Inhibition of Kv channel expression by NSAIDs depolarizes membrane potential and inhibits cell migration by disrupting calpain signaling

Biochemical Pharmacology

Volumn 98, Issue 4, 2015, Pages 614-628

  Silver, Kristopher ^a   Littlejohn, Alaina ^a   Thomas, Laurel ^a   Marsh, Elizabeth ^a   Lillich, James D ^a  

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

Calpain; Cell migration; Membrane potential; NSAID; Voltage gated potassium channel

Indexed keywords

CALPAIN; INDOMETACIN; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; NONSTEROID ANTIINFLAMMATORY AGENT; VOLTAGE GATED POTASSIUM CHANNEL; KCNA6 PROTEIN, RAT; POTASSIUM CHANNEL KV1.3; POTASSIUM CHANNEL KV1.4; POTASSIUM CHANNEL KV1.6;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL MIGRATION; CONTROLLED STUDY; EPITHELIUM CELL; GASTROINTESTINAL TOXICITY; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; INTESTINE EPITHELIUM CELL; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CELL MOTION; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CALPAIN; CELL LINE; CELL MOVEMENT; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; KV1.3 POTASSIUM CHANNEL; KV1.4 POTASSIUM CHANNEL; KV1.6 POTASSIUM CHANNEL; MEMBRANE POTENTIALS; POTASSIUM CHANNELS, VOLTAGE-GATED; RATS; SIGNAL TRANSDUCTION;

EID: 84947281702     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2015.10.017     Document Type: Article

References (77)

