Spatiotemporal patterning during T cell activation is highly diverse

Science Signaling

Volumn 2, Issue 65, 2009, Pages

  Singleton, Kentner L ^a   Roybal, Kole T ^a   Sun, Yi ^a   Fu, Guo ^b   Gascoigne, Nicholas R J ^b   Van Oers, Nicolai S C ^a   Wülfing, Christoph ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CD2 ANTIGEN; CD28 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; GREEN FLUORESCENT PROTEIN; INTERLEUKIN 2; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOLIPASE C GAMMA; PROTEIN CDC42; PROTEIN KINASE C; PROTEIN KINASE ZAP 70; RAC PROTEIN; RHO FACTOR; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR NFAT; LYMPHOCYTE ANTIGEN RECEPTOR; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTING CELL; ARTICLE; BIOCHEMISTRY; CYTOSKELETON; IMAGE ANALYSIS; IMAGE DISPLAY; MICROTUBULE ORGANIZING CENTER; MOUSE; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPATIAL DISCRIMINATION; T LYMPHOCYTE ACTIVATION; TEMPORAL CORTEX; TRANSGENIC MOUSE; ANIMAL; COMPARATIVE STUDY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; T LYMPHOCYTE; WESTERN BLOTTING;

ANIMALS; ANTIGEN-PRESENTING CELLS; BLOTTING, WESTERN; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOCYTE ACTIVATION; MICE; MICE, TRANSGENIC; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 66149112471     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2000199     Document Type: Article

References (59)

1. J. M. Kavran, D. E. Klein, A. Lee, M. Falasca, S. J. Isakoff, E. Y. Skolnik, M. A. Lemmon, Specificity and promiscuity in phosphoinositide binding by pleckstrin homology domains. J. Biol. Chem. 273, 30497-30508 (1998).
2. Z. Songyang, S. E. Shoelson, M. Chaudhuri, G. Gish, T. Pawson, W. G. Haser, F. King, T. Roberts, S. Ratnofsky, R. J. Lechleider, B. G. Neel, R. B. Birge, J. E. Fajardo, M. M. Chou, H. Hanafusa, B. Schaffhausen, L. C. Cantley, SH2 domains recognize specific phosphopeptide sequences. Cell 72, 767-778 (1993).
3. S. Feng, C. Kasahara, R. J. Rickles, S. L. Schreiber, Specific interactions outside the proline-rich core of two classes of Src homology 3 ligands. Proc. Natl. Acad. Sci. U.S.A. 92, 12408-12415 (1995).
4. T. Pawson, P. Nash, Assembly of cell regulatory systems through protein interaction domains. Science 300, 445-452 (2003).
5. R. T. Alexander, W. Furuya, K. Szászi, J. Orlowski, S. Grinstein, Rho GTPases dictate the mobility of the Na/H exchanger NHE3 in epithelia: Role in apical retention and targeting. Proc. Natl. Acad. Sci. U.S.A. 102, 12253-12258 (2005).
6. J. T. Chang, V. R. Palanivel, I. Kinjyo, F. Schambach, A. M. Intlekofer, A. Banerjee, S. A. Longworth, K. E. Vinup, P. Mrass, J. Oliaro, N. Killeen, J. S. Orange, S. M. Russell, W. Weninger, S. L. Reiner, Asymmetric T lymphocyte division in the initiation of adaptive immune responses. Science 315, 1687-1691 (2007).
7. F. Martin-Belmonte, A. Gassama, A. Datta, W. Yu, U. Rescher, V. Gerke, K. Mostov, PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128, 383-397 (2007).
8. N. Osmani, N. Vitale, J. P. Borg, S. Etienne-Manneville, Scrib controls Cdc42 localization and activity to promote cell polarization during astrocyte migration. Curr. Biol. 16, 2395-2405 (2006).
9. A. Van Keymeulen, K. Wong, Z. A. Knight, C. Govaerts, K. M. Hahn, K. M. Shokat, H. R. Bourne, To stabilize neutrophil polarity, PIP3 and Cdc42 augment RhoA activity at the back as well as signals at the front. J. Cell Biol. 174, 437-445 (2006).
