NSOM/QD-based direct visualization of CD3-induced and CD28-enhanced nanospatial coclustering of TCR and coreceptor in nanodomains in T cell activation

PLoS ONE

Volumn 4, Issue 6, 2009, Pages

  Zhong, Liyun ^a   Zeng, Gucheng ^a   Lu, Xiaoxu ^b   Wang, Richard C ^a   Gong, Guangming ^a   Yan, Lin ^a   Huang, Dan ^a   Chen, Zheng W ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b SOUTH CHINA NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CD3 ANTIGEN; CD3 ANTIGEN RECEPTOR; CD4 ANTIGEN RECEPTOR; CD8 ANTIGEN RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR; PROTEIN KINASE LCK; QUANTUM DOT; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; CD4 ANTIGEN; CD8 ANTIGEN; NANOPARTICLE;

ANIMAL CELL; ANTIBODY LABELING; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; MAJOR HISTOCOMPATIBILITY COMPLEX; NANOIMAGING; NANOTECHNOLOGY; NONHUMAN; PROTEIN PROTEIN INTERACTION; SCANNING NEAR FIELD OPTICAL MICROSCOPY; T LYMPHOCYTE ACTIVATION; ANIMAL; BIOSYNTHESIS; CHEMISTRY; CLUSTER ANALYSIS; COMPUTER PROGRAM; IMAGE PROCESSING; LYMPHOCYTE ACTIVATION; MACACA; METABOLISM; METHODOLOGY;

ANIMALS; ANTIGENS, CD28; ANTIGENS, CD3; ANTIGENS, CD4; ANTIGENS, CD8; CLUSTER ANALYSIS; IMAGE PROCESSING, COMPUTER-ASSISTED; LYMPHOCYTE ACTIVATION; MACACA MULATTA; NANOPARTICLES; NANOTECHNOLOGY; QUANTUM DOTS; RECEPTORS, ANTIGEN, T-CELL; SOFTWARE;

EID: 67650178399     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005945     Document Type: Article

References (59)

