cellular events in T‐cell activation and synapse formation.” . Semin Immunol. , 15 : 307 – 315 .
  • Krogsgaard , M , Li , QJ , Sumen , C , Huppa , JB , Huse , M and Davis , MM . 2005 . “Agonist/endogenous peptide‐MHC heterodimers drive T‐cell activation and sensitivity.” . Nature (London) , 434 : 238 – 243 .
  • Krummel , MF , Sjaastad , MD , Wulfing , C and Davis , MM . 2000 . “Differential clustering of CD4 and CD3zeta during T‐cell recognition.” . Science , 289 : 1349 – 1352 .
  • Lee , SJ , Hori , Y , Groves , JT , Dustin , ML and Chakraborty , AK . 2002 . “Correlation of a dynamic model for immunological synapse formation with effector functions: two pathways to synapse formation.” . Trends Immunol. , 23 : 492 – 499 .
  • Levitt , JA , Matthews , DR , Ameer‐Beg , SM and Suhling , K . 2009 . “Fluorescence lifetime and polarization‐resolved imaging in cell biology.” . Curr. Opin. Biotechnol. , 20 : 28 – 36 .
  • Linke , WA and Grutzner , A . 2008 . “Pulling single molecules of tit in by AFM—recent advances and physiological implications.” . Pfluegers Arch. Eur. J. Physiol. , 456 : 101 – 115 .
  • Ma , Z , Janmey , PA and Finkel , TH . 2007 . “The receptor deformation model of TCR triggering.” . FASEB J. , 22 : 1002 – 1008 .
  • Ma , Z , Sharp , KA , Janmey , PA and Finkel , TH . 2008 . “Surface‐anchored monomeric agonist pMHCs alone trigger TCR with high sensitivity.” . PLoS Biol. , 6 : e43
  • Martinez‐Martin , N , Risueno , RM , Morreale , A , Zaldivar , I , Fernandez‐Arenas , E , Herranz , F , Ortiz , AR and Alarcon , B . 2009 . “Cooperativity between T‐cell receptor complexes revealed by conformational mutants of CD3epsilon.” . Sci. Signal. , 2 : ra43
  • Mazza , G , Housset , D , Piras , C , Gregoire , C , Lin , SY , Fontecilla‐Camps , JC and Malissen , B . 1998 . “Glimpses at the recognition of peptide/MHC complexes by T‐cell antigen receptors.” . Immunol. Rev. , 163 : 187 – 196 .
  • McKeithan , TW . 1995 . “Kinetic proofreading in T‐cell receptor signal transduction.” . Proc. Natl. Acad. Sci. U.S.A. , 92 : 5042 – 5046 .
  • Merkel , R , Nassoy , P , Leung , A , Ritchie , K and Evans , E . 1999 . “Energy landscapes of receptor‐ligand bonds explored with dynamic force spectroscopy.” . Nature (London) , 397 : 50 – 53 .
  • Mingueneau , M , Sansoni , A , Gregoire , C , Roncagalli , R , Aguado , E , Weiss , A , Malissen , M and Malissen , B . 2008 . “The proline‐rich sequence of CD3epsilon controls T‐cell antigen receptor expression on and signaling potency in preselection CD4+CD8+ thymocytes.” . Nat. Immunol. , 9 : 522 – 532 .
  • Minguet , S and Schamel , WW . 2008 . “A permissive geometry model for TCR‐CD3 activation.” . Trends Biochem. Sci. , 33 : 51 – 57 .
  • Monks , CR , Freiberg , BA , Kupfer , H , Sciaky , N and Kupfer , A . 1998 . “Three‐dimensional segregation of supramolecular activation clusters in T cells.” . Nature (London) , 395 : 82 – 86 .
  • Mossman , KD , Campi , G , Groves , JT and Dustin , ML . 2005 . “Altered TCR signaling from geometrically repatterned immunological synapses.” . Science , 310 : 1191 – 1193 .
  • Muller , DJ , Helenius , J , Alsteens , D and Dufrene , YF . 2009 . “Force probing surfaces of living cells to molecular resolution.” . Nat. Chem. Biol. , 5 : 383 – 390 .
  • Negulescu , PA , Krasieva , TB , Khan , A , Kerschbaum , HH and Cahalan , MD . 1996 . “Polarity of T‐cell shape, motility, and sensitivity to antigen.” . Immunity , 4 : 421 – 430 .
  • Nguyen , AW and Daugherty , PS . 2005 . “Evolutionary optimization of fluorescent proteins for intracellular FRET.” . Nat. Biotechnol. , 23 : 355 – 360 .
  • Paul , WE and Seder , RA . 1994 . “Lymphocyte responses and cytokines.” . Cell , 76 : 241 – 251 .
  • Qi , S , Krogsgaard , M , Davis , MM and Chakraborty , AK . 2006 . “Molecular flexibility can influence the stimulatory ability of receptor‐ligand interactions at cell‐cell junctions.” . Proc. Natl. Acad. Sci. U.S.A. , 103 : 4416 – 4421 .
  • Qi , SY , Groves , JT and Chakraborty , AK . 2001 . “Synaptic pattern formation during cellular recognition.” . Proc. Natl. Acad. Sci. U.S.A. , 98 : 6548 – 6553 .
  • Rabinowitz , JD , Beeson , C , Lyons , DS , Davis , MM and McConnell , HM . 1996 . “Kinetic discrimination in T‐cell activation.” . Proc. Natl. Acad. Sci. U.S.A. , 93 : 1401 – 1405 .
  • Reich , Z , Boniface , JJ , Lyons , DS , Borochov , N , Wachtel , EJ and Davis , MM . 1997 . “Ligand‐specific oligomerization of T‐cell receptor molecules.” . Nature (London) , 387 : 617 – 620 .