10. K. Y. Wu, U. Hengst, L. J. Cox, E. Z. Macosko, A. Jeromin, E. R. Urquhart, S. R. Jaffrey, Local translation of RhoA regulates growth cone collapse. Nature 436, 1020-1024 (2005).
11. A. Malliri, J. G. Collard, Role of Rho-family proteins in cell adhesion and cancer. Curr. Opin. Cell Biol. 15, 583-589 (2003).
12. Q. Gong, A. M. Cheng, A. M. Akk, J. Alberola-Ila, G. Gong, T. Pawson, A. C. Chan, Disruption of T cell signaling networks and development by Grb2 haploid insufficiency. Nat. Immunol. 2, 29-36 (2001).
13. R. J. Cornall, J. G. Cyster, M. L. Hibbs, A. R. Dunn, K. L. Otipoby, E. A. Clark, C. C. Goodnow, Polygenic autoimmune traits: Lyn, CD22, and SHP-1 are limiting elements of a biochemical pathway regulating BCR signaling and selection. Immunity 8, 497-508 (1998).
14. A. B. Satterthwaite, F. Willis, P. Kanchanastit, D. Fruman, L. C. Cantley, C. D. Helgason, R. K. Humphries, C. A. Lowell, M. Simon, M. Leitges, A. Tarakhovsky, T. F. Tedder, R. Lesche, H. Wu, O. N. Witte, A sensitized genetic system for the analysis of murine B lymphocyte signal transduction pathways dependent on Bruton's tyrosine kinase. Proc. Natl. Acad. Sci. U.S.A. 97, 6687-6692 (2000).
15. M. M. Davis, J. J. Boniface, Z. Reich, D. Lyons, J. Hampl, B. Arden, Y. Chien, Ligand recognition by ab T cell receptors. Annu. Rev. Immunol. 16, 523-544 (1998).
16. S. J. Davis, S. Ikemizu, E. J. Evans, L. Fugger, T. R. Bakker, P. A. van der Merwe, The nature of molecular recognition by T cells. Nat. Immunol. 4, 217-224 (2003).
17. J. Sprent, Presidential address to the American Association of Immunologists. Stimulating naive T cells. J. Immunol. 163, 4629-4636 (1999).
18. P. A. Negulescu, T. B. Krasieva, A. Khan, H. H. Kerschbaum, M. D. Cahalan, Polarity of T cell shape, motility, and sensitivity to antigen. Immunity 4, 421-430 (1996).
19. S. H. Wei, O. Safrina, Y. Yu, K. R. Garrod, M. D. Cahalan, I. Parker, Ca2+ signals in CD4+ T cells during early contacts with antigen-bearing dendritic cells in lymph node. J. Immunol. 179, 1586-1594 (2007).
20. J. Jacobelli, P. G. Andres, J. Boisvert, M. F. Krummel, New views of the immunological synapse: Variations in assembly and function. Curr. Opin. Immunol. 16, 345-352 (2004).
21. M. L. Dustin, T-cell activation through immunological synapses and kinapses. Immunol. Rev. 221, 77-89 (2008).
22. C. R. Monks, H. Kupfer, I. Tamir, A. Barlow, A. Kupfer, Selective modulation of protein kinase C-θ during T-cell activation. Nature 385, 83-86 (1997).
23. S. C. Bunnell, D. I. Hong, J. R. Kardon, T. Yamazaki, C. J. McGlade, V. A. Barr, L. E. Samelson, T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J. Cell Biol. 158, 1263-1275 (2002).
24. A. D. Douglass, R. D. Vale, 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 (2005).
25. J. G. Egen, J. P. Allison, Cytotoxic T lymphocyte antigen-4 accumulation in the immunological synapse is regulated by TCR signal strength. Immunity 16, 23-35 (2002).
26. B. A. Freiberg, H. Kupfer, W. Maslanik, J. Delli, J. Kappler, D. M. Zaller, A. Kupfer, Staging and resetting T cell activation in SMACs. Nat. Immunol. 3, 911-917 (2002).
27. A. Grakoui, S. K. Bromley, C. Sumen, M. M. Davis, A. S. Shaw, P. M. Allen, M. L. Dustin, The immunological synapse: A molecular machine controlling T cell activation. Science 285, 221-227 (1999). (Pubitemid 29329988)
28. K. H. Lee, A. D. Holdorf, M. L. Dustin, A. C. Chan, P. M. Allen, A. S. Shaw, T cell receptor signaling precedes immunological synapse formation. Science 295, 1539-1542 (2002).