1. Davis MM, Boniface JJ, Reich Z, Lyons D, Hampl J, et al. (1998) Ligand recognition by alpha beta T cell receptors. Annu Rev Immunol 16: 523-544.
2. Gascoigne NR, Zal T, Alam SM (2001) T-cell receptor binding kinetics in T-cell development and activation. Expert Rev Mol Med. pp 1-17.
3. Krogsgaard M, Li QJ, Sumen C, Huppa JB, Huse M, et al. (2005) Agonist/ endogenous peptide-MHC heterodimers drive T cell activation and sensitivity. Nature 434: 238-243.
4. Wulfing C, Sumen C, Sjaastad MD, Wu LC, Dustin ML, et al. (2002) Costimulation and endogenous MHC ligands contribute to T cell recognition. Nat Immunol 3: 42-47.
5. Zamoyska R (1998) CD4 and CD8: modulators of T-cell receptor recognition of antigen and of immune responses? Curr Opin Immunol 10: 82-87.
6. Potter TA, Rajan TV, Dick RF 2nd, Bluestone JA (1989) Substitution at residue 227 of H-2 class I molecules abrogates recognition by CD8-dependent, but not CD8-independent, cytotoxic T lymphocytes. Nature 337: 73-75.
7. Madrenas J, Chau LA, Smith J, Bluestone JA, Germain RN (1997) The efficiency of CD4 recruitment to ligand-engaged TCR controls the agonist/ partial agonist properties of peptide-MHC molecule ligands. J Exp Med 185: 219-229.
8. Janeway CA Jr (1992) The T cell receptor as a multicomponent signalling machine: CD4/CD8 coreceptors and CD45 in T cell activation. Annu Rev Immunol 10: 645-674.
9. Wyer JR, Willcox BE, Gao GF, Gerth UC, Davis SJ, et al. (1999) T cell receptor and coreceptor CD8 alphaalpha bind peptide-MHC independently and with distinct kinetics. Immunity 10: 219-225.
10. Arcaro A, Gregoire C, Bakker TR, Baldi L, Jordan M, et al. (2001) CD8beta endows CD8 with efficient coreceptor function by coupling T cell receptor/CD3 to raft-associated CD8/p56(lck) complexes. J Exp Med 194: 1485-1495.
11. Krummel MF, Sjaastad MD, Wulfing C, Davis MM(2000) Differential clustering of CD4 and CD3zeta during T cell recognition. Science 289: 1349-1352.
12. Xavier R, Brennan T, Li Q, McCormack C, Seed B (1998) Membrane compartmentation is required for efficient T cell activation. Immunity 8: 723-732.
13. Block MS, Johnson AJ, Mendez-Fernandez Y, Pease LR (2001) Monomeric class I molecules mediate TCR/CD3 epsilon/CD8 interaction on the surface of T cells. J Immunol 167: 821-826.
14. Doucey MA, Goffin L, Naeher D, Michielin O, Baumgartner P, et al. (2003) CD3 delta establishes a functional link between the T cell receptor and CD8. J Biol Chem 278: 3257-3264.
15. Yachi PP, Ampudia J, Gascoigne NR, Zal T (2005) Nonstimulatory peptides contribute to antigen-induced CD8-T cell receptor interaction at the immunological synapse. Nat Immunol 6: 785-792.
16. Zal T, Zal MA, 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.
17. Betzig E, Chichester RJ (1993) Single Molecules Observed by Near-Field Scanning Optical Microscopy. Science 262: 1422-1425.
18. Dunn RC (1999) Near-field scanning optical microscopy. Chem Rev 99: 2891-2928.
19. Lewis A, Taha H, Strinkovski A, Manevitch A, Khatchatouriants A, et al. (2003) Near-field optics: from subwavelength illumination to nanometric shadowing. Nat Biotechnol 21: 1378-1386.
20. Tokumasu F, Hwang J, Dvorak JA (2004) Heterogeneous molecular distribution in supported multicomponent lipid bilayers. Langmuir 20: 614-618.
21. Teetsov J, Vanden Bout DA (2000) Near-field scanning optical microscopy (NSOM) studies of nanoscale polymer ordering in pristine films of poly(9,9-dialkylfluorene). Journal of Physical Chemistry B 104: 9378-9387.
22. Ozcan A, Cubukcu E, Bilenca A, Crozier KB, Bouma BE, et al. (2006) Differential near-field scanning optical microscopy. Nano Lett 6: 2609-2616.
23. Chan WC, Nie S (1998) Quantum dot bioconjugates for ultrasensitive nonisotopic detection. Science 281: 2016-2018.
24. Chen Y, Shao L, Ali Z, Cai J, Chen ZW (2008) NSOM/QD-based nanoscale immunofluorescence imaging of antigen-specific T-cell receptor responses during an in vivo clonal V{gamma}2V{delta}2 T-cell expansion. Blood 111: 4220-4232.
25. Zeng G, Chen J, Zhong L, Wang R, Jiang L, et al. (2009) NSOM- and AFM-based nanotechnology elucidates nano-structural and atomic-force features of a Y. pestis V immunogen-containing particle vaccine capable of eliciting robust response. Proteomics 9: 1538-1547.
26. Chen Y, Qin J, Chen ZW (2008) Fluorescence-topographic NSOM directly visualizes peak-valley polarities of GM1/GM3 rafts in cell membrane fluctuations. J Lipid Res 49: 2268-2275.
27. Chen Y, Qin J, Cai J, Chen ZW (2009) Cold induces micro- and nano-scale reorganization of lipid raft markers at mounds of T-cell membrane fluctuations. PLoS ONE 4: e5386.
28. Ianoul A, Grant DD, Rouleau Y, Bani-Yaghoub M, Johnston LJ, et al. (2005) Imaging nanometer domains of beta-adrenergic receptor complexes on the surface of cardiac myocytes. Nat Chem Biol 1: 196-202.
