Selective inhibition of KCa3.1 channels mediates adenosine regulation of the motility of human T cells

Journal of Immunology

Volumn 191, Issue 12, 2013, Pages 6273-6280

  Chimote, Ameet A ^a   Hajdu, Peter ^a   Kucher, Vladimir ^a   Boiko, Nina ^a   Kuras, Zerrin ^a   Szilagyi, Orsolya ^a   Yun, Yeo Heung ^b   Conforti, Laura ^a  

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

^b North Carolina Agricultural and Technical State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 [(2 CHLOROPHENYL)DIPHENYLMETHYL] 1H PYRAZOLE; 2 [4 (2 CARBOXYETHYL)PHENETHYLAMINO]ADENOSINE 5' (N ETHYLCARBOXAMIDE); 5 AMINO 2 (2 FURYL) 7 (2 PHENYLETHYL)PYRAZOLO[4,3 E][1,2,4]TRIAZOLO[1,5 C]PYRIMIDINE; ADENOSINE; ADENYLATE CYCLASE; CYCLIC AMP DEPENDENT PROTEIN KINASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 2; ION CHANNEL; KCA3.1 CHANNEL; N (4 CYANOPHENYL) 2 [4 (2,3,6,7 TETRAHYDRO 2,6 DIOXO 1,3 DIPROPYL 1H PURIN 8 YL)PHENOXY]ACETAMIDE; POTASSIUM CHANNEL KV1.3; TRANSIENT RECEPTOR POTENTIAL CHANNEL M7; UNCLASSIFIED DRUG;

ARTICLE; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; CYTOKINE RELEASE; HUMAN; HUMAN CELL; IMMUNOSUPPRESSIVE TREATMENT; MALE; MOLECULAR MIMICRY; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

EID: 84890345279     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300702     Document Type: Article

References (55)

