Quercetin enhances intestinal barrier function through the assembly of zonnula occludens-2, occludin, and claudin-1 and the expression of claudin-4 in caco-2 cells

Journal of Nutrition

Volumn 139, Issue 5, 2009, Pages 965-974

  Suzuki, Takuya ^a   Hara, Hiroshi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CLAUDIN 1; CLAUDIN 4; MYRICETIN; OCCLUDIN; PROTEIN KINASE C DELTA; QUERCETIN; ROTTLERIN; UNCLASSIFIED DRUG; ZONNULA OCCLUDEN 2; ACETOPHENONE DERIVATIVE; BENZOPYRAN DERIVATIVE; ENZYME INHIBITOR; FLAVONOID; MEMBRANE PROTEIN; RECOMBINANT PROTEIN; ZONULA OCCLUDENS 2 PROTEIN; ZONULA OCCLUDENS-2 PROTEIN;

ARTICLE; CELL ACTIVITY; CELL LEVEL; CELL STRAIN CACO 2; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; DOSE RESPONSE; DRUG INHIBITION; DRUG MECHANISM; ELECTRIC RESISTANCE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; INCUBATION TIME; INTESTINE MUCOSA PERMEABILITY; MONOLAYER CULTURE; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TIGHT JUNCTION; CELL MEMBRANE PERMEABILITY; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; IMPEDANCE; INTESTINE; KINETICS; METABOLISM; PHYSIOLOGY;

ACETOPHENONES; BENZOPYRANS; CACO-2 CELLS; CELL MEMBRANE PERMEABILITY; ELECTRIC IMPEDANCE; ENZYME INHIBITORS; FLAVONOIDS; HUMANS; IMMUNOBLOTTING; INTESTINES; KINETICS; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; PROTEIN KINASE C-DELTA; QUERCETIN; RECOMBINANT PROTEINS;

EID: 65349095529     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.108.100867     Document Type: Article

References (37)

