Inhibition of cAMP-Activated Intestinal Chloride Secretion by Diclofenac: Cellular Mechanism and Potential Application in Cholera

PLoS Neglected Tropical Diseases

Volumn 8, Issue 9, 2014, Pages

  Pongkorpsakol, Pawin ^a   Pathomthongtaweechai, Nutthapoom ^a   Srimanote, Potjanee ^b   Soodvilai, Sunhapas ^a   Chatsudthipong, Varanuj ^a   Muanprasat, Chatchai ^a  

^a Mahidol University ^*  (Thailand)

^b THAMMASAT UNIVERSITY   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CHLORIDE CHANNEL; CHLORIDE ION; CHOLERA TOXIN; CYCLIC AMP; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DICLOFENAC; POTASSIUM CHANNEL; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; CALCIUM; CFTR PROTEIN, HUMAN; CHLORIDE; POTASSIUM CHANNEL BLOCKING AGENT;

ANIMAL MODEL; ANIMAL TISSUE; ANTIDIARRHEAL ACTIVITY; ARTICLE; CELL CULTURE; CELL VIABILITY; CHLORIDE CURRENT; CHOLERA; CONTROLLED STUDY; ELECTROPHYSIOLOGICAL PROCEDURES; HUMAN; HUMAN CELL; IC50; INTESTINAL SECRETION; INTESTINE ABSORPTION; INTESTINE CELL; INTESTINE EPITHELIUM; INTESTINE FLUID; MOUSE; NONHUMAN; PERMEABILITY BARRIER; VIBRIO CHOLERAE; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CELL SURVIVAL; DRUG EFFECTS; EPITHELIUM CELL; GENETICS; INTESTINE MUCOSA; MALE; METABOLISM; PATHOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CALCIUM; CELL LINE; CELL SURVIVAL; CHLORIDES; CHOLERA; CHOLERA TOXIN; CYCLIC AMP; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DICLOFENAC; EPITHELIAL CELLS; HUMANS; INTESTINAL MUCOSA; MALE; MICE; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS;

EID: 84907587752     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003119     Document Type: Article

References (38)