1. C. Sostres, C.J. Gargallo, and A. Lanas Nonsteroidal anti-inflammatory drugs and upper and lower gastrointestinal mucosal damage Arthritis Res. Ther. 15 2013
2. J.L. Wallace Mechanisms, prevention and clinical implications of nonsteroidal anti-inflammatory drug-enteropathy World J. Gastroenterol. 19 2013 1861 1876
3. G. Singh Gastrointestinal complications of prescription and over-the-counter nonsteroidal anti-inflammatory drugs: a view from the ARAMIS database. Arthritis, Rheumatism, and Aging Medical Information System Am. J. Ther. 7 2000 115 122
4. W. Tomisato, S. Tsutsumi, T. Hoshino, H.J. Hwang, M. Mio, T. Tsuchiya, and et al. Role of direct cytotoxic effects of NSAIDs in the induction of gastric lesions Biochem. Pharmacol. 67 2004 575 585
5. L.M. Lichtenberger Where is the evidence that cyclooxygenase inhibition is the primary cause of neonsteroidal anti-inflammatory drug (NSAID)-induced gastrointestinal injury? Topical injury revisited Biochem. Pharmacol. 61 2001 631 637
6. J.L. Wallace, and L. Vong NSAID-induced gastrointestinal damage and the design of GI-sparing NSAIDs Curr. Opin. Investig. Drugs 9 2008 1151 1156
7. L.F. Karcher, S.G. Dill, W.I. Anderson, and J.M. King Right dorsal colitis J. Vet. Intern. Med. 4 1990 247 253
8. L.H. Israel, J.B. Koea, I.D. Stewart, C.L. Wright, and P.D. Frankish Nonsteroidal anti-inflammatory drug-induced strictures of the colon Dis. Colon Rectum 44 2001 1362 1364
9. C.G. MacAllister, S.J. Morgan, A.T. Borne, and R.A. Pollet Comparison of adverse effects of phenylbutazone, flunixin meglumine, and ketoprofen in horses J. Am. Vet. Med. Assoc. 202 1993 71 77
10. D. Little, S.A. Brown, N.B. Campbell, A.J. Moeser, J.L. Davis, and A.T. Blikslager Effects of the cyclooxygenase inhibitor meloxicam on recovery of ischemia-injured equine jejunum Am. J. Vet. Res. 68 2007 614 624
11. T. Mahmud, S.S. Rafi, D.L. Scott, J.M. Wrigglesworth, and I. Bjarnason Nonsteroidal antiinflammatory drugs and uncoupling of mitochondrial oxidative phosphorylation Arthritis Rheumatol. 39 1996 1998 2003
12. S. Somasundaram, G. Sigthorsson, R.J. Simpson, J. Watts, M. Jacob, I.A. Tavares, and et al. Uncoupling of intestinal mitochondrial oxidative phosphorylation and inhibitiion of cyclooxygenase are required for the development of NSAID-enteropathy in the rat Aliment Pharmacol. Ther. 14 2000 639 650
13. M. Ashton, and P.J. Hanson Disparate effects of non-steroidal anti-inflammatory drugs on apoptosis in guinea pig gastric mucous cells: inhibition of basal apoptosis by diclofenac Br. J. Pharmacol. 135 2002 407 416
14. R. Pai, I.L. Szabo, A.Q. Giap, H. Kawanaka, and A.S. Tarnawski Nonsteroidal anti-inflammatory drugs inhibit re-epithelialization of wounded gastric monolayers by interfering with actin, Src, FAK, and tensin signaling Life Sci. 69 2001 3055 3071
15. N.N. Raveendran, K. Silver, L.C. Freeman, D. Narvaez, K. Weng, S. Ganta, and et al. Drug-induced alterations to gene and protein expression in intestinal epithelial cell 6 cells suggest a role for calpains in the gastrointestinal toxicity of nonsteroidal anti-inflammatory agents J. Pharmacol. Exp. Ther. 325 2008 389 399
16. A. Schmassmann, A.S. Tarnawski, B.M. Peskar, L. Varga, B. Flogerzi, and F. Halter Influence of acid and angiogenesis on kinetics of gastric ulcer healing in rats: interaction with indomethacin Am. J. Physiol. Gastrointest. Liver Physiol. 268 1995 G276 G285
17. A.G. Penney, C. Malcontenti-Wilson, P.E. O'Brien, and F.J. Andrews NSAID-induced delay in gastric ulcer healing is not associated with decreased epithelial cell proliferation in rats Dig. Dis. Sci. 40 1995 2684 2693
18. + channels contribute to NSAID-inhibition of intestinal restitution Biochem. Pharmacol. 74 2007 74 85
19. A.U. Dignass Mechanisms and modulation of intestinal epithelial repair Inflamm. Bowel Dis. 7 2001 68 77
20. W.-M. Qi, K. Yamamoto, Y. Yokoo, H. Miyata, T. Inamoto, K.G.S. Udayanga, and et al. Histoplanimetrical study on the relationship between the cell kinetics of villus columnar epithelial cells and the proliferation of indigenous bacteria in rat small intestine J. Vet. Med. Sci. 71 2009 463 470
21. H. Han, T. Iwanaga, and T. Fujita Species-differences in the process of apoptosis in epithelial cells of the small intestine: an ultrastructural and cytochemical study of luminal cell elements Arch. Histol. Cytol. 56 1993 83 90
22. S. Onishi, H. Miyata, T. Inamoto, W.M. Qi, K. Yamamoto, T. Yokoyama, and et al. Immunohistochemical study on the delayed progression of epithelial apoptosis in follicle-associated epithelium of rat Peyer's patch J. Vet. Med. Sci. 69 2007 1123 1129