  • Roumier , A , Olivo‐Marin , JC , Arpin , M , Michel , F , Martin , M , Mangeat , P , Acuto , O , Dautry‐Varsat , A and Alcover , A . 2001 . “The membrane‐microfilament linker ezrin is involved in the formation of the immunological synapse and in T‐cell activation.” . Immunity , 15 : 715 – 728 .
  • Rudolph , MG , Stanfield , RL and Wilson , IA . 2006 . “HowTCRs bind MHCs, peptides, and coreceptors.” . Annu. Rev. Immunol. , 24 : 419 – 466 .
  • Schermelleh , L . 2008 . “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy.” . Science , 320 : 1332 – 1336 .
  • Schultz , C . 2007 . “Molecular tools for cells and systems biology.” . HFSP J. , 1 (4) : 230 – 248 .
  • Smith‐Garvin , JE , Koretzky , GA and Jordan , MS . 2009 . “T‐cell activation.” . Annu. Rev. Immunol. , 27 : 591 – 619 .
  • Sun , ZJ , Kim , KS , Wagner , G and Reinherz , EL . 2001 . “Mechanisms contributing to T‐cell receptor signaling and assembly revealed by the solution structure of an ectodomain fragment of the CD3 epsilon gamma heterodimer.” . Cell , 105 : 913 – 923 .
  • Sykulev , Y , Joo , M , Vturina , I , Tsomides , TJ and Eisen , HN . 1996 . “Evidence that a single peptide‐MHC complex on a target cell can elicit a cytolytic T‐cell response.” . Immunity , 4 : 565 – 571 .
  • Tolentino , TP , Wu , J , Zarnitsyna , VI , Fang , Y , Dustin , ML and Zhu , C . 2008 . “Measuring diffusion and binding kinetics by contact area FRAP.” . Biophys. J. , 95 : 920 – 930 .
  • Torres , AJ , Wu , M , Holowka , D and Baird , B . 2008 . “Nanobiotechnology and cell biology: micro‐ and nanofabricated surfaces to investigate receptor‐mediated signaling.” . Ann. Rev. Biophys. , 37 : 265 – 288 .
  • Trautmann , A and Randriamampita , C . 2003 . “Initiation of TCR signalling revisited.” . Trends Immunol. , 24 : 425 – 428 .
  • Valitutti , S and Lanzavecchia , A . 1997 . “Serial triggering of TCRs: a basis for the sensitivity and specificity of antigen recognition.” . Immunol. Today , 18 : 299 – 304 .
  • Valitutti , S , Muller , S , Cella , M , Padovan , E and Lanzavecchia , A . 1995 . “Serial triggering of many T‐cell receptors by a few peptide‐MHC complexes.” . Nature (London) , 375 : 148 – 151 .
  • van der Merwe , PA . 2001 . “The TCR triggering puzzle.” . Immunity , 14 : 665 – 668 .
  • Varma , R . 2008 . “TCR triggering by the pMHC complex: valency, affinity, and dynamics.” . Sci. Signal. , 1 : pe21
  • Vilardaga , JP , Bunemann , M , Krasel , C , Castro , M and Lohse , MJ . 2003 . “Measurement of the millisecond activation switch of G protein‐coupled receptors in living cells.” . Nat. Biotechnol. , 21 : 807 – 812 .
  • Voldman , J , Gray , ML and Schmidt , MA . 1999 . “Microfabrication in biology and medicine.” . Annu. Rev. Biomed. Eng. , 1 : 401 – 425 .
  • Wallrabe , H and Periasamy , A . 2005 . “Imaging protein molecules using FRET andFLIM microscopy.” . Curr. Opin. Biotechnol. , 16 : 19 – 27 .
  • Wedagedera , JR and Burroughs , NJ . 2006 . “T‐cell activation: a queuing theory analysis at low agonist density.” . Biophys. J. , 91 : 1604 – 1618 .
  • Wu , J , Fang , Y , Zarnitsyna , VI , Tolentino , TP , Dustin , ML and Zhu , C . 2008 . “A coupled diffusion‐kinetics model for analysis of contact‐area FRAP experiment.” . Biophys. J. , 95 : 910 – 919 .
  • Wulfing , C and Davis , MM . 1998 . “A receptor/cytoskeletal movement triggered by costimulation during T‐cell activation.” . Science , 282 : 2266 – 2269 .
  • Xiong , Y , Lee , AC , Suter , DM and Lee , GU . 2009 . “Topography and nanomechanics of live neuronal growth cones analyzed by atomic force microscopy.” . Biophys. J. , 96 : 5060 – 5072 .
  • Xu , C , Gagnon , E , Call , ME , Schnell , JR , Schwieters , CD , Carman , CV , Chou , JJ and Wucherpfennig , KW . 2008 . “Regulation of T‐cell receptor activation by dynamic membrane binding of the CD3epsilon cytoplasmic tyrosine‐based motif.” . Cell , 135 : 702 – 713 .
  • Zal , T and Gascoigne , NR . 2004 . “Using live FRET imaging to reveal early protein‐protein interactions during T‐cell activation.” . Curr. Opin. Immunol. , 16 : 674 – 683 .
  • Zal , T , Zal , MA and Gascoigne , NR . 2002 . “Inhibition of T‐cell receptor‐coreceptor interactions by antagonist ligands visualized by live FRET imaging of the T‐hybridoma immunological synapse.” . Immunity , 16 : 521 – 534 .
  • Zhu , DM , Dustin , ML , Cairo , CW and Golan , DE . 2007 . “Analysis of two‐dimensional dissociation constant of laterally mobile cell adhesion molecules.” . Biophys. J. , 92 : 1022 – 1034 .

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