Expression of T-cell KV1.3 potassium channel correlates with pro-inflammatory cytokines and disease activity in ulcerative colitis

Journal of Crohn's and Colitis

Volumn 8, Issue 11, 2014, Pages 1378-1391

  Koch Hansen, Lars ^a,c   Sevelsted Møller, Linda ^a,b   Rabjerg, Maj ^b   Larsen, Dorte ^a   Hansen, Tine Plato ^b   Klinge, Lone ^b   Wulff, Heike ^d   Knudsen, Torben ^c   Kjeldsen, Jens ^b   Köhler, Ralf ^a,e  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b ODENSE UNIVERSITY HOSPITAL   (Denmark)

^c ESBJERG HOSPITAL   (Denmark)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e INSTITUTO ARAGONÉS DE CIENCIAS DE LA SALUD   (Spain)

Author keywords

Colitis ulcerosa; ; Interleukins; ; KCa3.1; KCNA3; ; KCNN4; ; Novel treatment strategy;

Indexed keywords

AZATHIOPRINE; C REACTIVE PROTEIN; CALGRANULIN; CYTOKINE; GAMMA INTERFERON; GLUCOCORTICOID; INFLIXIMAB; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 2; MESSENGER RNA; POTASSIUM CHANNEL; POTASSIUM CHANNEL KCA3.1; POTASSIUM CHANNEL KV1.3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ACETAMIDE DERIVATIVE; BIOLOGICAL MARKER; CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; FC RECEPTOR; INTERMEDIATE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; KCNN4 PROTEIN, HUMAN; SENICAPOC; TRITYL DERIVATIVE;

ADULT; ARTICLE; CASE CONTROL STUDY; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COLON MUCOSA; CONTROLLED STUDY; CORTICOSTEROID THERAPY; CROSS-SECTIONAL STUDY; CYTOKINE PRODUCTION; DISEASE ACTIVITY; FEMALE; FOLLOW UP; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INFLAMMATION; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MALE; MONOCYTE; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RELAPSE; REMISSION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; ULCERATIVE COLITIS; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL PROLIFERATION; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION; GENETICS; IMMUNOLOGY; INTESTINE MUCOSA; LYMPHOCYTE; METABOLISM; MIDDLE AGED; PATHOLOGY; SEVERITY OF ILLNESS INDEX;

ACETAMIDES; ADULT; ANTIGENS, CD3; ANTIGENS, CD4; ANTIGENS, CD8; BIOMARKERS; CASE-CONTROL STUDIES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CELLS, CULTURED; COLITIS, ULCERATIVE; CROSS-SECTIONAL STUDIES; FEMALE; GENE EXPRESSION; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-17; INTERMEDIATE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; INTESTINAL MUCOSA; KV1.3 POTASSIUM CHANNEL; LYMPHOCYTES; MALE; MIDDLE AGED; RECEPTORS, IGG; RNA, MESSENGER; SEVERITY OF ILLNESS INDEX; TRITYL COMPOUNDS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84927786835     PISSN: 18739946     EISSN: 18764479     Source Type: Journal    
DOI: 10.1016/j.crohns.2014.04.003     Document Type: Article

References (57)