23. T. Shibahara, N. Sato, S. Waguri, T. Iwanaga, A. Nakahara, H. Fukutomi, and et al. The fate of effete epithelial cells at the villus tips of the human small intestine Arch. Histol. Cytol. 58 1995 205 219
24. T. Takeuchi, H. Kitagawa, T. Imagawa, and M. Uehara Proliferation and cellular kinetics of villous epithelial cells and M cells in the chicken caecum J. Anat. 193 1998 233 239
25. T. Takeuchi, H. Kitagawa, T. Imagawa, and M. Uehara Apoptosis of villous epithelial cells and follicle-associated epithelial cells in chicken cecum J. Vet. Med. Sci. 61 1999 149 154
26. ATP opener, accelerates restitution of ethanol or indomethacin-induced gastric ulceration in rats independent of polyamines J. Gastroenterol. Hepatol. 16 2001 290 296
27. K. Silver, A. Desormaux, L.C. Freeman, and J.D. Lillich Expression of pleiotrophin, an important regulator of cell migration, is inhibited in intestinal epithelial cells by treatment with non-steroidal anti-inflammatory drugs Growth Factors 30 2012 258 266
28. K. Silver, L. Leloup, L.C. Freeman, A. Wells, and J.D. Lillich Non-steroidal anti-inflammatory drugs inhibit calpain activity and membrane localization of calpain 2 protease Int. J. Biochem. Cell Biol. 42 2010 2030 2036
29. A. Schwab, A. Fabian, P.J. Hanley, and C. Stock Role of ion channels and transporters in cell migration Physiol. Rev. 92 2012 1865 1913
30. C. Stock, F.T. Ludwig, P.J. Hanley, and A. Schwab Roles of ion transport in control of cell motility Compr. Physiol. 3 2013 59 119
31. + channels and increased migration of differentiated intestinal epithelial cells after wounding Am. J. Physiol. Cell Physiol. 282 2002 C885 C898
32. v1.3, is expressed in epithelia Biochim. Biophys. Acta 1616 2003 85 94
33. ir2.1 expressions in human macrophages and affects the membrane potential and foam cell formation J. South Med. Univ. 32 2012 1067 1073
34. v1. 3 in rabbit ciliary epithelium regulates the membrane potential via coupling intracellular calcium Chin. Med. J. 121 2008 2272 2277
35. v1.3 channels and beta1 integrins J. Exp. Med. 191 2000 1167 1176
36. v1.3 voltage-dependent potassium channels Biochem. Pharmacol. 80 2010 858 866
37. + channel pathway participates in the antinociceptive effect of diclofenac, but not of indomethacin Pharmacol. Biochem. Behav. 76 2003 187 195
38. M.I. Ortiz, J.E. Torres-Lopez, G. Castaneda-Hernandez, R. Rosas, G.C. Vidal-Cantu, and V. Granados-Soto Pharmacological evidence for the activation of K(+) channels by diclofenac Eur. J. Pharmacol. 438 2002 85 91
39. A. Gwanyanya, R. Mcaclanskiene, and K. Mubagwa Insights into the effects of diclofenac and other non-steroidal anti-inflammatory agents on ion channels J. Pharm. Pharmacol. 64 2012 1359 1375
40. A. Quaroni, J. Wands, R.L. Trelstad, and K.J. Isselbacher Epithelioid cell cultures from rat small intestine: characterization by morphologic and immunologic criteria J. Cell Biol. 80 1979 248 265
41. S.A. McCormack, and L.R. Johnson Polyamines and cell migration J. Physiol. Pharmacol. 52 2001 327 349
42. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔC(T) method Methods 25 2001 402 408
43. + channel with an ABC transporter Neuron 26 2000 155 167
44. ATP channels Neuron 22 1999 537 548
45. A. Glading, P. Chang, D.A. Lauffenburger, and A. Wells Epidermal growth factor receptor activation of calpain is required for fibroblast motility and occurs via an ERK/MAP kinase signaling pathway J. Biol. Chem. 275 2000 2390 2398
46. 2+-RhoA signaling pathway required for polyamine-dependent intestinal epithelial cell migration Am. J. Physiol. Cell Physiol. 280 2001 C993 C1007
47. + channel expression in polyamine-dependent intestinal epithelial cell migration Am. J. Physiol. Cell Physiol. 278 2000 C303 C314
48. v1.3 voltage-gated potassium channels and beta(1)-integrins on the plasma membrane of melanoma cells: effects of cell adherence and channel blockers J. Gen. Physiol. 120 2002 29 37
49. C. Vogel, and E.M. Marcotte Insights into the regulation of protein abundance from proteomic and transcriptomic analyses Nat. Rev. Genet. 13 2012 227 232
50. v1.3 K(+) channel in effector memory T cells as new target for MS J. Clin. Investig. 111 2003 1703 1713
51. v1.3 channels are a therapeutic target for T cell-mediated autoimmune diseases Proc. Natl. Acad. Sci. U. S. A. 103 2006 17414 17419
52. L.I. Brueggemann, B.K. Mani, A.R. Mackie, L.L. Cribbs, and K.L. Byron Novel actions of nonsteroidal anti-inflammatory drugs on vascular ion channels: accounting for cardiovascular side effects and identifying new therapeutic applications Mol. Cell. Pharmacol. 2 2010 15 19