1. Kobayashi, S., H. Zimmermann, and D. E. Millhorn. 2000. Chronic hypoxia enhances adenosine release in rat PC12 cells by altering adenosine metabolism and membrane transport. J. Neurochem. 74: 621-632.
2. Sitkovsky, M. V., D. Lukashev, S. Apasov, H. Kojima, M. Koshiba, C. Caldwell, A. Ohta, and M. Thiel. 2004. Physiological control of immune response and inflammatory tissue damage by hypoxia-inducible factors and adenosine A2A receptors. Annu. Rev. Immunol. 22: 657-682.
3. Whiteside, T. L. 2010. Immune responses to malignancies. J. Allergy Clin. Immunol. 125(Suppl 2): S272-S283.
4. Blay, J., T. D. White, and D. W. Hoskin. 1997. The extracellular fluid of solid carcinomas contains immunosuppressive concentrations of adenosine. Cancer Res. 57: 2602-2605.
5. Sitkovsky, M. V. 2009. T regulatory cells: hypoxia-adenosinergic suppression and re-direction of the immune response. Trends Immunol. 30: 102-108.
6. Conrad, P. W., L. Conforti, S. Kobayashi, D. Beitner-Johnson, R. T. Rust, Y. Yuan, H. W. Kim, R. H. Kim, K. Seta, and D. E. Millhorn. 2001. The molecular basis of O2-sensing and hypoxia tolerance in pheochromocytoma cells. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 128: 187-204.
7. Deaglio, S., K. M. Dwyer, W. Gao, D. Friedman, A. Usheva, A. Erat, J.-F. Chen, K. Enjyoji, J. Linden, M. Oukka, et al. 2007. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J. Exp. Med. 204: 1257-1265.
8. Mandapathil, M., B. Hilldorfer, M. J. Szczepanski, M. Czystowska, M. Szajnik, J. Ren, S. Lang, E. K. Jackson, E. Gorelik, and T. L. Whiteside. 2010. Generation and accumulation of immunosuppressive adenosine by human CD4+ CD25highFOXP3+ regulatory T cells. J. Biol. Chem. 285: 7176-7186.
9. Linden, J., and C. Cekic. 2012. Regulation of lymphocyte function by adenosine. Arterioscler. Thromb. Vasc. Biol. 32: 2097-2103.
10. Eltzschig, H. K., M. V. Sitkovsky, and S. C. Robson. 2012. Purinergic signaling during inflammation. N. Engl. J. Med. 367: 2322-2333.
11. Fredholm, B. B., A. P. IJzerman, K. A. Jacobson, K.-N. Klotz, and J. Linden. 2001. International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol. Rev. 53: 527-552.
12. Stagg, J., and M. J. Smyth. 2010. Extracellular adenosine triphosphate and adenosine in cancer. Oncogene 29: 5346-5358.
13. Lappas, C. M., J. M. Rieger, and J. Linden. 2005. A2A adenosine receptor induction inhibits IFN-gamma production in murine CD4+ T cells. J. Immunol. 174: 1073-1080.
14. Ohta, A., A. Ohta, M. Madasu, R. Kini, M. Subramanian, N. Goel, and M. Sitkovsky. 2009. A2A adenosine receptor may allow expansion of T cells lacking effector functions in extracellular adenosine-rich microenvironments. J. Immunol. 183: 5487-5493.
15. Ohta, A., E. Gorelik, S. J. Prasad, F. Ronchese, D. Lukashev, M. K.Wong, X. Huang, S. Caldwell, K. Liu, P. Smith, et al. 2006. A2A adenosine receptor protects tumors from antitumor T cells. Proc. Natl. Acad. Sci. USA 103: 13132-13137.
16. Hesdorffer, C. S., E. Malchinkhuu, A. Biragyn, O. S. Mabrouk, R. T. Kennedy, K. Madara, D. D. Taub, D. L. Longo, J. B. Schwartz, L. Ferrucci, and E. J. Goetzl. 2012. Distinctive immunoregulatory effects of adenosine on T cells of older humans. FASEB J. 26: 1301-1310.
17. Duffy, S. M., G. Cruse, C. E. Brightling, and P. Bradding. 2007. Adenosine closes the K+ channel KCa3.1 in human lung mast cells and inhibits their migration via the adenosine A2A receptor. Eur. J. Immunol. 37: 1653-1662.
18. Schwab, A., A. Fabian, P. J. Hanley, and C. Stock. 2012. Role of ion channels and transporters in cell migration. Physiol. Rev. 92: 1865-1913.
19. Cahalan, M. D., and K. G. Chandy. 2009. The functional network of ion channels in T lymphocytes. Immunol. Rev. 231: 59-87.
20. Feske, S., E. Y. Skolnik, and M. Prakriya. 2012. Ion channels and transporters in lymphocyte function and immunity. Nat. Rev. Immunol. 12: 532-547.
21. Schwab, A., P. Hanley, A. Fabian, and C. Stock. 2008. Potassium channels keep mobile cells on the go. Physiology (Bethesda) 23: 212-220.