1. Sheth S.G., LaMont J.T. Toxic megacolon. Lancet 1998, 351(9101):509-513.
2. Neuman M.G., Nanau R.M. Inflammatory bowel disease: role of diet, microbiota, life style. Transl Res 2012, 160(1):29-44.
3. Lopez-Serrano P., Perez-Calle J.L., Perez-Fernandez M.T., Fernandez-Font J.M., Boixeda de Miguel D., Fernandez-Rodriguez C.M. Environmental risk factors in inflammatory bowel diseases. Investigating the hygiene hypothesis: a Spanish case-control study. Scand J Gastroenterol 2010, 45(12):1464-1471.
4. Porter C.K., Tribble D.R., Aliaga P.A., Halvorson H.A., Riddle M.S. Infectious gastroenteritis and risk of developing inflammatory bowel disease. Gastroenterology 2008, 135(3):781-786.
5. Halfvarson J., Bodin L., Tysk C., Lindberg E., Jarnerot G. Inflammatory bowel disease in a Swedish twin cohort: a long-term follow-up of concordance and clinical characteristics. Gastroenterology 2003, 124(7):1767-1773.
6. Orholm M., Binder V., Sorensen T.I., Rasmussen L.P., Kyvik K.O. Concordance of inflammatory bowel disease among Danish twins. Results of a nationwide study. Scand J Gastroenterol 2000, 35(10):1075-1081.
7. Wen Z., Fiocchi C. Inflammatory bowel disease: autoimmune or immune-mediated pathogenesis?. Clin Dev Immunol 2004, 11(3-4):195-204.
8. Patel D.D., Lee D.M., Kolbinger F., Antoni C. Effect of IL-17A blockade with secukinumab in autoimmune diseases. Ann Rheum Dis 2013, 72(Suppl. 2):ii116-ii123.
9. Holmen N., Lundgren A., Lundin S., Bergin A.M., Rudin A., Sjovall H., et al. Functional CD4+CD25high regulatory T cells are enriched in the colonic mucosa of patients with active ulcerative colitis and increase with disease activity. Inflamm Bowel Dis 2006, 12(6):447-456.
10. Schoenborn J.R., Wilson C.B. Regulation of interferon-gamma during innate and adaptive immune responses. Adv Immunol 2007, 96:41-101.
11. Feghali C.A., Wright T.M. Cytokines in acute and chronic inflammation. Front Biosci 1997, 2:d12-d26.
12. Ouyang W., Kolls J.K., Zheng Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 2008, 28(4):454-467.
13. Fuss I.J., Neurath M., Boirivant M., Klein J.S., de la Motte C., Strong S.A., et al. Disparate CD4+ lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease. Crohn's disease LP cells manifest increased secretion of IFN-gamma, whereas ulcerative colitis LP cells manifest increased secretion of IL-5. J Immunol 1996, 157(3):1261-1270.
14. Tsukada Y., Nakamura T., Iimura M., Iizuka B.E., Hayashi N. Cytokine profile in colonic mucosa of ulcerative colitis correlates with disease activity and response to granulocytapheresis. Am J Gastroenterol 2002, 97(11):2820-2828.
15. Ordas I., Eckmann L., Talamini M., Baumgart D.C., Sandborn W.J. Ulcerative colitis. Lancet 2012, 380(9853):1606-1619.
16. Danese S., Fiocchi C. Ulcerative colitis. N Engl J Med 2011, 365(18):1713-1725.
17. Mosmann T.R., Coffman R.L. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol 1989, 7:145-173.
18. Fuss I.J., Heller F., Boirivant M., Leon F., Yoshida M., Fichtner-Feigl S., et al. Nonclassical CD1d-restricted NK T cells that produce IL-13 characterize an atypical Th2 response in ulcerative colitis. J Clin Invest 2004, 113(10):1490-1497.
19. Cahalan M.D., Chandy K.G. The functional network of ion channels in T lymphocytes. Immunol Rev 2009, 231(1):59-87.
20. Feske S., Prakriya M., Rao A., Lewis R.S. A severe defect in CRAC Ca2+ channel activation and altered K+channel gating in T cells from immunodeficient patients. J Exp Med 2005, 202(5):651-662.
21. Shaw P.J., Qu B., Hoth M., Feske S. Molecular regulation of CRAC channels and their role in lymphocyte function. Cell Mol Life Sci 2013, 70(15):2637-2656.
22. Oh-hora M., Rao A. Calcium signaling in lymphocytes. Curr Opin Immunol 2008, 20(3):250-258.