1. Barrett KE, Keely SJ, (2000) Chloride secretion by the intestinal epithelium: molecular basis and regulatory aspects. Annu Rev Physiol 62: 535–572.
2. Field M, (2003) Intestinal ion transport and the pathophysiology of diarrhea. J Clin Invest 111: 931–943.
3. Kunzelmann K, Mall M, (2002) Electrolyte transport in the mammalian colon: mechanisms and implications for disease. Physiol Rev 82: 245–289.
4. Preston P, Wartosch L, Gunzel D, Fromm M, Kongsuphol P, et al. (2010) Disruption of the K+ channel beta-subunit KCNE3 reveals an important role in intestinal and tracheal Cl- transport. J Biol Chem 285: 7165–7175.
5. Vallon V, Grahammer F, Volkl H, Sandu CD, Richter K, et al. (2005) KCNQ1-dependent transport in renal and gastrointestinal epithelia. Proc Natl Acad Sci U S A 102: 17864–17869.
6. Thiagarajah JR, Verkman AS, (2012) CFTR inhibitors for treating diarrheal disease. Clin Pharmacol Ther 92: 287–290.
7. Hoque KM, Woodward OM, van Rossum DB, Zachos NC, Chen L, et al. (2010) Epac1 mediates protein kinase A-independent mechanism of forskolin-activated intestinal chloride secretion. J Gen Physiol 135: 43–58.
8. Verkman AS, Galietta LJ, (2009) Chloride channels as drug targets. Nat Rev Drug Discov 8: 153–171.
9. Harris JB, LaRocque RC, Qadri F, Ryan ET, Calderwood SB, (2012) Cholera. Lancet 379: 2466–2476.
10. Hodges K, Gill R, (2010) Infectious diarrhea: Cellular and molecular mechanisms. Gut Microbes 1: 4–21.
11. Sack DA, Sack RB, Nair GB, Siddique AK, (2004) Cholera. Lancet 363: 223–233.
12. Muanprasat C, Chatsudthipong V, (2013) Cholera: pathophysiology and emerging therapeutic targets. Future Med Chem 5: 781–798.
13. Muanprasat C, Kaewmokul S, Chatsudthipong V, (2007) Identification of new small molecule inhibitors of cystic fibrosis transmembrane conductance regulator protein: in vitro and in vivo studies. Biol Pharm Bull 30: 502–507.
14. Muanprasat C, Sonawane ND, Salinas D, Taddei A, Galietta LJ, et al. (2004) Discovery of glycine hydrazide pore-occluding CFTR inhibitors: mechanism, structure-activity analysis, and in vivo efficacy. J Gen Physiol 124: 125–137.
15. Muanprasat C, Sirianant L, Soodvilai S, Chokchaisiri R, Suksamrarn A, et al. (2012) Novel Action of the Chalcone Isoliquiritigenin as a Cystic Fibrosis Transmembrane Conductance Regulator (CFTR) Inhibitor: Potential Therapy for Cholera and Polycystic Kidney Disease. J Pharmacol Sci 118: 82–91.
16. Luerang W, Khammee T, Kumpum W, Suksamrarn S, Chatsudthipong V, et al. (2012) Hydroxyxanthone as an inhibitor of cAMP-activated apical chloride channel in human intestinal epithelial cell. Life Sci 90: 988–994.
17. Sawasvirojwong S, Srimanote P, Chatsudthipong V, Muanprasat C, (2013) An Adult Mouse Model of -induced Diarrhea for Studying Pathogenesis and Potential Therapy of Cholera. PLoS Negl Trop Dis 7: e2293.
18. Gwanyanya A, Macianskiene R, Mubagwa K, (2012) Insights into the effects of diclofenac and other non-steroidal anti-inflammatory agents on ion channels. J Pharm Pharmacol 64: 1359–1375.
19. Devor DC, Schultz BD, (1998) Ibuprofen inhibits cystic fibrosis transmembrane conductance regulator-mediated Cl- secretion. J Clin Invest 102: 679–687.
20. McCarty NA, McDonough S, Cohen BN, Riordan JR, Davidson N, et al. (1993) Voltage-dependent block of the cystic fibrosis transmembrane conductance regulator Cl- channel by two closely related arylaminobenzoates. J Gen Physiol 102: 1–23.
21. Voilley N, de Weille J, Mamet J, Lazdunski M, (2001) Nonsteroid anti-inflammatory drugs inhibit both the activity and the inflammation-induced expression of acid-sensing ion channels in nociceptors. J Neurosci 21: 8026–8033.
22. Carmosino M, Rizzo F, Torretta S, Procino G, Svelto M, (2013) High-throughput fluorescent-based NKCC functional assay in adherent epithelial cells. BMC Cell Biol 14: 16.
23. Zhu Y, Zhang QY, (2012) Role of intestinal cytochrome p450 enzymes in diclofenac-induced toxicity in the small intestine. J Pharmacol Exp Ther 343: 362–370.
24. Linder CD, Renaud NA, Hutzler JM, (2009) Is 1-aminobenzotriazole an appropriate in vitro tool as a nonspecific cytochrome P450 inactivator? Drug Metab Dispos 37: 10–13.
25. Hallows KR, Raghuram V, Kemp BE, Witters LA, Foskett JK, (2000) Inhibition of cystic fibrosis transmembrane conductance regulator by novel interaction with the metabolic sensor AMP-activated protein kinase. J Clin Invest 105: 1711–1721.
26. Kongsuphol P, Cassidy D, Hieke B, Treharne KJ, Schreiber R, et al. (2009) Mechanistic insight into control of CFTR by AMPK. J Biol Chem 284: 5645–5653.
27. Sheppard DN, Welsh MJ, (1999) Structure and function of the CFTR chloride channel. Physiol Rev 79: S23–45.
28. Luo J, Pato MD, Riordan JR, Hanrahan JW, (1998) Differential regulation of single CFTR channels by PP2C, PP2A, and other phosphatases. Am J Physiol 274: C1397–1410.
29. Li C, Krishnamurthy PC, Penmatsa H, Marrs KL, Wang XQ, et al. (2007) Spatiotemporal coupling of cAMP transporter to CFTR chloride channel function in the gut epithelia. Cell 131: 940–951.
30. Worrell RT, Frizzell RA, (1991) CaMKII mediates stimulation of chloride conductance by calcium in T84 cells. Am J Physiol 260: C877–882.
31. Reagan-Shaw S, Nihal M, Ahmad N, (2008) Dose translation from animal to human studies revisited. FASEB J 22: 659–661.
32. Rufo PA, Merlin D, Riegler M, Ferguson-Maltzman MH, Dickinson BL, et al. (1997) The antifungal antibiotic, clotrimazole, inhibits chloride secretion by human intestinal T84 cells via blockade of distinct basolateral K+ conductances. Demonstration of efficacy in intact rabbit colon and in an in vivo mouse model of cholera. J Clin Invest 100: 3111–3120.
33. Thiagarajah JR, Verkman AS, (2005) New drug targets for cholera therapy. Trends Pharmacol Sci 26: 172–175.
34. Ousingsawat J, Mirza M, Tian Y, Roussa E, Schreiber R, et al. (2011) Rotavirus toxin NSP4 induces diarrhea by activation of TMEM16A and inhibition of Na+ absorption. Pflugers Arch 461: 579–589.
35. Ko EA, Jin BJ, Namkung W, Ma T, Thiagarajah JR, et al. (2013) Chloride channel inhibition by a red wine extract and a synthetic small molecule prevents rotaviral secretory diarrhoea in neonatal mice. Gut 63 (7) 1120–9.
36. Jones RH, Tait CL, (1995) Gastrointestinal side-effects of NSAIDs in the community. Br J Clin Pract 49: 67–70.
37. Riff DS, Duckor S, Gottlieb I, Diamond E, Soulier S, et al. (2009) Diclofenac potassium liquid-filled soft gelatin capsules in the management of patients with postbunionectomy pain: a Phase III, multicenter, randomized, double-blind, placebo-controlled study conducted over 5 days. Clin Ther 31: 2072–2085.
38. Thiagarajah JR, Broadbent T, Hsieh E, Verkman AS, (2004) Prevention of toxin-induced intestinal ion and fluid secretion by a small-molecule CFTR inhibitor. Gastroenterology 126: 511–519.