29. C. R. Monks, B. A. Freiberg, H. Kupfer, N. Sciaky, A. Kupfer, Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395, 82-86 (1998).
30. B. Purtic, L. A. Pitcher, N. S. van Oers, C. Wülfing, 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 (2005).
31. B. C. Schaefer, J. W. Kappler, A. Kupfer, P. Marrack, Complex and dynamic redistribution of NF-kB signaling intermediates in response to T cell receptor stimulation. Proc. Natl. Acad. Sci. U.S.A. 101, 1004-1009 (2004).
32. C. Wülfing, C. Sumen, M. D. Sjaastad, L. C. Wu, M. L. Dustin, M. M. Davis, Costimulation and endogenous MHC ligands contribute to T cell recognition. Nat. Immunol. 3, 42-47 (2002).
33. T. Yokosuka, K. Sakata-Sogawa, W. Kobayashi, M. Hiroshima, A. Hashimoto-Tane, M. Tokunaga, M. L. Dustin, T. Saito, Newly generated T cell receptor microclusters initiate and sustain T cell activation by recruitment of Zap70 and SLP-76. Nat. Immunol. 6, 1253-1262 (2005).
34. R. Zaru, T. O. Cameron, L. J. Stern, S. Müller, S. Valitutti, Cutting edge: TCR engagement and triggering in the absence of large-scale molecular segregation at the T cell-APC contact site. J. Immunol. 168, 4287-4291 (2002).
35. C. Wülfing, I. Tskvitaria-Fuller, N. Burroughs, M. D. Sjaastad, J. Klem, J. D. Schatzle, Interface accumulation of receptor/ligand couples in lymphocyte activation: Methods, mechanisms, and significance. Immunol. Rev. 189, 64-83 (2002).
36. G. L. Costa, J. M. Benson, C. M. Seroogy, P. Achacoso, C. G. Fathman, G. P. Nolan, Targeting rare populations of murine antigen-specific T lymphocytes by retroviral transduction for potential application in gene therapy for autoimmune disease. J. Immunol. 164, 3581-3590 (2000).
37. I. Tskvitaria-Fuller, N. Mistry, S. Sun, C. Wülfing, Protein transduction as a means of effective manipulation of Cdc42 activity in primary T cells. J. Immunol. Methods 319, 64-78 (2007).
38. T. Mustelin, K. Taskén, Positive and negative regulation of T-cell activation through kinases and phosphatases. Biochem. J. 371, 15-27 (2003).
39. C. Wülfing, J. D. Rabinowitz, C. Beeson, M. D. Sjaastad, H. M. McConnell, M. M. Davis, Kinetics and extent of T cell activation as measured with the calcium signal. J. Exp. Med. 185, 1815-1825 (1997).
40. R. A. Seder, W. E. Paul, M. M. Davis, B. Fazekas de St. Groth, The presence of interleukin 4 during in vitro priming determines the lymphokine-producing potential of CD4+ T cells from T cell receptor transgenic mice. J. Exp. Med. 176, 1091-1098 (1992).
41. T. Ilani, C. Khanna, M. Zhou, T. D. Veenstra, A. Bretscher, Immune synapse formation requires ZAP-70 recruitment by ezrin and CD43 removal by moesin. J. Cell Biol. 179, 733-746 (2007).
42. N. S. van Oers, B. Tohlen, B. Malissen, C. R. Moomaw, S. Afendis, C. A. Slaughter, The 21- and 23-kD forms of TCRz generated by specific ITAM phosphorylations. Nat. Immunol. 1, 322-328 (2000).
43. K. Singelton, N. Parvaze, K. R. Dama, K. S. Chen, P. Jennings, B. Purtic, M. D. Sjaastad, C. Gilpin, M. M. Davis, C. Wülfing, A large T cell invagination with CD2 enrichment resets receptor engagement in the immunological synapse. J. Immunol. 177, 4402-4413 (2006).