22. Gomez, T. S., D. D. Billadeau, and W. A. Frederick. 2008. T cell activation and the cytoskeleton: you can't have one without the other. Adv. Immunol. 97: 1-64.
23. Kuras, Z., Y. H. Yun, A. A. Chimote, L. Neumeier, and L. Conforti. 2012. KCa3.1 and TRPM7 channels at the uropod regulate migration of activated human T cells. PLoS ONE 7: e43859.
24. Nicolaou, S. A., L. Neumeier, K. Takimoto, S. M. Lee, H. J. Duncan, S. K. Kant, A. B. Mongey, A. H. Filipovich, and L. Conforti. 2010. Differential calcium signaling and Kv1.3 trafficking to the immunological synapse in systemic lupus erythematosus. Cell Calcium 47: 19-28.
25. Szigligeti, P., L. Neumeier, E. Duke, C. Chougnet, K. Takimoto, S. M. Lee, A. H. Filipovich, and L. Conforti. 2006. Signalling during hypoxia in human T lymphocytes - critical role of the src protein tyrosine kinase p56Lck in the O2 sensitivity of Kv1.3 channels. J. Physiol. 573: 357-370.
26. Robbins, J. R., S. M. Lee, A. H. Filipovich, P. Szigligeti, L. Neumeier, M. Petrovic, and L. Conforti. 2005. Hypoxia modulates early events in T cell receptor-mediated activation in human T lymphocytes via Kv1.3 channels. J. Physiol. 564: 131-143.
27. Smith, A., M. Bracke, B. Leitinger, J. C. Porter, and N. Hogg. 2003. LFA-1-induced T cell migration on ICAM-1 involves regulation of MLCK-mediated attachment and ROCK-dependent detachment. J. Cell Sci. 116: 3123-3133.
28. Wulff, H., M. J. Miller, W. Hänsel, S. Grissmer, M. D. Cahalan, and K. G. Chandy. 2000. Design of a potent and selective inhibitor of the intermediate-conductance Ca2+-activated K+ channel, IKCa1: a potential immunosuppressant. Proc. Natl. Acad. Sci. USA 97: 8151-8156.
29. Cahalan, M. D., H. Wulff, and K. G. Chandy. 2001. Molecular properties and physiological roles of ion channels in the immune system. J. Clin. Immunol. 21: 235-252.
30. Zocchi, C., E. Ongini, A. Conti, A. Monopoli, A. Negretti, P. G. Baraldi, and S. Dionisotti. 1996. The non-xanthine heterocyclic compound SCH 58261 is a new potent and selective A2a adenosine receptor antagonist. J. Pharmacol. Exp. Ther. 276: 398-404.
31. Ji, X., Y.-C. Kim, D. G. Ahern, J. Linden, and K. A. Jacobson. 2001. [3H]MRS 1754, a selective antagonist radioligand for A(2B) adenosine receptors. Biochem. Pharmacol. 61: 657-663.
32. Mayer, C. A., M. A. Haxhiu, R. J. Martin, and C. G. Wilson. 2006. Adenosine A2A receptors mediate GABAergic inhibition of respiration in immature rats. J. Appl. Physiol. 100: 91-97.
33. Jacobson, K. A., and Z. G. Gao. 2006. Adenosine receptors as therapeutic targets. Nat. Rev. Drug Discov. 5: 247-264.
34. Ruppelt, A., R. Mosenden, M. Grönholm, E. M. Aandahl, D. Tobin, C. R. Carlson, H. Abrahamsen, F. W. Herberg, O. Carpén, and K. Taskén. 2007. Inhibition of T cell activation by cyclic adenosine 5′-monophosphate requires lipid raft targeting of protein kinase A type I by the A-kinase anchoring protein ezrin. J. Immunol. 179: 5159-5168.
35. Désaubry, L., I. Shoshani, and R. A. Johnson. 1996. 2′,5′-Dideoxyadenosine 3′-polyphosphates are potent inhibitors of adenylyl cyclases. J. Biol. Chem. 271: 2380-2382.
36. Kuras, Z., V. Kucher, S. M. Gordon, L. Neumeier, A. A. Chimote, A. H. Filipovich, and L. Conforti. 2012. Modulation of Kv1.3 channels by protein kinase A I in T lymphocytes is mediated by the disc large 1-tyrosine kinase Lck complex. Am. J. Physiol. Cell Physiol. 302: C1504-C1512.
37. Säve, S., C. Mohlin, R. Vumma, and K. Persson. 2011. Activation of adenosine A2A receptors inhibits neutrophil transuroepithelial migration. Infect. Immun. 79: 3431-3437.
38. Xu, F., J. Xu, F. W. Tse, and A. Tse. 2006. Adenosine stimulates depolarization and rise in cytoplasmic [Ca2+] in type I cells of rat carotid bodies. Am. J. Physiol. Cell Physiol. 290: C1592-C1598.
39. Kobayashi, S., L. Conforti, R. Y. Pun, and D. E. Millhorn. 1998. Adenosine modulates hypoxia-induced responses in rat PC12 cells via the A2A receptor. J. Physiol. 508: 95-107.