23. Chi V., Pennington M.W., Norton R.S., Tarcha E.J., Londono L.M., Sims-Fahey B., et al. Development of a sea anemone toxin as an immunomodulator for therapy of autoimmune diseases. Toxicon 2012, 59(4):529-546.
24. Rus H., Pardo C.A., Hu L., Darrah E., Cudrici C., Niculescu T., et al. The voltage-gated potassium channel Kv1.3 is highly expressed on inflammatory infiltrates in multiple sclerosis brain. Proc Natl Acad Sci U S A 2005, 102(31):11094-11099.
25. Wulff H., Calabresi P.A., Allie R., Yun S., Pennington M., Beeton C., et al. The voltage-gated Kv1.3K(+) channel in effector memory T cells as new target for MS. J Clin Invest 2003, 111(11):1703-1713.
26. Beeton C., Wulff H., Standifer N.E., Azam P., Mullen K.M., Pennington M.W., et al. Kv1.3 channels are a therapeutic target for T cell-mediated autoimmune diseases. Proc Natl Acad Sci U S A 2006, 103(46):17414-17419.
27. Gocke A.R., Lebson L.A., Grishkan I.V., Hu L., Nguyen H.M., Whartenby K.A., et al. Kv1.3 deletion biases T cells toward an immunoregulatory phenotype and renders mice resistant to autoimmune encephalomyelitis. J Immunol 2012, 188(12):5877-5886.
28. Hyodo T., Oda T., Kikuchi Y., Higashi K., Kushiyama T., Yamamoto K., et al. Voltage-gated potassium channel Kv1.3 blocker as a potential treatment for rat anti-glomerular basement membrane glomerulonephritis. Am J Physiol Renal Physiol 2010, 299(6):F1258-F1269.
29. Wulff H., Pennington M. Targeting effector memory T-cells with Kv1.3 blockers. Curr Opin Drug Discov Devel 2007, 10(4):438-445.
30. Al-Hazza A., Linley J.E., Aziz Q., Maclennan K.A., Hunter M., Sandle G.I. Potential role of reduced basolateral potassium (IKCa3.1) channel expression in the pathogenesis of diarrhoea in ulcerative colitis. J Pathol 2011.
31. Izu L.T., McCulle S.L., Ferreri-Jacobia M.T., Devor D.C., Duffey M.E. Vasoactive intestinal peptide-stimulated Cl- secretion: activation of cAMP-dependent K+ channels. J Membr Biol 2002, 186(3):145-157.
32. Schroeder K.W., Tremaine W.J., Ilstrup D.M. Coated oral 5-aminosalicylic acid therapy for mildly to moderately active ulcerative colitis. A randomized study. N Engl J Med 1987, 317(26):1625-1629.
33. Morson B.C., Dawson I.M.P. Gastrointestinal pathology 1979, 551-562. Blackwell Scientific, Oxford. 2nd Edition.
34. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 2009, 55(4):611-622.
35. Carpenter A.E., Jones T.R., Lamprecht M.R., Clarke C., Kang I.H., Friman O., et al. Cell Profiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 2006, 7(10):R100.
36. Schmitz A., Sankaranarayanan A., Azam P., Schmidt-Lassen K., Homerick D., Hansel W., et al. Design of PAP-1, a selective small molecule Kv1.3 blocker, for the suppression of effector memory T cells in autoimmune diseases. Mol Pharmacol 2005, 68(5):1254-1270.
37. Ataga K.I., Stocker J. Senicapoc (ICA-17043): a potential therapy for the prevention and treatment of hemolysis-associated complications in sickle cell anemia. Expert Opin Investig Drugs 2009, 18(2):231-239.
38. Stocker J.W., De Franceschi L., McNaughton-Smith G.A., Corrocher R., Beuzard Y., Brugnara C. ICA-17043, a novel Gardos channel blocker, prevents sickled red blood cell dehydration in vitro and in vivo in SAD mice. Blood 2003, 101(6):2412-2418.
39. Matos J.E., Sausbier M., Beranek G., Sausbier U., Ruth P., Leipziger J. Role of cholinergic-activated KCa1.1 (BK), KCa3.1 (SK4) and KV7.1 (KCNQ1) channels in mouse colonic Cl-secretion. Acta Physiol 2007, 189(3):251-258.
40. Morgan A.J., Jacob R. Ionomycin enhances Ca2+ influx by stimulating store-regulated cation entry and not by a direct action at the plasma membrane. Biochem J 1994, 300(Pt 3):665-672.
