Modulation of T cell activation by localized K + accumulation at the immunological synapse-A mathematical model

Journal of Theoretical Biology

Volumn 300, Issue , 2012, Pages 173-182

  Martin, Geoffrey V ^a   Yun, Yeoheung ^b   Conforti, Laura ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b NORTH CAROLINA A AND T STATE UNIVERSITY   (United States)

Author keywords

Immunological synapse; K + channels; K + diffusion; Mathematical model; T cell activation

Indexed keywords

CALCIUM ION; POTASSIUM ION;

ANTIGEN; BIOLOGY; CALCIUM; COMPUTER SIMULATION; DIFFUSION; IMMUNE RESPONSE; IMMUNOASSAY; NUMERICAL MODEL;

ARTICLE; CALCIUM CELL LEVEL; CALCULATION; CELL MEMBRANE; CONTROLLED STUDY; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL SYNAPSE; MATHEMATICAL MODEL; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIMULATION; T LYMPHOCYTE ACTIVATION;

CALCIUM; FEEDBACK, PHYSIOLOGICAL; HUMANS; IMMUNOLOGICAL SYNAPSES; LYMPHOCYTE ACTIVATION; MODELS, IMMUNOLOGICAL; POTASSIUM CHANNELS; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS;

EID: 84856778505     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2012.01.018     Document Type: Article

References (67)