44. B. B. Au-Yeung, S. D. Katzman, D. J. Fowell, Cutting edge: Itk-dependent signals required for CD4+ T cells to exert, but not gain, Th2 effector function. J. Immunol. 176, 3895-3899 (2006).
45. M. J. Barnden, J. Allison, W. R. Heath, F. R. Carbone, Defective TCR expression in transgenic mice constructed using cDNA-based α- and β-chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 76, 34-40 (1998).
46. T. He, C. Tang, S. Xu, T. Moyana, J. Xiang, Interferon γ stimulates cellular maturation of dendritic cell line DC2.4 leading to induction of efficient cytotoxic T cell responses and antitumor immunity. Cell. Mol. Immunol. 4, 105-111 (2007).
47. K. S. Weber, M. J. Miller, P. M. Allen, Th17 cells exhibit a distinct calcium profile from Th1 and Th2 cells and have Th1-like motility and NF-AT nuclear localization. J. Immunol. 180, 1442-1450 (2008).
48. R. Varma, G. Campi, T. Yokosuka, T. Saito, M. L. Dustin, T cell receptor-proximal signals are sustained in peripheral microclusters and terminated in the central supramolecular activation cluster. Immunity 25, 117-127 (2006).
49. K. H. Lee, A. R. Dinner, C. Tu, G. Campi, S. Raychaudhuri, R. Varma, T. N. Sims, W. R. Burack, H. Wu, J. Wang, O. Kanagawa, M. Markiewicz, P. M. Allen, M. L. Dustin, A. K. Chakraborty, A. S. Shaw, The immunological synapse balances T cell receptor signaling and degradation. Science 302, 1218-1222 (2003).
50. L. M. Carlin, K. Yanagi, A. Verhoef, E. N. Nolte-'t Hoen, J. Yates, L. Gardner, J. Lamb, G. Lombardi, M. J. Dallman, D. M. Davis, Secretion of IFN-γ and not IL-2 by anergic human T cells correlates with assembly of an immature immune synapse. Blood 106, 3874-3879 (2005).
51. R. A. Maldonado, D. J. Irvine, R. Schreiber, L. H. Glimcher, A role for the immunological synapse in lineage commitment of CD4 lymphocytes. Nature 431, 527-532 (2004).
52. I. Tskvitaria-Fuller, A. Seth, N. Mistry, H. Gu, M. K. Rosen, C. Wülfing, Specific patterns of Cdc42 activity are related to distinct elements of T cell polarization. J. Immunol. 177, 1708-1720 (2006).
53. M. F. Krummel, M. D. Sjaastad, C. Wülfing, M. M. Davis, Differential clustering of CD4 and CD3ζ during T cell recognition. Science 289, 1349-1352 (2000).
54. C. Wülfing, M. D. Sjaastad, M. M. Davis, 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. Proc. Natl. Acad. Sci. U.S.A. 95, 6302-6307 (1998).
55. C. Ballestrem, B. Wehrle-Haller, B. Hinz, B. A. Imhof, Actin-dependent lamellipodia formation and microtubule-dependent tail retraction control-directed cell migration. Mol. Biol. Cell 11, 2999-3012 (2000).
56. I. Tskvitaria-Fuller, A. L. Rozelle, H. L. Yin, C. Wülfing, Regulation of sustained actin dynamics by the TCR and costimulation as a mechanism of receptor localization. J. Immunol. 171, 2287-2295 (2003).
57. P. Várnai, T. Balla, Visualization of phosphoinositides that bind pleckstrin homology domains: Calcium- and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. J. Cell Biol. 143, 501-510 (1998).
58. T. Oikawa, H. Yamaguchi, T. Itoh, M. Kato, T. Ijuin, D. Yamazaki, S. Suetsugu, T. Takenawa, PtdIns(3,4,5)P3 binding is necessary for WAVE2-induced formation of lamellipodia. Nat. Cell Biol. 6, 420-426 (2004).
59. We thank A. Hall, A. Altman, J. D. Schatzle, L. J. Berg, H. L. Yin, M. K. Rosen, and M. G. Roth for plasmids; D. J. Fowell for DO11.10 lymph node suspensions; and W. Woodward for statistical advice. This work was supported by the NIH. K.L.S. and K.T.R. were supported by the institutional training grant T32AI005284.