1. Kandaswami C, Middleton E Jr. Free radical scavenging and antioxidant activity of plant flavonoids. Adv Exp Med Biol. 1994;366:351-76.
2. Sim GS, Lee BC, Cho HS, Lee JW, Kim JH, Lee DH, Pyo HB, Moon DC, Oh KW, et al. Structure activity relationship of antioxidative property of flavonoids and inhibitory effect on matrix metalloproteinase activity in UVA-irradiated human dermal fibroblast. Arch Pharm Res. 2007;30:290-8.
3. Hamalainen M, Nieminen R, Vuorela P, Heinonen M, Moilanen E. Anti-inflammatory effects of flavonoids: genistein, kaempferol, querce-tin, and daidzein inhibit STAT-1 and NF-kappaB activations, whereas flavone, isorhamnetin, naringenin, and pelargonidin inhibit only NF-kappaB activation along with their inhibitory effect on iNOS expression and NO production in activated macrophages. Mediators Inflamm. 2007;2007:45673.
4. Huang YT, Hwang JJ, Lee PP, Ke FC, Huang JH, Huang CJ, Kandaswami C, Middleton E Jr, Lee MT. Effects of luteolin and quercetin, inhibitors of tyrosine kinase, on cell growth and metastasis-associated properties in A431 cells overexpressing epidermal growth factor receptor. Br J Pharmacol. 1999;128:999-1010.
5. Agullo G, Gamet-Payrastre L, Manenti S, Viala C, Remesy C, Chap H, Payrastre B. Relationship between flavonoid structure and inhibition of phosphatidylinositol 3-kinase: a comparison with tyrosine kinase and protein kinase C inhibition. Biochem Pharmacol. 1997;53:1649-57.
6. Hiermann A, Schramm HW, Laufer S. Anti-inflammatory activity of myricetin-3-O-beta-D-glucuronide and related compounds. Inflamm Res. 1998;47:421-7.
7. Rodgers EH, Grant MH. The effect of the flavonoids, quercetin, myricetin and epicatechin on the growth and enzyme activities of MCF7 human breast cancer cells. Chem Biol Interact. 1998;116:213-28.
8. Jenkins RT, Jones DB, Goodacre RL, Collins SM, Coates G, Hunt RH, Bienenstock J. Reversibility of increased intestinal permeability to 51Cr-EDTA in patients with gastrointestinal inflammatory diseases. Am J Gastroenterol. 1987;82:1159-64.
9. Parlesak A, Schafer C, Schutz T, Bode JC, Bode C. Increased intestinal permeability to macromolecules and endotoxemia in patients with chronic alcohol abuse in different stages of alcohol-induced liver disease. J Hepatol. 2000;32:742-7.
10. Gonzalez-Mariscal L, Betanzos A, Nava P, Jaramillo BE. Tight junction proteins. Prog Biophys Mol Biol. 2003;81:1-44.
11. Furuse M, Hirase T, Itoh M, Nagafuchi A, Yonemura S, Tsukita S. Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol. 1993;123:1777-88.
12. Furuse M, Fujita K, Hiiragi T, Fujimoto K, Tsukita S. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol. 1998;141:1539-50.
13. Martin-Padura I, Lostaglio S, Schneemann M, Williams L, Romano M, Fruscella P, Panzeri C, Stoppacciaro A, Ruco L, et al. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol. 1998;142:117-27.
14. Gonzalez-Mariscal L, Tapia R, Chamorro D. Crosstalk of tight junction components with signaling pathways. Biochim Biophys Acta. 1778;2008:729-56.
15. Suzuki A, Yamanaka T, Hirose T, Manabe N, Mizuno K, Shimizu M, Akimoto K, Izumi Y, Ohnishi T, et al. Atypical protein kinase C is involved in the evolutionarily conserved par protein complex and plays a critical role in establishing epithelia-specific junctional structures. J Cell Biol. 2001;152:1183-96.
16. Banan A, Farhadi A, Fields JZ, Zhang LJ, Shaikh M, Keshavarzian A. The delta-isoform of protein kinase C causes inducible nitric-oxide synthase and nitric oxide up-regulation: key mechanism for oxidant-induced carbonylation, nitration, and disassembly of the microtubule cytoskeleton and hyperpermeability of barrier of intestinal epithelia. J Pharmacol Exp Ther. 2003;305:482-94.
17. Sheth P, Basuroy S, Li C, Naren AP, Rao RK. Role of phosphatidyl-inositol 3-kinase in oxidative stress-induced disruption of tight junctions. J Biol Chem. 2003;278:49239-45.
18. Amasheh M, Schlichter S, Amasheh S, Mankertz J, Zeitz M, Fromm M, Schulzke JD. Quercetin enhances epithelial barrier function and increases claudin-4 expression in Caco-2 cells. J Nutr. 2008;138:1067-73.
19. Li N, Lewis P, Samuelson D, Liboni K, Neu J. Glutamine regulates Caco-2 cell tight junction proteins. Am J Physiol Gastrointest Liver Physiol. 2004;287:G726-33.
20. Bruewer M, Luegering A, Kucharzik T, Parkos CA, Madara JL, Hopkins AM, Nusrat A. Proinflammatory cytokines disrupt epithelial barrier function by apoptosis-independent mechanisms. J Immunol. 2003;171:6164-72.
21. Suzuki T, Yoshida S, Hara H. Physiological concentrations of short-chain fatty acids immediately suppress colonic epithelial permeability. Br J Nutr. 2008;100:297-305.
22. Suzuki T, Seth A, Rao R. Role of phospholipase Cgamma-induced activation of protein kinase Cepsilon (PKCepsilon) and PKCbetal in epidermal growth factor-mediated protection of tight junctions from acetaldehyde in Caco-2 cell monolayers. J Biol Chem. 2008;283: 3574-83.
23. Powell DW. Barrier function of epithelia. Am J Physiol. 1981;241:G275-88.
24. Basuroy S, Seth A, Elias B, Naren AP, Rao R. MAPK interacts with occludin and mediates EGF-induced prevention of tight junction disruption by hydrogen peroxide. Biochem J. 2006;393:69-77.
25. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680-5.
26. Li W, Zhang J, Bottaro DP, Pierce JH. Identification of serine 643 of protein kinase C-delta as an important autophosphorylation site for its enzymatic activity. J Biol Chem. 1997;272:24550-5.
27. Sakakibara A, Furuse M, Saitou M, Ando-Akatsuka Y, Tsukita S. Possible involvement of phosphorylation of occludin in tight junction formation. J Cell Biol. 1997;137:1393-401.
28. Rao RK, Basuroy S, Rao VU, Karnaky KJ Jr, Gupta A. Tyrosine phosphorylation and dissociation of occludin-ZO-1 and E-cadherin-beta-catenin complexes from the cytoskeleton by oxidative stress. Biochem J. 2002;368:471-81.
29. Fujibe M, Chiba H, Kojima T, Soma T, Wada T, Yamashita T, Sawada N. Thr203 of claudin-1, a putative phosphorylation site for MAP kinase, is required to promote the barrier function of tight junctions. Exp Cell Res. 2004;295:36-47.
30. Avila-Flores A, Rendon-Huerta E, Moreno J, Islas S, Betanzos A, Robles-Flores M, Gonzalez-Mariscal L. Tight-junction protein zonula occludens 2 is a target of phosphorylation by protein kinase C. Biochem J. 2001;360:295-304.
31. Suzuki T, Elias BC, Seth A, Shen L, Turner JR, Giorgianni F, Desiderio D, Guntaka R, Rao R. PKC eta regulates occludin phosphorylation and epithelial tight junction integrity. Proc Natl Acad Sci USA. 2009;106:61-6.
32. Honda H, Pazin MJ, Ji H, Wernyj RP, Morin PJ. Crucial roles of Sp1 and epigenetic modifications in the regulation of the CLDN4 promoter in ovarian cancer cells. J Biol Chem. 2006;281:21433-44.
33. Pan W, Chang MJ, Booyse FM, Grenett HE, Bradley KM, Wolkowicz PE, Shang Q, Tabengwa EM. Quercetin induced tissue-type plasminogen activator expression is mediated through Sp1 and p38 mitogen-activated protein kinase in human endothelial cells. J Thromb Haemost. 2008;6:976-85.
34. Boyer J, Brown D, Liu RH. Uptake of quercetin and quercetin 3-glucoside from whole onion and apple peel extracts by Caco-2 cell monolayers. J Agric Food Chem. 2004;52:7172-9.
35. Graf BA, Ameho C, Dolnikowski GG, Milbury PE, Chen CY, Blumberg JB. Rat gastrointestinal tissues metabolize quercetin. J Nutr. 2006;136:39-44.
36. Manach C, Williamson G, Morand C, Scalbert A, Remesy C. Bioavail-ability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am J Clin Nutr. 2005;81:S230-42.
37. van der Woude H, Gliszczynska-Swiglo A, Struijs K, Smeets A, Alink GM, Rietjens IM. Biphasic modulation of cell proliferation by quercetin at concentrations physiologically relevant in humans. Cancer Lett. 2003;200:41-7.