Blocking Kv1.3 channels inhibits Th2 lymphocyte function and treats a rat model of asthma

Journal of Biological Chemistry

Volumn 289, Issue 18, 2014, Pages 12623-12632

  Koshy, Shyny ^a   Huq, Redwan ^a,b   Tanner, Mark R ^a,c   Atik, Mustafa A ^d,e   Porter, Paul C ^e   Khan, Fatima S ^a   Pennington, Michael W ^f   Hanania, Nicola A ^d,e   Corry, David B ^a,e   Beeton, Christine ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Graduate Program in Molecular Physiology and Biophysics   (United States)

^c Interdepartmental Graduate Program in Translational Biology and Molecular Medicine   (United States)

^d Asthma Clinical Research Center   (United States)

^e Department of Medicine ^*  (United States)

^f Peptides International   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYMPHOCYTES;

ALLERGIC ASTHMA; CHANNEL BLOCKERS; IMMUNO MODULATIONS; LUNG INFLAMMATION; RAT MODEL; T LYMPHOCYTES;

DISEASES;

INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 5; OVALBUMIN; POTASSIUM CHANNEL BLOCKING AGENT; POTASSIUM CHANNEL KV1.3; SHK 186; UNCLASSIFIED DRUG;

ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; EFFECTOR CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; EOSINOPHIL COUNT; FEMALE; HUMAN; HUMAN CELL; IMMUNOMODULATION; LEUKOCYTE DIFFERENTIAL COUNT; LUNG LAVAGE; LYMPHOCYTIC INFILTRATION; MEMORY T LYMPHOCYTE; NEUTROPHIL COUNT; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RAT MODEL; TH2 CELL;

AIRWAY INFLAMMATION; ALLERGY; ANIMAL MODELS; ASTHMA; CELLULAR IMMUNE RESPONSE; KCNA3; KV1.3; POTASSIUM CHANNELS; T LYMPHOCYTE; THERAPY;

ADULT; ANIMALS; ASTHMA; BRONCHOALVEOLAR LAVAGE FLUID; DISEASE MODELS, ANIMAL; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNOLOGIC MEMORY; INTERLEUKIN-10; INTERLEUKIN-13; INTERLEUKIN-4; INTERLEUKIN-5; KV1.3 POTASSIUM CHANNEL; MALE; MIDDLE AGED; OVALBUMIN; POTASSIUM CHANNEL BLOCKERS; PROTEINS; RATS; RATS, INBRED F344; T-LYMPHOCYTES; TH2 CELLS; YOUNG ADULT;

EID: 84899748553     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.517037     Document Type: Article

References (53)