1. Anton van der Merwe P., Davis S.J., Shaw A.S., Dustin M.L. Cytoskeletal polarization and redistribution of cell-surface molecules during T cell antigen recognition. Semin. Immunol. 2000, 12:5-21.
2. Bautista D.M., Lewis R.S. Modulation of plasma membrane calcium-ATPase activity by local calcium microdomains near CRAC channels in human T cells. J. Physiol. 2004, 556:805-817.
3. Borst J.G., Sakmann B. Depletion of calcium in the synaptic cleft of a calyx-type synapse in the rat brainstem. J. Physiol. 1999, 521(Pt. 1):123-133.
4. Bowlby M.R., Fadool D.A., Holmes T.C., Levitan I.B. Modulation of the Kv1.3 potassium channel by receptor tyrosine kinases. J. Gen. Physiol. 1997, 110:601-610.
5. Burroughs N.J., Lazic Z., van der Merwe P.A. Ligand detection and discrimination by spatial relocalization: a kinase-phosphatase segregation model of TCR activation. Biophys. J. 2006, 91:1619-1629.
6. Cahalan M.D., Chandy K.G. The functional network of ion channels in T lymphocytes. Immunol. Rev. 2009, 231:59-87.
7. Cahalan M.D., Chandy K.G., DeCoursey T.E., Gupta S. A voltage-gated potassium channel in human T lymphocytes. J. Physiol. 1985, 358:197-237.
8. Cai Y.C., Douglass J. In vivo and in vitro phosphorylation of the T lymphocyte type n (Kv1.3) potassium channel. J. Biol. Chem. 1993, 268:23720-23727.
9. Cemerski S., Shaw A. Immune synapses in T-cell activation. Curr. Opin. Immunol. 2006, 18:298-304.
10. Cemerski S., Das J., Giurisato E., Markiewicz M.A., Allen P.M., Chakraborty A.K., Shaw A.S. The balance between T cell receptor signaling and degradation at the center of the immunological synapse is determined by antigen quality. Immunity 2008, 29:414-422.
11. Donnadieu E., Bismuth G., Trautmann A. Calcium fluxes in T lymphocytes. J. Biol. Chem. 1992, 267:25864-25872.
12. Dushek O., Coombs D. Analysis of serial engagement and peptide-MHC transport in T cell receptor microclusters. Biophys. J. 2008, 94:3447-3460.
13. Dustin M.L., Chan A.C. Signaling takes shape in the immune system. Cell 2000, 103:283-294.
14. Egelman D.M., Montague P.R. Calcium dynamics in the extracellular space of mammalian neural tissue. Biophys. J. 1999, 76:1856-1867.
15. Fadool D.A. Tyrosine phosphorylation downregulates a potassium current in rat olfactory bulb neurons and a cloned Kv1.3 channel. Ann. N. Y. Acad. Sci. 1998, 855:529-532.
16. Fomina A.F., Fanger C.M., Kozak J.A., Cahalan M.D. Single channel properties and regulated expression of Ca(2+) release-activated Ca(2+) (CRAC) channels in human T cells. J. Cell Biol. 2000, 150:1435-1444.
17. Freiberg B.A., Kupfer H., Maslanik W., Delli J., Kappler J., Zaller D.M., Kupfer A. Staging and resetting T cell activation in SMACs. Nat. Immunol. 2002, 3:911-917.
18. Galush W.J., Nye J.A., Groves J.T. Quantitative fluorescence microscopy using supported lipid bilayer standards. Biophys. J. 2008, 95:2512-2519.
19. Grakoui A., Bromley S.K., Sumen C., Davis M.M., Shaw A.S., Allen P.M., Dustin M.L. The immunological synapse: a molecular machine controlling T cell activation. Science 1999, 285:221-227.
20. Grissmer S., Nguyen A.N., Cahalan M.D. Calcium-activated potassium channels in resting and activated human T lymphocytes. Expression levels, calcium dependence, ion selectivity, and pharmacology. J. Gen. Physiol. 1993, 102:601-630.
21. Hajdu P., Varga Z., Pieri C., Panyi G., Gaspar R. Cholesterol modifies the gating of Kv1.3 in human T lymphocytes. Pflugers Arch. 2003, 445:674-682.
22. Hodgkin A.L., Huxley A.F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 1952, 117:500-544.
23. Holmes T.C., Fadool D.A., Levitan I.B. Tyrosine phosphorylation of the Kv1.3 potassium channel. J. Neurosci. 1996, 16:1581-1590.
24. Hori S., Collette A., Demengeot J., Stewart J. A new statistical method for quantitative analyses: application to the precise quantification of T cell receptor repertoires. J. Immunol. Methods 2002, 268:159-170.
25. Hoth M., Button D.C., Lewis R.S. Mitochondrial control of calcium-channel gating: a mechanism for sustained signaling and transcriptional activation in T lymphocytes. Proc. Natl. Acad. Sci. USA 2000, 97:10607-10612.
26. Kargacin G.J. Calcium signaling in restricted diffusion spaces. Biophys. J. 1994, 67:262-272.
27. Kesten H. The critical probability of bond percolation on the square lattice equals 1/2. Commun. Math. Phys. 1980, 74:41-59. (Springer, Berlin/Heidelberg).
28. Koo G.C., Blake J.T., Talento A., Nguyen M., Lin S., Sirotina A., Shah K., Mulvany K., Hora D., Cunningham P., Wunderler D.L., McManus O.B., Slaughter R., Bugianesi R., Felix J., Garcia M., Williamson J., Kaczorowski G., Sigal N.H., Springer M.S., Feeney W. Blockade of the voltage-gated potassium channel Kv1.3 inhibits immune responses in vivo. J. Immunol. 1997, 158:5120-5128.
29. Krummel M.F., Cahalan M.D. The immunological synapse: a dynamic platform for local signaling. J. Clin. Immunol. 2010, 30:364-372.
30. Kummerow C., Junker C., Kruse K., Rieger H., Quintana A., Hoth M. The immunological synapse controls local and global calcium signals in T lymphocytes. Immunol. Rev. 2009, 231:132-147.
31. + in recovery from C-type inactivation. Biophys. J. 1996, 71:3157-3166.
32. Levy D.I., Deutsch C. Recovery from C-type inactivation is modulated by extracellular potassium. Biophys. J. 1996, 70:798-805.
33. Lewis R.S. Calcium signaling mechanisms in T lymphocytes. Annu. Rev. Immunol. 2001, 19:497-521.
34. 2+ current in human leukemic T cells. Cell Regul. 1989, 1:99-112.
35. Lioudyno M.I., Kozak J.A., Penna A., Safrina O., Zhang S.L., Sen D., Roos J., Stauderman K.A., Cahalan M.D. Orai1 and STIM1 move to the immunological synapse and are up-regulated during T cell activation. Proc. Natl. Acad. Sci. USA 2008, 105:2011-2016.
