Quercetin inhibits pacemaker potentials via nitric oxide/cGMP-dependent activation and TRPM7/ANO1 channels in cultured interstitial cells of cajal from mouse small intestine

Cellular Physiology and Biochemistry

Volumn 35, Issue 6, 2015, Pages 2422-2436

  Gim, Huijin ^a   Nam, Joo Hyun ^b   Lee, Soojin ^a   Shim, Ji Hwan ^a   Kim, Hyun Jung ^a   Ha, Ki Tae ^a   Kim, Byung Joo ^a  

^a Pusan National University   (South Korea)

^b Dongguk University College of Medicine   (South Korea)

Author keywords

ANO1; Gastrointestinal tract; Interstitial Cells of Cajal; Quercetin; TRPM7 channel

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; ANOCTAMIN1 PROTEIN; CYCLIC GMP; EVANS BLUE; GUANOSINE DIPHOSPHATE SUGAR; N(G) NITROARGININE METHYL ESTER; NALOXONE; NITRIC OXIDE; PROTEIN; QUERCETIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL M7; TRANSMEMBRANE PROTEIN 16A; UNCLASSIFIED DRUG; CHLORIDE CHANNEL; CYCLIC GMP DEPENDENT PROTEIN KINASE; TMEM16A PROTEIN, MOUSE; TRANSIENT RECEPTOR POTENTIAL CHANNEL M; TRPM7 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG INHIBITION; ELECTRIC POTENTIAL; EMBRYO; GASTROINTESTINAL MOTILITY; GASTROINTESTINAL TRANSIT; GENE OVEREXPRESSION; HEK293 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTERSTITIAL CELL OF CAJAL; MEMBRANE CURRENT; MOUSE; NONHUMAN; PACEMAKER POTENTIAL; PRIORITY JOURNAL; SMALL INTESTINE; WHOLE CELL PATCH CLAMP; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; DRUG EFFECTS; MEMBRANE POTENTIAL; METABOLISM; SIGNAL TRANSDUCTION;

MURINAE; MUS;

ANIMALS; CELL LINE; CHLORIDE CHANNELS; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; GASTROINTESTINAL MOTILITY; HEK293 CELLS; HUMANS; INTERSTITIAL CELLS OF CAJAL; INTESTINE, SMALL; MEMBRANE POTENTIALS; MICE; MICE, INBRED BALB C; NITRIC OXIDE; QUERCETIN; SIGNAL TRANSDUCTION; TRPM CATION CHANNELS;

EID: 84931480523     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000374043     Document Type: Article

References (64)