1. Bousquet, J., Jeffery, P. K., Busse, W. W., Johnson, M., and Vignola, A. M. (2000) Asthma. From bronchoconstriction to airways inflammation and remodeling. Am. J. Respir. Crit. Care Med. 161, 1720-1745
2. Barnes, P. J. (2010) New therapies for asthma: is there any progress? Trends Pharmacol. Sci. 31, 335-343
3. Follenweider, L. M., and Lambertino, A. (2013) Epidemiology of asthma in the United States. Nurs. Clin. North Am. 48, 1-10
4. Baïz, N., and Annesi-Maesano, I. (2012) Is the asthma epidemic still ascending? Clin. Chest Med. 33, 419-429
5. Holgate, S. T. (2008) Pathogenesis of asthma. Clin. Exp. Allergy 38, 872-897
6. Medoff, B. D., Thomas, S. Y., and Luster, A. D. (2008) T cell trafficking in allergic asthma: the ins and outs. Annu. Rev. Immunol. 26, 205-232
7. Schuijs, M. J., Willart, M. A., Hammad, H., and Lambrecht, B. N. (2013) Cytokine targets in airway inflammation. Curr. Opin. Pharmacol. 13, 351-361
8. Syed, F., Blakemore, S. J., Wallace, D. M., Trower, M. K., Johnson, M., Markham, A. F., and Morrison, J. F. (1999) CCR7 (EBI1) receptor downregulation in asthma: differential gene expression in human CD4 T lymphocytes. QJM 92, 463-471
9. Cahalan, M. D., and Chandy, K. G. (2009) The functional network of ion channels in T lymphocytes. Immunol. Rev. 231, 59-87
10. Feske, S., Skolnik, E. Y., and Prakriya, M. (2012) Ion channels and transporters in lymphocyte function and immunity. Nat. Rev. Immunol. 12, 532-547
11. Beeton, C., Pennington, M. W., Wulff, H., Singh, S., Nugent, D., Crossley, G., Khaytin, I., Calabresi, P. A., Chen, C.-Y., Gutman, G. A., and Chandy, K. G. (2005) Targeting effector memory T cells with a selective peptide inhibitor of KV1.3 channels for therapy of autoimmune diseases. Mol. Pharmacol. 67, 1369-1381
12. Beeton, C., Wulff, H., Standifer, N. E., Azam, P., Mullen, K. M., Pennington, M. W., Kolski-Andreaco, A., Wei, E., Grino, A., Counts, D. R., Wang, P. H., LeeHealey, C. J., S. Andrews, B., Sankaranarayanan, A., Homerick, D., Roeck, W. W., Tehranzadeh, J., Stanhope, K. L., Zimin, P., Havel, P. J., Griffey, S., Knaus, H. G., Nepom, G. T., Gutman, G. A., Calabresi, P. A., and Chandy, K. G. (2006) KV1.3 channels are a therapeutic target for T cell-mediated autoimmune diseases. Proc. Natl. Acad. Sci. U.S.A. 103, 17414-17419
13. Wulff, H., Calabresi, P. A., Allie, R., Yun, S., Pennington, M., Beeton, C., and Chandy, K. G. (2003) The voltage-gated KV1.3 K+ channel in effector memory T cells as new target for MS. J. Clin. Invest. 111, 1703-1713
14. Beeton, C., Pennington, M. W., and Norton, R. S. (2011) Analogs of the sea anemone potassium channel blocker ShK for the treatment of autoimmune diseases. Inflamm. Allergy Drug Targets 10, 313-321
15. Chi, V., Pennington, M. W., Norton, R. S., Tarcha, E. J., Londono, L. M., Sims-Fahey, B., Upadhyay, S. K., Lakey, J. T., Iadonato, S., Wulff, H., Beeton, C., and Chandy, K. G. (2012) Development of a sea anemone toxin as an immunomodulator for therapy of autoimmune diseases. Toxicon 59, 529-546
16. Ghanshani, S., Wulff, H., Miller, M. J., Rohm, H., Neben, A., Gutman, G. A., Cahalan, M. D., and Chandy, K. G. (2000) Up-regulation of the IKCa1 potassium channel during T-cell activation: molecular mechanism and functional consequences. J. Biol. Chem. 275, 37137-37149
