Anti-inflammatory effects of resveratrol occur via inhibition of lipopolysaccharide-induced NF-κB activation in Caco-2 and SW480 human colon cancer cells

British Journal of Nutrition

Volumn 108, Issue 9, 2012, Pages 1623-1632

  Panaro, Maria Antonietta ^a   Carofiglio, Vito ^a   Acquafredda, Angela ^a   Cavallo, Pasqua ^a   Cianciulli, Antonia ^a  

^a UNIVERSITY OF BARI   (Italy)

Author keywords

Intestinal cells; Lipopolysaccharide; NF B; Nitric oxide; Resveratrol

Indexed keywords

I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPOLYSACCHARIDE; NITRIC OXIDE; RESVERATROL; TOLL LIKE RECEPTOR 4;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CANCER CELL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG STRUCTURE; GENE EXPRESSION; HUMAN; HUMAN CELL; INTESTINE CELL; NUCLEOTIDE SEQUENCE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTINEOPLASTIC AGENTS, PHYTOGENIC; CACO-2 CELLS; CELL LINE, TUMOR; CELL SURVIVAL; COLONIC NEOPLASMS; DIETARY SUPPLEMENTS; DOWN-REGULATION; ENTEROCYTES; HUMANS; I-KAPPA B PROTEINS; INFLAMMATORY BOWEL DISEASES; LIPOPOLYSACCHARIDES; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; RNA, MESSENGER; STILBENES; TOLL-LIKE RECEPTOR 4;

VITACEAE;

EID: 84869995154     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114511007227     Document Type: Article

References (55)