29. de Bakker BI, Bodnar A, van Dijk EM, Vamosi G, Damjanovich S, et al. (2008) Nanometer-scale organization of the alpha subunits of the receptors for IL2 and IL15 in human T lymphoma cells. J Cell Sci 121: 627-633.
30. Enderle T, Ha T, Ogletree DF, Chemla DS, Magowan C, et al. (1997) Membrane specific mapping and colocalization of malarial and host skeletal proteins in the Plasmodium falciparum infected erythrocyte by dual-color near-field scanning optical microscopy. Proc Natl Acad Sci U S A 94: 520-525.
31. Alarcon B, Swamy M, van Santen HM, Schamel WW (2006) T-cell antigen-receptor stoichiometry: pre-clustering for sensitivity. EMBO Rep 7: 490-495.
32. Purtic B, Pitcher LA, van Oers NS, Wulfing C (2005) T cell receptor (TCR) clustering in the immunological synapse integrates TCR and costimulatory signaling in selected T cells. Proc Natl Acad Sci U S A 102: 2904-2909.
33. 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.
34. Varma R, Campi G, Yokosuka T, Saito T, Dustin ML (2006) T cell receptor-proximal signals are sustained in peripheral microclusters and terminated in the central supramolecular activation cluster. Immunity 25: 117-127.
35. Alegre ML, Frauwirth KA, Thompson CB (2001) T-cell regulation by CD28 and CTLA-4. Nat Rev Immunol 1: 220-228.
36. Sharpe AH, Freeman GJ (2002) The B7-CD28 superfamily. Nat Rev Immunol 2: 116-126.
37. Acuto O, Michel F (2003) CD28-mediated co-stimulation: a quantitative support for TCR signalling. Nat Rev Immunol 3: 939-951.
38. Linsley PS, Ledbetter JA (1993) The role of the CD28 receptor during T cell responses to antigen. Annu Rev Immunol 11: 191-212.
39. Lenschow DJ, Walunas TL, Bluestone JA (1996) CD28/B7 system of T cell costimulation. Annu Rev Immunol 14: 233-258.
40. Chen L (2004) Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity. Nat Rev Immunol 4: 336-347.
41. Zapata DA, Schamel WW, Torres PS, Alarcon B, Rossi NE, et al. (2004) Biochemical differences in the alphabeta T cell receptor.CD3 surface complex between CD8+ and CD4+ human mature T lymphocytes. J Biol Chem 279: 24485-24492.
42. Garcia KC, Scott CA, Brunmark A, Carbone FR, Peterson PA, et al. (1996) CD8 enhances formation of stable T-cell receptor/MHC class I molecule complexes. Nature 384: 577-581.
43. Crawford F, Kozono H, White J, Marrack P, Kappler J (1998) Detection of antigen-specific T cells with multivalent soluble class II MHC covalent peptide complexes. Immunity 8: 675-682.
44. Cui B, Wu C, Chen L, Ramirez A, Bearer EL, et al. (2007) One at a time, live tracking of NGF axonal transport using quantum dots. Proc Natl Acad Sci U S A 104: 13666-13671.
45. Jouvenet N, Bieniasz PD, Simon SM (2008) Imaging the biogenesis of individual HIV-1 virions in live cells. Nature 454: 236-240.
46. Douglass AD, Vale RD (2005) Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 121: 937-950.
47. Billadeau DD, Nolz JC, Gomez TS (2007) Regulation of T-cell activation by the cytoskeleton. Nat Rev Immunol 7: 131-143.
48. Yachi PP, Ampudia J, Zal T, Gascoigne NR (2006) Altered peptide ligands induce delayed CD8-T cell receptor interaction-a role for CD8 in distinguishing antigen quality. Immunity 25: 203-211.
49. Iezzi G, Karjalainen K, Lanzavecchia A (1998) The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity 8: 89-95.
50. Viola A, Schroeder S, Sakakibara Y, Lanzavecchia A (1999) T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science 283: 680-682.
51. Shen K, Thomas VK, Dustin ML, Kam LC (2008) Micropatterning of costimulatory ligands enhances CD4+ T cell function. Proc Natl Acad Sci U S A 105: 7791-7796.
52. Tavano R, Contento RL, Baranda SJ, Soligo M, Tuosto L, et al. (2006) CD28 interaction with filamin-A controls lipid raft accumulation at the T-cell immunological synapse. Nat Cell Biol 8: 1270-1276.
53. Tavano R, Gri G, Molon B, Marinari B, Rudd CE, et al. (2004) CD28 and lipid rafts coordinate recruitment of Lck to the immunological synapse of human T lymphocytes. J Immunol 173: 5392-5397.
54. Sykulev Y, Joo M, Vturina I, Tsomides TJ, 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.
55. 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.
56. Bosselut R, Zhang W, Ashe JM, Kopacz JL, Samelson LE, et al. (1999) Association of the adaptor molecule LAT with CD4 and CD8 coreceptors identifies a new coreceptor function in T cell receptor signal transduction. J Exp Med 190: 1517-1526.
57. Shen Y, Zhou D, Qiu L, Lai X, Simon M, et al. (2002) Adaptive immune response of Vgamma2Vdelta2+ T cells during mycobacterial infections. Science 295: 2255-2258.
58. Gong G, Shao L, Wang Y, Chen CY, Huang D, Zhan X, Yao S, Chen ZW (2008) Phosphoantigen-activated Vgamma2Vdelta2+ T cells antagonize IL-2-induced CD4+CD25+Foxp3+ T regulatory Cells. Blood.
59. Zeng G, Yang P, Zheng Z, Feng Q, Cai J, et al. (2005) Nanostructures and molecular force bases of a highly sensitive capacitive immunosensor. Proteomics 5: 4347-4353.