17. Pennington, M. W., Beeton, C., Galea, C. A., Smith, B. J., Chi, V., Monaghan, K. P., Garcia, A., Rangaraju, S., Giuffrida, A., Plank, D., Crossley, G., Nugent, D., Khaytin, I., Lefievre, Y., Peshenko, I., Dixon, C., Chauhan, S., Orzel, A., Inoue, T., Hu, X., Moore, R. V., Norton, R. S., and Chandy, K. G. (2009) Engineering a stable and selective peptide blocker of the KV1.3 channel in T lymphocytes. Mol. Pharmacol. 75, 762-773
18. Matheu, M. P., Beeton, C., Garcia, A., Chi, V., Rangaraju, S., Safrina, O., Monaghan, K., Uemura, M. I., Li, D., Pal, S., de la Maza, L. M., Monuki, E., Flügel, A., Pennington, M. W., Parker, I., Chandy, K. G., and Cahalan, M. D. (2008) Imaging of effector memory T cells during a delayed-type hypersensitivity reaction and suppression by KV1.3 channel block. Immunity 29, 602-614
19. Tarcha, E. J., Chi, V., Munoz-Elías, E. J., Bailey, D., Londono, L. M., Upadhyay, S. K., Norton, K., Banks, A., Tjong, I., Nguyen, H., Hu, X., Ruppert, G. W., Boley, S. E., Slauter, R., Sams, J., Knapp, B., Kentala, D., Hansen, Z., Pennington, M. W., Beeton, C., Chandy, K. G., and Iadonato, S. P. (2012) Durable pharmacological responses from the peptide ShK-186, a specific KV1.3 channel inhibitor that suppresses T cell mediators of autoimmune diseases. J. Pharmacol. Exp. Ther. 342, 642-653
20. Norton, R. S., Pennington, M. W., and Beeton, C. (2013) Transforming a toxin into a therapeutic: the sea anemone potassium channel blocker ShK toxin for treatment of autoimmune diseases in Venoms to drugs: Venom as a source for the development of human therapeutics (King, G. F., ed.) Royal Society of Chemistry, London, in press
21. Pizzichini, M. M., Popov, T. A., Efthimiadis, A., Hussack, P., Evans, S., Pizzichini, E., Dolovich, J., and Hargreave, F. E. (1996) Spontaneous and induced sputum to measure indices of airway inflammation in asthma. Am. J. Respir. Crit. Care Med. 154, 866-869
22. Wulff, H., Knaus, H. G., Pennington, M., and Chandy, K. G. (2004) K+ channel expression during B cell differentiation: implications for immunomodulation and autoimmunity. J. Immunol. 173, 776-786
23. Beeton, C., Wulff, H., Barbaria, J., Clot-Faybesse, O., Pennington, M., Bernard, D., Cahalan, M. D., Chandy, K. G., and Béraud, E. (2001) Selective blockade of T lymphocyte K+ channels ameliorates experimental autoimmune encephalomyelitis, a model for multiple sclerosis. Proc. Natl. Acad. Sci. U.S.A. 98, 13942-13947
24. Beeton, C., Wulff, H., Singh, S., Botsko, S., Crossley, G., Gutman, G. A., Cahalan, M. D., Pennington, M., and Chandy, K. G. (2003) A novel fluorescent toxin to detect and investigate KV1.3 channel up-regulation in chronically activated T lymphocytes. J. Biol. Chem. 278, 9928-9937
25. Beeton, C., Barbaria, J., Giraud, P., Devaux, J., Benoliel, A. M., Gola, M., Sabatier, J. M., Bernard, D., Crest, M., and Béraud, E. (2001) Selective blocking of voltage-gated K+ channels improves experimental autoimmune encephalomyelitis and inhibits T cell activation. J. Immunol. 166, 936-944
26. Chang, S. C., Galea, C. A., Leung, E. W., Tajhya, R. B., Beeton, C., Pennington, M. W., and Norton, R. S. (2012) Expression and isotopic labeling of the potassium channel blocker ShK toxin as a thioredoxin fusion protein in bacteria. Toxicon 60, 840-850
27. Kruschinski, C., Skripuletz, T., Bedoui, S., Tschernig, T., Pabst, R., Nassenstein, C., Braun, A., and von Hörsten, S. (2005) CD26 (dipeptidylpeptidase IV)-dependent recruitment of T cells in a rat asthma model. Clin. Exp. Immunol. 139, 17-24