1. Soleas GJ, Diamandis EP & Goldberg DM (1997) Resveratrol: a molecule whose time has come? And gone? Clin Biochem 30, 91-113.
2. Renaud S & De Lorgeril M (1993) Wine, alcohol, platelets, and the French paradox for coronary heart disease. Lancet 339, 1523-1526.
3. Araújo JR, Gonçalves P & Martel F (2011) Chemopreventive effect of dietary polyphenols in colorectal cancer cell lines. Nutr Res 31, 77-87.
4. Martin AR, Villegas I, Casa CL, et al. (2004) Resveratrol, a polyphenol found in grapes, suppresses oxidative damage and stimulates apoptosis during early colonic inflammation in rats. Biochem Pharmacol 67, 1399-1410.
5. Feng YH, Zhou WL, Wu QL, et al. (2002) Low dose resvera-trol enhanced immune response of mice. Acta Pharmacol Sin 23, 893-897.
6. Belguendouz L, Fremont L & Gozzelino MT (1998) Interaction of transresveratrol with plasma proteins. Biochem Pharmacol 55, 811-816.
7. Tsai SH, Lin-Shiau SY & Lin JK (1999) Suppression of nitric oxide synthase and the down-regulation of the activation of NF-kB in macrophages by resveratrol. Br J Pharmacol 126, 673-680.
8. Romier B, Schneider YJ, Larondelle Y, et al. (2009) Dietary polyphenols can modulate the intestinal inflammatory response. Nutr Rev 67, 363-378.
9. Pohl C, Hombach A & Kruis W (2000) Chronic inflammatory bowel disease and cancer. Hepatogastroenterology 47, 57-70.
10. Lakatos PL, Fischer S, Lakatos L, et al. (2006) Current concept on the pathogenesis of inflammatory bowel disease-crosstalk between genetic and microbial factors: pathogenic bacteria and altered bacterial sensing or changes in mucosal integrity take "toll"? World J Gastroenterol 12, 1829-1841.
11. Ianaro A, Tersigni M & D'Acquisto F (2009) New insight in LPS antagonist. Mini Rev Med Chem 9, 306-317.
12. Triantafilou M & Triantafilou K (2005) The dynamics of LPS recognition: complex orchestration of multiple receptors. J Endotoxin Res 11, 5-11.
13. Won JH, Im HT, Kim YH, et al. (2006) Antiinflammatory effect of buddlejasaponin IV through the inhibition of iNOS and COX-2 expression in RAW 264·7 macrophages via the NF-kB inactivation. Br J Pharmacol 148, 216-225.
14. Mayer B & Hemmens B (1997) Biosynthesis and action of nitric oxide in mammalian cells. Trends Biochem Sci 22, 477-481.
15. Baeuerle PA & Baltimore D (1996) NF-kappa B: ten years after. Cell 87, 13-20.
16. Viatour P, Merville MP, Bours V, et al. (2005) Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation. Trends Biochem Sci 30, 43-52.
17. Campbell KJ & Perkins ND (2006) Regulation of NF-kappaB function. Biochem Soc Symp 73, 165-180.
18. Xie QW, Whisnant R & Nathan C (1993) Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J Exp Med 177, 1779-1784.
19. Ding AH, Nathan CF & Stuehr DJ (1988) Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J Immunol 141, 2407-2412.
20. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
21. Li C & Wang MH (2011) Anti-inflammatory effect of the water fraction from hawthorn fruit on LPS-stimulated RAW 264·7 cells. Nutr Res Pract 5, 101-106.
22. Almeida WS, Maciel TT, Di Marco GS, et al. (2006) Escheri-chia coli lipopolysaccharide inhibits renin activity in human mesangial cells. Kidney Int 69, 974-980.
23. Maier-Salamon A, Hagenauer B, Wirth M, et al. (2006) Increased transport of resveratrol across monolayers of the human intestinal Caco-2 cells is mediated by inhibition and saturation of metabolites. Pharm Res 23, 2107-2115.
24. Aumont V, Krisa S, Battaglia E, et al. (2001) Regioselective and stereospecific glucuronidation of trans-and cis-resvera-trol in human. Arch Biochem Biophys 393, 281-289.
25. Kaldas M, Walle UK & Walle T (2003) Resveratrol transport and metabolism by human intestinal Caco-2 cells. J Pharm Pharmacol 55, 307-312.
26. Goldberg DM, Yan J & Soleas GJ (2003) Absorption of three wine-related polyphenols in three different matrices by healthy subjects. Clin Biochem 36, 79-87.
27. Rahman I, Biswas SK & Kirkham PA (2006) Regulation of inflammation and redox signaling by dietary polyphenols. Biochem Pharmacol 72, 1439-1452.
28. Nathan C & Xie Q (1994) Nitric oxide synthases: roles, tolls and controls. Cell 78, 915-918.
29. Potoka DA, Nadler EP, Upperman JS, et al. (2002) Role of nitric oxide and peroxinitrite in gut barrier failure. World J Surg 26, 806-811.
30. Zamora R, Vodovotz Y & Biliar TR (2003) Inducible nitric oxide synthase and inflammatory diseases. Mol Med 6, 347-373.