1. Hertog MG, Feskens EJ, Hollman PC, Katan MB, Kromhout D: Dietary antioxidant flavonoids and risk of coronary heart disease: the Zutphen Elderly Study. Lancet 1993;342:1007-1011.
2. Nijveldt RJ, van Nood E, van Hoorn DE, Boelens PG, van Norren K, van Leeuwen PA: Flavonoids: a review of probable mechanisms of action and potential applications. Am J Clin Nutr 2001;74:418-425.
3. Kahraman A, Erkasap N, Köken T, Serteser M, Aktepe F, Erkasap S: The antioxidative and antihistaminic properties of quercetin in ethanol-induced gastric lesions. Toxicology 2003;183:133-142.
4. Erlund I, Freese R, Marniemi J, Hakala P, Alfthan G: Bioavailability of quercetin from berries and the diet. Nutr Cancer 2006;54:13-17.
5. Mann GE, Rowlands DJ, Li FY, de Winter P, Siow RC: Activation of endothelial nitric oxide synthase by dietary isoflavones: role of NO in Nrf2-mediated antioxidant gene expression. Cardiovasc Res 2007;75:261-274.
6. Ertug PU, Aydinoglu F, Goruroglu Ozturk O, Singirik E, Ogulener N: Comparative study of the quercetin, ascorbic acid, glutathione and superoxide dismutase for nitric oxide protecting effects in mouse gastric fundus. Eur J Pharmacol 2013;698:379-387.
7. Lopez-Lopez G,Moreno L, Cogolludo A, Galisteo M, Ibarra M, Duarte J, Lodi F, Tamargo J, Perez-Vizcaino F: Nitric oxide (NO) scavenging and NO protecting effects of quercetin and their biological significance in vascular smooth muscle. Mol Pharmacol 2004;65:851-859.
8. Mahmoud MF, Hassan NA, El Bassossy HM, Fahmy A: Quercetin protects against diabetes-induced exaggerated vasoconstriction in rats: effect on low grade inflammation. PLoS One 2013;8:e63784.
9. Crowe FL, Crowe FL, Roddam AW, Key TJ, Appleby PN, Overvad K, Jakobsen MU, Tjønneland A, Hansen L, Boeing H, Weikert C, Linseisen J, Kaaks R, Trichopoulou A, Misirli G, Lagiou P, Sacerdote C, Pala V, Palli D, Tumino R, Panico S, Bueno-de-Mesquita HB, Boer J, Gils CH, Beulens JW, Barricarte A, Rodríguez L, Larrañaga N, Sánchez MJ, Tormo MJ, Buckland G, Lund E, Hedblad B, Melander O, Jansson JH, Wennberg P, Wareham NJ, Slimani N, Romieu I, Jenab M, Danesh J, Gallo V, Norat T, Riboli E: Fruit and vegetable intake and mortality from ischaemic heart disease: results from the European Prospective Investigation into Cancer and Nutrition (EPIC)-Heart study. Eur Heart J 2011;32:1235-1243.
10. Vasanthi HR, ShriShriMal N, Das DK: Phytochemicals from plants to combat cardiovascular disease. Curr Med Chem 2012;19:2242-2251.
11. Pignatelli P, Pulcinelli FM, Celestini A, Lenti L, Ghiselli A, Gazzaniga PP, Violi F: The flavonoids quercetin and catechin synergistically inhibit platelet function by antagonizing the intracellular production of hydrogen peroxide. Am J Clin Nutr 2000;72:1150-1155.
12. Das DK, Chakraborty A, Sinha M, Manna K, Mukherjee D, Chakraborty A, Bhattacharjee S, Dey S: Modulatory role of quercetin against gamma radiation-mediated biochemical and morphological alterations of red blood cells. Int J Radiat Biol 2013;89:471-481.
13. Liu CJ, Lin JY: Anti-inflammatory effects of phenolic extracts from strawberry and mulberry fruits on cytokine secretion profiles using mouse primary splenocytes and peritoneal macrophages. Int Immunopharmacol 2013;16:165-170.
14. Bardy G, Virsolvy A, Quignard JF, Ravier MA, Bertrand G, Dalle S, Cros G, Magous R, Richard S, Oiry C: Quercetin induces insulin secretion by direct activation of L-type calcium channels in pancreatic beta cells. Br J Pharmacol 2013;169:1102-1113.
15. Kim MC, Lee HJ, Lim B, Ha KT, Kim SY, So I, Kim BJ: Quercetin induces apoptosis by inhibiting MAPKs and TRPM7 channels in AGS cells. Int J Mol Med 2014;33:1657-1663.
16. Moon J, Lee SM, Do HJ, Cho Y, Chung JH, Shin MJ: Quercetin up-regulates LDL receptor expression in HepG2 cells. Phytother Res 2012;26:1688-1694.
17. Shen Y, Ward NC, Hodgson JM, Puddey IB, Wang Y, Zhang D, Maghzal GJ, Stocker R, Croft KD: Dietary quercetin attenuates oxidant-induced endothelial dysfunction and atherosclerosis in apolipoprotein E knockout mice fed a high-fat diet: a critical role for heme oxygenase-1. Free Radic Biol Med 2013;65:908-915.
18. Kressler J, Millard-Stafford M, Warren GL: Quercetin and endurance exercise capacity: a systematic review and meta-analysis. Med Sci Sports Exerc 2011;43:2396-2404.