28. Polikepahad, S., Barranco, W. T., Porter, P., Anderson, B., Kheradmand, F., and Corry, D. B. (2010) A reversible, non-invasive method for airway resistance measurements and bronchoalveolar lavage fluid sampling in mice. J. Vis. Exp. 38, 1720
29. Porter, P. C., Roberts, L., Fields, A., Knight, M., Qian, Y., Delclos, G. L., Han, S., Kheradmand, F., and Corry, D. B. (2011) Necessary and sufficient role for T helper cells to prevent fungal dissemination in allergic lung disease. Infect. Immun. 79, 4459-4471
30. Grissmer, S., Nguyen, A. N., Aiyar, J., Hanson, D. C., Mather, R. J., Gutman, G. A., Karmilowicz, M. J., Auperin, D. D., and Chandy, K. G. (1994) Pharmacological characterization of five cloned voltage-gated K+ channels, types KV1.1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines. Mol. Pharmacol. 45, 1227-1234
31. Bunce, C., and Bell, E. (1997) CD45RC isoforms define two types of CD4 memory T cells, one of which depends on persisting antigen. J. Exp. Med. 185, 767-776
32. Ohtsuka, R., Shutoh, Y., Fujie, H., Yamaguchi, S., Takeda, M., Harada, T., and Doi, K. (2005) Changes in histology and expression of cytokines and chemokines in the rat lung following exposure to ovalbumin. Exp. Toxicol. Pathol. 56, 361-368
33. Chung, F. (2001) Anti-inflammatory cytokines in asthma and allergy: interleukin- 10, interleukin-12, interferon-gamma. Mediators Inflamm. 10, 51-59
34. Gocke, A. R., Lebson, L. A., Grishkan, I. V., Hu, L., Nguyen, H. M., Whartenby, K. A., Chandy, K. G., and Calabresi, P. A. (2012) KV1.3 deletion biases T cells toward an immunoregulatory phenotype and renders mice resistant to autoimmune encephalomyelitis. J. Immunol. 188, 5877-5886
35. Rus, H., Pardo, C. A., Hu, L., Darrah, E., Cudrici, C., Niculescu, T., Niculescu, F., Mullen, K. M., Allie, R., Guo, L., Wulff, H., Beeton, C., Judge, S. I., Kerr, D. A., Knaus, H. G., Chandy, K. G., and Calabresi, P. A. (2005) The voltage-gated potassium channelKV1.3 is highly expressed on inflammatory infiltrates in multiple sclerosis brain. Proc. Natl. Acad. Sci. U.S.A. 102, 11094-11099
36. Gilhar, A., Bergman, R., Assay, B., Ullmann, Y., and Etzioni, A. (2011) The beneficial effect of blocking KV1.3 in the psoriasiform SCID mouse model. J. Invest. Dermatol. 131, 118-124
37. Bradding, P., and Wulff, H. (2009) The K+ channels KCa3.1 and KV1.3 as novel targets for asthma therapy. Br. J. Pharmacol. 157, 1330-1339
38. Porter, P., Polikepahad, S., Qian, Y., Knight, J. M., Lu, W., Tai, W. M., Roberts, L., Ongeri, V., Yang, T., Seryshev, A., Abramson, S., Delclos, G. L., Kheradmand, F., and Corry, D. B. (2011) Respiratory tract allergic disease and atopy: experimental evidence for a fungal infectious etiology. Med. Mycol. 49, S158-SS163
39. van Woerden, H. C., Gregory, C., Brown, R., Marchesi, J. R., Hoogendoorn, B., and Matthews, I. P. (2013) Differences in fungi present in induced sputum samples from asthma patients and non-atopic controls: a community based case control study. BMC Infect. Dis. 13, 69
40. Agbetile, J., Fairs, A., Desai, D., Hargadon, B., Bourne, M., Mutalithas, K., Edwards, R., Morley, J. P., Monteiro, W. R., Kulkarni, N. S., Green, R. H., Pavord, I. D., Bradding, P., Brightling, C. E., Wardlaw, A. J., and Pashley, C. H. (2012) Isolation of filamentous fungi from sputum in asthma is associated with reduced post-bronchodilator FEV1. Clin. Exp. Allergy 45, 782-791