31. Salerno L, Sorrenti V, Di Giacomo C, et al. (2002) Progress in the development of selective nitric oxide synthase (NOS) inhibitors. Curr Pharm Des 8, 177-200.
32. Nadler E & Ford HR (2000) Regulation of bacterial translocation by nitric oxide. Pediatr Surg Int 16, 165-168.
33. Nadler EP, Dickinson EC, Beer-Stolz D, et al. (2001) Scavenging nitric oxide reduces hepatocellular injury after endo-toxin challenge. Am J Physiol Gastrointest Liver Physiol 281, G173-G181.
34. Nadler E, Upperman J & Ford HR (2001) Controversies in the management of necrotizing enterocolitis. Surg Infect (Larchmt) 2, 113-120.
35. Zuckerbraun BS, Otterbein LE, Boyle P, et al. (2005) Carbon monoxide protects against the development of experimental necrotizing enterocolitis. Am J Physiol Gastrointest Liver Phy-siol 289, G607-G613.
36. Martínez J & Moreno JJ (2000) Effect of resveratrol, a natural polyphenolic compound, on reactive oxygen species and prostaglandin production. Biochem Pharmacol 59, 865-870.
37. Moreno JJ (2000) Resveratrol modulates arachidonic acid release, prostaglandin synthesis, and 3T6 fibroblast growth. J Pharmacol Exp Ther 294, 333-338.
38. Sebai H, Sani M, Yacoubi MT, et al. (2010) Resveratrol, a red wine polyphenol, attenuates lipopolysaccharide-induced oxidative stress in rat liver. Ecotoxicol Environ Saf 73, 1078-1083.
39. Sánchez-Fidalgo S, Cárdeno A, Villegas I, et al. (2010) Dietary supplementation of resveratrol attenuates chronic colonic inflammation in mice. Eur J Pharmacol 633, 78-84.
40. Akira S, Uematsu S & Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124, 783-801.
41. Magalhaes JG, Tattoli I & Girardin SE (2009) The intestinal epithelial barrier: how to distinguish between the microbial flora and pathogens. Semin Immunol 19, 106-115.
42. Takeda K & Akira S (2004) Microbial recognition by Toll-like receptors. J Dermatol Sci 34, 73-82.
43. Simiantonaki N, Kurzik-Dumke U, Karyofylli G, et al. (2007) Reduced expression of TLR4 is associated with the metastatic status of human colorectal cancer. Int J Mol Med 20, 21-29.
44. Ibeagha-Awemu EM, Lee JW, Ibeagha AE, et al. (2008) Bacterial lipopolysaccharide induces increased expression of toll-like receptor (TLR) 4 and downstream TLR signaling molecules in bovine mammary epithelial cells. Vet Res 39, 11.
45. Gatti G, Quintar AA, Andreani V, et al. (2009) Expression of Toll-like receptor 4 in the prostate gland and its association with the severity of prostate cancer. Prostate 69, 1387-1397.
46. Cook DN, Pisetsky DS & Schwartz DA (2004) Toll-like receptors in the pathogenesis of human disease. Nat Immunol 5975-5979.
47. Michelsen KS, Wong MH, Shah PK, et al. (2004) Lack of Toll-like receptor 4 or myeloid differentiation factor 88 reduces atherosclerosis and alters plaque phenotype in mice deficient in apolipoprotein E. Proc Natl Acad Sci USA 101, 10679-10684.
48. Björkbacka H, Kunjathoor VV, Moore KJ, et al. (2004) Reduced atherosclerosis in MyD88-null mice links elevated serum cholesterol levels to activation of innate immunity signaling pathways. Nat Med 10, 416-421.
49. Youn HS, Lee JY, Fitzgerald KA, et al. (2005) Specific inhibition of MyD88-independent signaling pathways of TLR3 and TLR4 by resveratrol: molecular targets are TBK1 and RIP1 in TRIF complex. J Immunol 175, 3339-3346.
50. Martín AR, Villegas I, Sánchez-Hidalgo M, et al. (2006) The effects of resveratrol, a phytoalexin derived from red wines, on chronic inflammation induced in an experimentally induced colitis model. Br J Pharmacol 147, 873-885.
51. Liang YC, Huang YT, Tsai SH, et al. (1999) Suppression of inducible cyclooxygenase and inducible nitric oxide synthase by apigenin and related flavonoids in mouse macrophages. Carcinogenesis 20, 1945-1952.
52. Bhat KP & Pezzuto JM (2002) Cancer chemopreventive activity of resveratrol. Ann N Y Acad Sci 957, 210-229.
53. Wadsworth TL & Koop DR (1999) Effects of the wine poly-phenolics quercetin and resveratrol on pro-inflammatory cytokine expression in RAW 264·7 macrophages. Biochem Pharmacol 57, 941-949.
54. Murakami A, Matsumoto K, Koshimizu K, et al. (2003) Effects of selected food factors with chemopreventive properties on combined lipopolysaccharide-and interferon-induced kB degradation in RAW264·7 macrophages. Cancer Lett 195, 17-25.
55. Adhami VM, Afaq F & Ahmad N (2003) Suppression of ultraviolet B exposure-mediated activation of NF-kB in normal human keratinocytes by resveratrol. Neoplasia 5, 74-82.