19. Di Carlo G, Mascolo N, Izzo AA, Capasso F: Effects of quercetin on the gastrointestinal tract in rats and mice. Phytother Res 1994;8:42-45.
20. Hammad HM, Abdalla SS: Pharmacological effects of selected flavonoids on rat isolated ileum: Structureactivity relationship. Gen Pharmacol 1997;28:767-771.
21. Galvez J, Crespo ME, Jimenez J, Suarez A, Zarzuelo A: Antidiarrhoeic activity of quercitrin in mice and rats. J Pharm Pharmacol 1993;45:157-159.
22. Huizinga JD, Thuneberg L, Kluppel M, Malysz J, Mikkelsen HB, Bernstein A: W/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity. Nature 1995;373:347-349.
23. Sanders KM: A case for interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract. Gastroenterology 1996;111:492-515.
24. Kim BJ, Lim HH, Yang DK, Jun JY, Chang IY, Park CS, So I, Stanfield PR, Kim KW: Melastatin-Type Transient Receptor Potential Channel 7 Is Required for Intestinal Pacemaking Activity. Gastroenterology 2005;129:1504-1517.
25. Berezin I, Huizinga JD, Farraway L, Daniel EE: Innervation of interstitial cells of Cajal by vasoactive intestinal polypeptide containing nerves in canine colon. Can J Physiol Pharmacol 1990;68:922-932.
26. Nam JH, Kim WK, Kim BJ: Sphingosine and FTY720 modulate pacemaking activity in interstitial cells of Cajal from mouse small intestine. Mol Cells 2013;36:235-244.
27. Ward SM, Beckertt EA, Wang X, Baker F, Khoyi M, Sanders KM: Interstitial cells of Cajal mediate cholinergic neurotransmission from enteric motorneurons. J Neurosci 2000;20:1393-1403.
28. Lee JH, Kim SY, Kwon YK, Kim BJ, So I: Characteristics of the cholecystokinin-induced depolarization of pacemaking activity in cultured interstitial cells of Cajal from murine small intestine. Cell Physiol Biochem. 2013;31:542-554.
29. Kim BJ, Kim SY, Lee S, Jeon JH, Matsui H, Kwon YK, Kim SJ, So I: The role of transient receptor potential channel blockers in human gastric cancer cell viability. Can J Physiol Pharmacol 2012;90:175-186.
30. Hwang MW, Kim JN, Song HJ, Lim B, Kwon YK, Kim BJ: Effects of Lizhong Tang on cultured mouse small intestine interstitial cells of Cajal. World J Gastroenterol 2013;19:2249-2255.
31. Kim BJ, Kim HW, Lee GS, Choi S, Jun JY, So I, Kim SJ: Poncirus trifoliate fruit modulates pacemaker activity in interstitial cells of Cajal from the murine small intestine. J Ethnopharmacol 2013;149:668-675.
32. Koh SD, Jun JY, Kim TW, Sanders KM: A Ca2+-inhibited non-selective cation conductance contributes to pacemaker currents in mouse interstitial cell of Cajal. J Physiol 2002;540:803-814.
33. Kim BJ, So I, Kim KW: The relationship of TRP channels to the pacemaker activity of interstitial cells of Cajal in the gastrointestinal tract. J Smooth Muscle Res 2006;42:1-7.
34. Huizinga JD, Zhu Y, Ye J, Molleman A: High conductance chloride channels generate pacemaker currents in interstitial cells of Cajal. Gastroenterology 2002;123:1627-1636.
35. Zhu MH, Kim TW, Ro S, Yan W, Ward SM, Koh SD, Sanders KM: A Ca2+-activated Cl-conductance in interstitial cells of Cajal linked to slow wave currents and pacemaker activity. J Physiol 2009;587:4905-4918.
36. Zhu Y, Mucci A, Huizinga JD: Inwardly rectifying chloride channel activity in intestinal pacemaker cells. Am J Physiol Gastrointest Liver Physiol 2005;288:G809-821.
37. Huang F, Rock JR, Harfe BD, Cheng T, Huang X, Jan YN, Jan LY: Studies on expression and function of the TMEM16A calcium-activated chloride channel. Proc Natl Acad Sci U S A 2009;106:21413-21418.
38. Namkung W, Yao Z, Finkbeiner WE, Verkman AS: Small-molecule activators of TMEM16A, a calciumactivated chloride channel, stimulate epithelial chloride secretion and intestinal contraction. FASEB J 2011;25:4048-4062.
39. Sanders KM, Zhu MH, Britton F, Koh SD, Ward SM: Anoctamins and gastrointestinal smooth muscle excitability. Exp Physiol. 2012;97:200-206.
40. Kim BJ, Nam JH, Kim KH, Joo M, Ha TS, Weon KY, Choi S, Jun JY, Park EJ, Wie J, So I, Nah SY: Characteristics of gintonin-mediated membrane depolarization of pacemaker activity in cultured interstitial cells of Cajal. Cell Physiol Biochem. 2014;34:873-890.
41. Shahi PK, Choi S, Zuo DC, Kim MY, Park CG, Kim YD, Lee J, Park KJ, So I, Jun JY: The possible roles of hyperpolarization-activated cyclic nucleotide channels in regulating pacemaker activity in colonic interstitial cells of Cajal. J Gastroenterol 2014;49:1001-1010.