41. Conforti, L., Petrovic, M., Mohammad, D., Lee, S., Ma, Q., Barone, S., and Filipovich, A. H. (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
42. de Pater-Huijsen, F. L., van der Loos, C. M., de Riemer, M. J., van der Zee, J. S., Jansen, H. M., and Out, T. A. (2000) Double staining of intracellular cytokine proteins and T-lymphocyte subsets. Evaluation of the method in blood and bronchoalveolar lavage fluid. Histochem. J. 32, 3-11
43. Machura, E., Mazur, B., Rusek-Zychma, M., and Bar-Czarnecka, M. (2010) Cytokine production by peripheral blood CD4 and CD8 T cells in atopic childhood asthma. Clin. Dev. Immunol. 2010, 606139
44. Krampera, M., Antico, A., Vinante, F., Morosato, L., and Pizzolo, G. (1999) Lymphocyte membrane antigen expression and intracellular cytokine patterns in an asymptomatic patient with persistently high serum levels of IgE. Ann. Allergy Asthma Immunol. 83, 144-148
45. Schwingshackl, A., Moqbel, R., and Duszyk, M. (2002) Nitric oxide activates ATP-dependent K+ channels in human eosinophils. J. Leukoc. Biol. 71, 807-812
46. Femling, J. K., Cherny, V. V., Morgan, D., Rada, B., Davis, A. P., Czirják, G., Enyedi, P., England, S. K., Moreland, J. G., Ligeti, E., Nauseef, W. M., and DeCoursey, T. E. (2006) The antibacterial activity of human neutrophils and eosinophils requires proton channels but no BK channels. J. Gen. Physiol. 127, 659-672
47. Spiller, F., Orrico, M. I., Nascimento, D. C., Czaikoski, P. G., Souto, F. O., Alves-Filho, J. C., Freitas, A., Carlos, D., Montenegro, M. F., Neto, A. F., Ferreira, S. H., Rossi, M. A., Hothersall, J. S., Assreuy, J., and Cunha, F. Q. (2010) Hydrogen sulfide improves neutrophil migration and survival in sepsis via K+ATP channel activation. Am. J. Respir. Crit. Care Med. 182, 360-368
48. Essin, K., Gollasch, M., Rolle, S., Weissgerber, P., Sausbier, M., Bohn, E., Autenrieth, I. B., Ruth, P., Luft, F. C., Nauseef, W. M., and Kettritz, R. (2009) BK channels in innate immune functions of neutrophils and macrophages. Blood 113, 1326-1331
49. Villalonga, N., Escalada, A., Vicente, R., Sánchez-Tilló, E., Celada, A., Solsona, C., and Felipe, A. (2007) KV1.3/KV1.5 heteromeric channels compromise pharmacological responses in macrophages. Biochem. Biophys. Res. Commun. 352, 913-918
50. Fadool, D. A., and Levitan, I. B. (1998) Modulation of olfactory bulb neuron potassium current by tyrosine phosphorylation. J. Neurosci. 18, 6126-6137
51. Beeton, C., Smith, B. J., Sabo, J. K., Crossley, G., Nugent, D., Khaytin, I., Chi, V., Chandy, K. G., Pennington, M. W., and Norton, R. S. (2008) The D-diastereoisomer of ShK toxin selectively blocks voltage-gated K+ channels and inhibits T lymphocyte proliferation. J. Biol. Chem. 283, 988-997
52. Lanigan, M. D., Kalman, K., Lefievre, Y., Pennington, M. W., Chandy, K. G., and Norton, R. S. (2002) Mutating a critical lysine in ShK toxin alters its binding configuration in the pore-vestibule region of the voltage-gated potassium channel, KV1.3. Biochemistry 41, 11963-11971
53. Koshy, S., Wu, D., Hu, X., Tajhya, R. B., Huq, R., Khan, F. S., Pennington, M. W., Wulff, H., Yotnda, P., and Beeton, C. (2013) Blocking KCa3.1 channels increases tumor cell killing by a subset of human natural killer lymphocytes. PLoS ONE 8, e76740