53. Y. Benyamin The structural basis of calpain behavior FEBS J. 273 2006 3413 3414
54. A. Glading, D.A. Lauffenburger, and A. Wells Cutting to the chase: calpain proteases in cell motility Trends Cell Biol. 12 2002 46 54
55. M.-C. Lebart, and Y. Benyamin Calpain involvement in the remodeling of cytoskeletal anchorage complexes FEBS J. 273 2006 3415 3426
56. M.A. Lokuta, P.A. Nuzzi, and A. Huttenlocher Calpain regulates neutrophil chemotaxis Proc. Natl. Acad. Sci. U. S. A. 100 2003 4006 4011
57. B.J. Perrin, and A. Huttenlocher Calpain Int. J. Biochem. Cell Biol. 34 2002 722 725
58. L. Leloup, and A. Wells Calpains as potential anti-cancer targets Expert Opin. Ther. Targets 15 2011 309 323
59. M. Kato, S. Nishida, H. Kitasato, N. Sakata, and S. Kawai Cyclooxygenase-1 and cyclooxygenase-2 selectivity of non-steroidal anti-inflammatory drugs: investigation using human peripheral monocytes J. Pharm. Pharmacol. 53 2001 1679 1685
60. B.M. Peskar, N. Maricic, B. Gretzera, R. Schuligoi, and A. Schmassmann Role of cyclooxygenase-2 in gastric mucosal defense Life Sci. 69 2001 2993 3003
61. I.A. Tavares The effects of meloxicam, indomethacin or NS-398 on eicosanoid synthesis by fresh human gastric mucosa Aliment Pharmacol. Ther. 14 2000 795 799
62. T. Brzozowski, P.C. Konturek, S.J. Konturek, Z. Sliwowski, R. Pajdo, D. Drozdowicz, and et al. Classic NSAID and selective cyclooxygenase (COX)-1 and COX-2 inhibitors in healing of chronic gastric ulcers Microsc. Res. Tech. 53 2001 343 353
63. C.J. Smith, Y. Zhang, C.M. Koboldt, J. Muhammad, B.S. Zweifel, A. Shaffer, and et al. Pharmacological analysis of cyclooxygenase-1 in inflammation Proc. Natl. Acad. Sci. U. S. A. 95 1998 13313 13318
64. A. Tanaka, H. Araki, Y. Komoike, S. Hase, and K. Takeuchi Inhibition of both COX-1 and COX-2 is required for development of gastric damage in response to nonsteroidal antiinflammatory drugs J. Physiol. 95 2001 21 27
65. E.R. Kokoska, G.S. Smith, Y. Deshpande, A.B. Wolff, and T.A. Miller Indomethacin increases susceptibility to injury in human gastric cells independent of PG synthesis inhibition Am. J. Physiol. Gastrointest. Liver Physiol. 275 1998 G620 G628
66. G. Alvan, M. Orme, L. Bertilsson, R. Ekstrand, and L. Palmer Pharmacokinetics of indomethacin Clin. Pharmacol. Ther. 18 1975 364 373
67. D.E. Duggan, A.F. Hogans, K.C. Kwan, and F.G. McMahon The metabolism of indomethacin in man J. Pharmacol. Exp. Ther. 181 1972 563 575
68. C. Brideau, S. Kargman, S. Liu, A.L. Dallob, E.W. Ehrich, I.W. Rodger, and et al. A human whole blood assay for clinical evaluation of biochemical efficacy of cyclooxygenase inhibitors Inflamm. Res. 45 1996 68 74
69. C. Brideau, S. Van, C. taden, and C.C. Chan In vitro effects of cyclooxygenase inhibitors in whole blood of horses, dogs, and cats Am. J. Vet. Res. 62 2001 1755 1760
70. D. Riendeau, M.D. Percival, C. Brideau, S. Charleson, D. Dube, D. Ethier, and et al. Etoricoxib (MK-0663): preclinical profile and comparison with other agents that selectively inhibit cyclooxygenase-2 J. Pharmacol. Exp. Ther. 296 2001 558 566
71. H.H. Frey, and M.A. El-Sayed Concentrations of acidic antiinflammatory drugs in gastric mucosa Arch. Int. Pharmacodyn. Ther. 230 1977 300 308
72. T. Suzuki, T. Suganuma, R. Shimizu, M. Aoki, and M. Hanano Relationship between pharmacokinetics and the analgesic effect of indomethacin in the rat Biol. Pharm. Bull. 20 1997 438 442
73. L.M. Lichtenberger, D. Bhattarai, T.M. Phan, E.J. Dial, and K. Uray Suppression of contractile activity in the small intestine by indomethacin and omeprazole Am. J. Physiol. Gastrointest. Liver Physiol. 308 2015 G785 G793
74. R.R. Petchi, S. Parasuraman, C. Vijaya, S.V. Gopala Krishna, and M.K. Kumar Antiarthritic activity of a polyherbal formulation against Freund's complete adjuvant induced arthritis in Female Wistar rats J. Basic Clin. Pharm. 6 2015 77 83
75. C. Pozzoli, A. Menozzi, D. Grandi, E. Solenghi, M.C. Ossiprandi, C. Zullian, and et al. Protective effects of proton pump inhibitors against indomethacin-induced lesions in the rat small intestine Naunyn Schmiedebergs Arch. Pharmacol. 374 2007 283 291
76. C. Euchenhofer, C. Maihofner, K. Brune, I. Tegeder, and G. Geisslinger Differential effect of selective cyclooxygenase-2 (COX-2) inhibitor NS 398 and diclofenac on formalin-induced nociception in the rat Neurosci. Lett. 248 1998 25 28
77. M.F. Prescott, C.K. McBride, C.M. Venturini, and S.C. Gerhardt Leukocyte stimulation of intimal lesion formation is inhibited by treatment with diclofenac sodium and dexamethasone J. Cardiovasc. Pharmacol. 14 Suppl. 6 1989 S76 S81