41. Toldi G., Vasarhelyi B., Kaposi A., Meszaros G., Panczel P., Hosszufalusi N., et al. Lymphocyte activation in type 1 diabetes mellitus: the increased significance of Kv1.3 potassium channels. Immunol Lett 2010, 133(1):35-41.
42. Olsen T., Rismo R., Cui G., Goll R., Christiansen I., Florholmen J. TH1 and TH17 interactions in untreated inflamed mucosa of inflammatory bowel disease, and their potential to mediate the inflammation. Cytokine 2011, 56(3):633-640.
43. Akazawa A., Sakaida I., Higaki S., Kubo Y., Uchida K., Okita K. Increased expression of tumor necrosis factor-alpha messenger RNA in the intestinal mucosa of inflammatory bowel disease, particularly in patients with disease in the inactive phase. J Gastroenterol 2002, 37(5):345-353.
44. Caprioli F., Bose F., Rossi R.L., Petti L., Vigano C., Ciafardini C., et al. Reduction of CD68+ macrophages and decreased IL-17 expression in intestinal mucosa of patients with inflammatory bowel disease strongly correlate with endoscopic response and mucosal healing following infliximab therapy. Inflamm Bowel Dis 2013, 19(4):729-739.
45. O'Connor W., Kamanaka M., Booth C.J., Town T., Nakae S., Iwakura Y., et al. A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat Immunol 2009, 10(6):603-609.
46. Azam P., Sankaranarayanan A., Homerick D., Griffey S., Wulff H. Targeting effector memory T cells with the small molecule Kv1.3 blocker PAP-1 suppresses allergic contact dermatitis. J Invest Dermatol 2007, 127(6):1419-1429.
47. Matsuzaki K., Hokari R., Kato S., Tsuzuki Y., Tanaka H., Kurihara C., et al. Differential expression of CCR5 and CRTH2 on infiltrated cells in colonic mucosa of patients with ulcerative colitis. J Gastroenterol Hepatol 2003, 18(9):1081-1088.
48. Heller F., Florian P., Bojarski C., Richter J., Christ M., Hillenbrand B., et al. Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology 2005, 129(2):550-564.
49. Calloway N., Vig M., Kinet J.P., Holowka D., Baird B. Molecular clustering of STIM1 with Orai1/CRACM1 at the plasma membrane depends dynamically on depletion of Ca2+ stores and on electrostatic interactions. Mol Biol Cell 2009, 20(1):389-399.
50. Arimilli S., Sharma S.K., Yammani R., Reid S.D., Parks G.D., Alexander-Miller M.A. Pivotal advance: nonfunctional lung effectors exhibit decreased calcium mobilization associated with reduced expression of ORAI1. J Leukoc Biol 2010, 87(6):977-988.
51. Lam J., Wulff H. The lymphocyte potassium channels Kv1.3 and KCa3.1 as targets for immunosuppression. Drug Dev Res 2011, 72(7):573-584.
52. Kuras Z., Yun Y.H., Chimote A.A., Neumeier L., Conforti L. KCa3.1 and TRPM7 channels at the uropod regulate migration of activated human T cells. PLoS One 2012, 7(8):e43859.
53. Ghanshani S., Wulff H., Miller M.J., Rohm H., Neben A., Gutman G.A., et al. Up-regulation of the IKCa1 potassium channel during T-cell activation. Molecular mechanism and functional consequences. J Biol Chem 2000, 275(47):37137-37149.
54. Wulff H., Castle N.A. Therapeutic potential of KCa3.1 blockers: recent advances and promising trends. Expert review of clinical. Pharmacology 2010, 3(3):385-396.
55. Warth R., Hamm K., Bleich M., Kunzelmann K., von Hahn T., Schreiber R., et al. Molecular and functional characterization of the small Ca(2+)-regulated K+channel (rSK4) of colonic crypts. Pflugers Arch 1999, 438(4):437-444.
56. Di L., Srivastava S., Zhdanova O., Ding Y., Li Z., Wulff H., et al. Inhibition of the K+ channel KCa3.1 ameliorates T cell-mediated colitis. Proc Natl Acad Sci U S A 2010, 107(4):1541-1546.
57. Strobaek D., Brown D.T., Jenkins D.P., Chen Y.J., Coleman N., Ando Y., et al. NS6180, a new K(Ca) 3.1 channel inhibitor prevents T-cell activation and inflammation in a rat model of inflammatory bowel disease. Br J Pharmacol 2013, 168(2):432-444.