42. Scott RB, Tan DT: Mediation of altered motility in food protein induced intestinal anaphylaxis in Hooded-Lister rat. Can J Physiol Pharmacol. 1996;74:320-330.
43. Salah AM, Gathumbi J, Vierling W: Inhibition of intestinal motility by methanol extracts of Hibiscus sabdariffa L. (Malvaceae) in rats. Phytother Res 2002;16:283-285.
44. Gharzouli K, Holzer P: Inhibition of guinea pig intestinal peristalsis by the flavonoids quercetin, naringenin, apigenin and genistein. Pharmacology 2004;70:5-14.
45. Baggio CH, Freitas CS, Mayer B, Dos Santos AC, Twardowschy A, Potrich FB, Cipriani TR, de Souza LM, Sassaki GL, Iacomini M, Marques MC, Mesia-Vela S: Muscarinic-dependent inhibition of gastric emptying and intestinal motility by fractions of Maytenus ilicifolia Mart ex. Reissek. J Ethnopharmacol 2009;123:385-391.
46. Kahle K, Kempf M, Schreier P, Scheppach W, Schrenk D, Kautenburger T, Hecker D, Huemmer W, Ackermann M, Richling E: Intestinal transit and systemic metabolism of apple polyphenols. Eur J Nutr 2011;50:507-522.
47. Foss JF: A review of the potential role of methylnaltrexone in opioid bowel dysfunction. Am J Surg 2001;182:19S-26S.
48. Anselmi L, Huynh J, Vegezzi G, Sternini C: Effects of methylnaltrexone on guinea pig gastrointestinal motility. Naunyn Schmiedebergs Arch Pharmacol 2013;386:279-286.
49. Gharzouli K, Holzer P: Inhibition of guinea pig intestinal peristalsis by the flavonoids quercetin, naringenin, apigenin and genistein. Pharmacology 2004;70:5-14.
50. Bagnol D, Mansour A, Akil H, Watson SJ: Cellular localization and distribution of the cloned mu and kappa opioid receptors in rat gastrointestinal tract. Neuroscience 1997;81:579-591.
51. Culpepper-Morgan JA, Inturrisi CE, Portenoy RK, Foley K, Houde RW, Marsh F, Kreek MJ: Treatment of opioid-induced constipation with oral naloxone: a pilot study. Clin Pharmacol Ther 1992;52:90-95.
52. Yuan CS, Foss JF, Moss J: Effects of methylnaltrexone on morphine-induced inhibition of contraction in isolated guinea pig ileum and human intestine. Eur J Pharmacol 1995;276:107-111.
53. Komori S, Kawai M, Takewaki T, Ohashi H. GTP-binding protein involvement in membrane currents evoked by carbachol and histamine in guinea-pig ileal muscle. J Physiol 1992;450:105-126.
54. Ogata R, Inoue Y, Nakano H, Ito Y, Kitamura K. Oestradiol-induced relaxation of rabbit basilar artery by inhibition of voltage-dependent Ca channels through GTP-binding protein. Br J Pharmacol 1996;117:351-359.
55. Moncada S, Palmer RMJ, Higgs EA: Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 1991;43:109-142.
56. Nadler MJS, Hermosura MC, Inabe K, Perraud AL, Zhu Q, Stokes AJ, Kurosaki T, Kinet JP, Penner R, Scharenberg AM, Fleig A: LTRPC7 is a MgNATP-regulated divalent cation channel required for cell viability. Nature 2001;411:590-595.
57. Runnels LW, Yue L, Clapham DE: The TRPM7 channel is inactivated by PIP(2) hydrolysis. Nat Cell Biol 2002;4:329-336.
58. Kim BJ, Kim HW, Lee GS, Choi S, Jun JY, So I, Kim SJ: Poncirus trifoliate fruit modulates pacemaker activity in interstitial cells of Cajal from the murine small intestine. J Ethnopharmacol 2013;149:668-675.
59. Lyu JH, Lee HT: Effects of dried Citrus unshiu peels on gastrointestinal motility in rodents. Arch Pharm Res 2013;36:641-648.
60. Lee HT, Seo EK, Chung SJ, Shim CK: Prokinetic activity of an aqueous extract from dried immature fruit of Poncirus trifoliata (L.) Raf. J Ethnopharmacol 2005;102:131-136.
61. Lee HT, Seo EK, Chung SJ, Shim CK: Effect of an aqueous extract of dried immature fruit of Poncirus trifoliata (L.) Raf. J Ethnopharmacol 2005;102:302-306.
62. Lozoya X, Meckes M, Abou-Zaid M, Tortoriello J, Nozzolillo C, Arnason JT: Quercetin glycosides in Psidium guajava L. leaves and determination of a spasmolytic principle. Arch Med Res 1994;25:11-5.
63. Gharzouli K, Holzer P: Inhibition of guinea pig intestinal peristalsis by the flavonoids quercetin, naringenin, apigenin and genistein. Pharmacology. 2004;70:5-14.
64. Espley RV, Butts CA, Laing WA, Martell S, Smith H, McGhie TK, Zhang J, Paturi G, Hedderley D, Bovy A, Schouten HJ, Putterill J, Allan AC, Hellens RP: Dietary flavonoids from modified apple reduce inflammation markers and modulate gut microbiota in mice. J Nutr 2014;144:146-154.