40. Wang, D., Y. Sun, W. Zhang, and P. Huang. 2008. Apical adenosine regulates basolateral Ca2+-activated potassium channels in human airway Calu-3 epithelial cells. Am. J. Physiol. Cell Physiol. 294: C1443-C1453.
41. Gerlach, A. C., C. A. Syme, L. Giltinan, J. P. Adelman, and D. C. Devor. 2001. ATPdependent activation of the intermediate conductance, Ca2+-activated K+ channel, hIK1, is conferred by a C-terminal domain. J. Biol. Chem. 276: 10963-10970.
42. Hayashi, M., C. Kunii, T. Takahata, and T. Ishikawa. 2004. ATP-dependent regulation of SK4/IK1-like currents in rat submandibular acinar cells: possible role of cAMP-dependent protein kinase. Am. J. Physiol. Cell Physiol. 286: C635-C646.
43. Pellegrino, M., and M. Pellegrini. 1998. Modulation of Ca2+-activated K+ channels of human erythrocytes by endogenous cAMP-dependent protein kinase. Pflugers Arch. 436: 749-756.
44. Neylon, C., T. D'Souza, and P. Reinhart. 2004. Protein kinase A inhibits intermediate conductance Ca2+-activated K+ channels expressed in Xenopus oocytes. Pflugers Arch. 448: 613-620.
45. Levite, M., L. Cahalon, A. Peretz, R. Hershkoviz, A. Sobko, A. Ariel, R. Desai, B. Attali, and O. Lider. 2000. Extracellular K(+) and opening of voltage-gated potassium channels activate T cell integrin function: physical and functional association between Kv1.3 channels and beta1 integrins. J. Exp. Med. 191: 1167-1176.
46. Matheu, M. P., C. Beeton, A. Garcia, V. Chi, S. Rangaraju, O. Safrina, K. Monaghan, M. I. Uemura, D. Li, S. Pal, et al. 2008. Imaging of effector memory T cells during a delayed-type hypersensitivity reaction and suppression by Kv1.3 channel block. Immunity 29: 602-614.
47. Toyama, K., H. Wulff, K. G. Chandy, P. Azam, G. Raman, T. Saito, Y. Fujiwara, D. L. Mattson, S. Das, J. E. Melvin, et al. 2008. The intermediate-conductance calcium-activated potassium channel KCa3.1 contributes to atherogenesis in mice and humans. J. Clin. Invest. 118: 3025-3037.
48. Ghanshani, S., H. Wulff, M. J. Miller, H. Rohm, A. Neben, G. A. Gutman, M. D. Cahalan, and K. G. Chandy. 2000. Up-regulation of the IKCa1 potassium channel during T-cell activation. Molecular mechanism and functional consequences. J. Biol. Chem. 275: 37137-37149.
49. Dustin, M. L., and T. A. Springer. 1989. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature 341: 619-624.
50. Csóka, B., L. Himer, Z. Selmeczy, E. S. Vizi, P. Pacher, C. Ledent, E. A. Deitch, Z. Spolarics, Z. H. Németh, and G. Haskó. 2008. Adenosine A2A receptor activation inhibits T helper 1 and T helper 2 cell development and effector function. FASEB J. 22: 3491-3499.
51. Mandapathil, M., M. Szczepanski, M. Harasymczuk, J. Ren, D. Cheng, E. K. Jackson, E. Gorelik, J. Johnson, S. Lang, and T. L. Whiteside. 2012. CD26 expression and adenosine deaminase activity in regulatory T cells (Treg) and CD4(+) T effector cells in patients with head and neck squamous cell carcinoma. OncoImmunology 1: 659-669.
52. Erdag, G., J. T. Schaefer, M. E. Smolkin, D. H. Deacon, S. M. Shea, L. T. Dengel, J. W. Patterson, and C. L. Slingluff, Jr. 2012. Immunotype and immunohistologic characteristics of tumor-infiltrating immune cells are associated with clinical outcome in metastatic melanoma. Cancer Res. 72: 1070-1080.
53. Mrass, P., H. Takano, L. G. Ng, S. Daxini, M. O. Lasaro, A. Iparraguirre, L. L. Cavanagh, U. H. von Andrian, H. C. Ertl, P. G. Haydon, and W. Weninger. 2006. Random migration precedes stable target cell interactions of tumor-infiltrating T cells. J. Exp. Med. 203: 2749-2761.
54. Chimote, A. A., Z. Kuras, and L. Conforti. 2012. Disruption of kv1.3 channel forward vesicular trafficking by hypoxia in human T lymphocytes. J. Biol. Chem. 287: 2055-2067.
55. Conforti, L., M. Petrovic, D. Mohammad, S. Lee, Q. Ma, S. Barone, and A. H. Filipovich. 2003. Hypoxia regulates expression and activity of Kv1.3 channels in T lymphocytes: a possible role in T cell proliferation. J. Immunol. 170: 695-702.