36. Luik R.M., Wang B., Prakriya M., Wu M.M., Lewis R.S. Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation. Nature 2008, 454:538-542.
37. Monks C.R., Freiberg B.A., Kupfer H., Sciaky N., Kupfer A. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 1998, 395:82-86.
38. Mossman K.D., Campi G., Groves J.T., Dustin M.L. Altered TCR signaling from geometrically repatterned immunological synapses. Science 2005, 310:1191-1193.
39. Nicolaou S.A., Neumeier L., Peng Y., Devor D.C., Conforti L. The Ca(2+)-activated K(+) channel KCa3.1 compartmentalizes in the immunological synapse of human T lymphocytes. Am. J. Physiol. Cell Physiol. 2007, 292:C1431-C1439.
40. Nicolaou S.A., Neumeier L., Steckly A., Kucher V., Takimoto K., Conforti L. Localization of Kv1.3 channels in the immunological synapse modulates the calcium response to antigen stimulation in T lymphocytes. J. Immunol. 2009, 183:6296-6302.
41. Nicolaou S.A., Szigligeti P., Neumeier L., Lee S.M., Duncan H.J., Kant S.K., Mongey A.B., Filipovich A.H., Conforti L. Altered dynamics of Kv1.3 channel compartmentalization in the immunological synapse in systemic lupus erythematosus. J. Immunol. 2007, 179:346-356.
42. Nicolaou S.A., Neumeier L., Takimoto K., Lee S.M., Duncan H.J., Kant S.K., Mongey A.B., Filipovich A.H., Conforti L. Differential calcium signaling and Kv1.3 trafficking to the immunological synapse in systemic lupus erythematosus. Cell Calcium 2010, 47:19-28.
43. Pahapill P.A., Schlichter L.C. Modulation of potassium channels in human T lymphocytes: effects of temperature. J. Physiol. 1990, 422:103-126.
44. Palti Y., Gold R., Stampfli R. Diffusion of ions in myelinated nerve fibers. Biophys. J. 1979, 25:17-31.
45. Panyi G., Varga Z., Gaspar R. Ion channels and lymphocyte activation. Immunol. Lett. 2004, 92:55-66.
46. Panyi G., Vamosi G., Bacso Z., Bagdany M., Bodnar A., Varga Z., Gaspar R., Matyus L., Damjanovich S. Kv1.3 potassium channels are localized in the immunological synapse formed between cytotoxic and target cells. Proc. Natl. Acad. Sci. USA 2004, 101:1285-1290.
47. Panyi G., Bagdany M., Bodnar A., Vamosi G., Szentesi G., Jenei A., Matyus L., Varga S., Waldmann T.A., Gaspar R., Damjanovich S. Colocalization and nonrandom distribution of Kv1.3 potassium channels and CD3 molecules in the plasma membrane of human T lymphocytes. Proc. Natl. Acad. Sci. USA 2003, 100:2592-2597.
48. Poulopoulou C., Papadopoulou-Daifoti Z., Hatzimanolis A., Fragiadaki K., Polissidis A., Anderzanova E., Davaki P., Katsiari C.G., Sfikakis P.P. Glutamate levels and activity of the T cell voltage-gated potassium Kv1.3 channel in patients with systemic lupus erythematosus. Arthritis Rheum. 2008, 58:1445-1450.
49. Prakriya M., Lewis R.S. CRAC channels: activation, permeation, and the search for a molecular identity. Cell Calcium 2003, 33:311-321.
50. Quintana A., Griesemer D., Schwarz E.C., Hoth M. Calcium-dependent activation of T-lymphocytes. Pflugers Arch. 2005, 450:1-12.
51. Rader R.K., Kahn L.E., Anderson G.D., Martin C.L., Chinn K.S., Gregory S.A. T cell activation is regulated by voltage-dependent and calcium-activated potassium channels. J. Immunol. 1996, 156:1425-1430.
52. Raychaudhuri S., Chakraborty A.K., Kardar M. Effective membrane model of the immunological synapse. Phys. Rev. Lett. 2003, 91:208101.
53. Robbins J.R., Lee S.M., Filipovich A.H., Szigligeti P., Neumeier L., Petrovic M., Conforti L. Hypoxia modulates early events in T cell receptor-mediated activation in human T lymphocytes via Kv1.3 channels. J. Physiol. 2005, 564:131-143.
54. 2+ depletion contributes to fast activity-dependent modulation of synaptic transmission in the brain. Neuron 2003, 37:287-297.
55. Sykova E., Nicholson C. Diffusion in brain extracellular space. Physiol. Rev. 2008, 88:1277-1340.
56. 2 sensitivity of Kv1.3 channels. J. Physiol. 2006, 573:357-370.
57. 2+ ion extruded. J. Physiol. 2009, 587:315-327.
58. Toth A., Szilagyi O., Krasznai Z., Panyi G., Hajdu P. Functional consequences of Kv1.3 ion channel rearrangement into the immunological synapse. Immunol. Lett. 2009, 125:15-21.
59. Treherne J.E., Lane N.J., Moreton R.B., Pichon Y. A quantitative study of potassium movements in the central nervous system of Periplaneta americana. J. Exp. Biol. 1970, 53:109-136.
60. 2+ in the synaptic cleft. Biophys. J. 1997, 72:2103-2116.
61. 2+ signaling. Cell Calcium 1995, 17:287-300.
62. + channels in intact human T lymphocytes. Noninvasive measurements of membrane currents, membrane potential, and intracellular calcium. J. Gen. Physiol. 1995, 105:765-794.
63. Weikl T.R., Lipowsky R. Pattern formation during T-cell adhesion. Biophys. J. 2004, 87:3665-3678.
64. Willemsen O.H., Snel M.M., van der Werf K.O., de Grooth B.G., Greve J., Hinterdorfer P., Gruber H.J., Schindler H., van Kooyk Y., Figdor C.G. Simultaneous height and adhesion imaging of antibody-antigen interactions by atomic force microscopy. Biophys. J. 1998, 75:2220-2228.
65. Wulff H., Calabresi P.A., Allie R., Yun S., Pennington M., Beeton C., Chandy K.G. The voltage-gated Kv1.3 K(+) channel in effector memory T cells as new target for MS. J. Clin. Invest. 2003, 111:1703-1713.
66. Zaniboni M., Swietach P., Rossini A., Yamamoto T., Spitzer K.W., Vaughan-Jones R.D. Intracellular proton mobility and buffering power in cardiac ventricular myocytes from rat, rabbit, and guinea pig. Am. J. Physiol. Heart Circ. Physiol. 2003, 285:H1236-H1246.
67. 2+ stores. Proc. Natl. Acad. Sci. USA 1993, 90:6295-6299.