Oxidative stress enhances IL-8 and inhibits CCL20 production from intestinal epithelial cells in response to bacterial flagellin

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 299, Issue 3, 2010, Pages

  Ivison, Sabine M ^a   Wang, Ce ^a   Himmel, Megan E ^a   Sheridan, Jared ^a   Delano, Jonathan ^a   Mayer, Matt L ^a   Yao, Yu ^a   Kifayet, Arnawaz ^a   Steiner, Theodore S ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Innate immunity; MAP kinases; NF B; Toll like receptor 5

Indexed keywords

BACTERIAL PROTEIN; FLAGELLIN; HYDROGEN PEROXIDE; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHOLIPASE C GAMMA; PROTEIN TYROSINE KINASE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 5; 1,2 BIS(2 AMINOPHENOXY)ETHANE N,N,N',N' TETRAACETIC ACID ACETOXYMETHYL ESTER; 1,2-BIS(2-AMINOPHENOXY)ETHANE N,N,N',N'-TETRAACETIC ACID ACETOXYMETHYL ESTER; 3 (4 METHYLPHENYLSULFONYL) 2 PROPENENITRILE; 3-(4-METHYLPHENYLSULFONYL)-2-PROPENENITRILE; CALCIUM; CCL20 PROTEIN, HUMAN; CHELATING AGENT; DRUG DERIVATIVE; EGTAZIC ACID; NITRILE; OXIDIZING AGENT; SULFONE;

ARTICLE; CALCIUM CELL LEVEL; CELL STRAIN CACO 2; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TISSUE INJURY; UPREGULATION; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; INTESTINE MUCOSA; METABOLISM; PHYSIOLOGY;

CACO-2 CELLS; CALCIUM; CHELATING AGENTS; CHEMOKINE CCL20; EGTAZIC ACID; EPITHELIAL CELLS; FLAGELLIN; GENE EXPRESSION REGULATION; HUMANS; HYDROGEN PEROXIDE; INTERLEUKIN-8; INTESTINAL MUCOSA; NF-KAPPA B; NITRILES; OXIDANTS; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; SULFONES;

EID: 77957002175     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00089.2010     Document Type: Article

References (53)

1. Buffinton GD, Doe WF. Depleted mucosal antioxidant defences in inflammatory bowel disease. Free Radic Biol Med 19: 911-918, 1995.
2. Chan HL, Chou HC, Duran M, Gruenewald J, Waterfield MD, Ridley A, Timms JF. Major role of EGFR and SRC kinases in promoting oxidative stress-dependent loss of adhesion and apoptosis in epithelial cells. J Biol Chem 285: 4307-4318, 2009.
3. Chen W, Syldath U, Bellmann K, Burkart V, Kolb H. Human 60-kDa heat-shock protein: a danger signal to the innate immune system. J Immunol 162: 3212-3219, 1999.
4. Di Virgilio F. Purinergic mechanism in the immune system: a signal of danger for dendritic cells. Purinergic Signal 1: 205-209, 2005.
5. Enesa K, Ito K, Luong le A, Thorbjornsen I, Phua C, To Y, Dean J, Haskard DO, Boyle J, Adcock I, Evans PC. Hydrogen peroxide prolongs nuclear localization of NF-kappaB in activated cells by suppressing negative regulatory mechanisms. J Biol Chem 283: 18582-18590, 2008.
6. Gilmour PS, Rahman I, Donaldson K, MacNee W. Histone acetylation regulates epithelial IL-8 release mediated by oxidative stress from environmental particles. Am J Physiol Lung Cell Mol Physiol 284: L533-L540, 2003.
7. Hawlisch H, Kohl J. Complement and Toll-like receptors: key regulators of adaptive immune responses. Mol Immunol 43: 13-21, 2006.
8. Ivison SM, Graham NR, Bernales CQ, Kifayet A, Ng N, Shobab LA, Steiner TS. Protein kinase D interaction with TLR5 is required for inflammatory signaling in response to bacterial flagellin. J Immunol 178: 5735-5743, 2007.
9. Ivison SM, Graham NR, Bernales CQ, Kifayet A, Ng N, Shobab LA, Steiner TS. Protein kinase D interaction with TLR5 is required for inflammatory signaling in response to bacterial flagellin. J Immunol 178: 5735-5743, 2007.
10. Ivison SM, Himmel ME, Mayer ML, Yao Y, Kifayet A, Levings MK, Steiner TS. The stress signal extracellular ATP modulates antiflagellin immune responses in intestinal epithelial cells. Inflamml Bowel Dis. In press.
11. Janeway CA, Jr Goodnow CC, Medzhitov R. Danger - pathogen on the premises! Immunological tolerance. Curr Biol 6: 519-522, 1996.
12. 2: distinct responses of Caco-2 and Madin-Darby canine kidney (MDCK) strains. Cell Mol Biol (Noisy-le-grand) 49: 101-112, 2003.
13. Joshi R, Kumar S, Unnikrishnan M, Mukherjee T. Free radical scavenging reactions of sulfasalazine, 5-aminosalicylic acid and sulfapyridine: mechanistic aspects and antioxidant activity. Free Radic Res 39: 1163-1172, 2005.
14. Kamata H, Manabe T, Oka S, Kamata K, Hirata H. Hydrogen peroxide activates IkappaB kinases through phosphorylation of serine residues in the activation loops. FEBS Lett 519: 231-237, 2002.
15. Klune JR, Dhupar R, Cardinal J, Billiar TR, Tsung A. HMGB1: endogenous danger signaling. Mol Med 14: 476-484, 2008.
16. Kruidenier L, Kuiper I, Lamers CB, Verspaget HW. Intestinal oxidative damage in inflammatory bowel disease: semi-quantification, localization, and association with mucosal antioxidants. J Pathol 201: 28-36, 2003.
17. Kruidenier L, Kuiper I, Van Duijn W, Mieremet-Ooms MA, van Hogezand RA, Lamers CB, Verspaget HW. Imbalanced secondary mucosal antioxidant response in inflammatory bowel disease. J Pathol 201: 17-27, 2003. (Pubitemid 37121199)
18. Kumar A, Wu H, Collier-Hyams LS, Hansen JM, Li T, Yamoah K, Pan ZQ, Jones DP, Neish AS. Commensal bacteria modulate cullin-dependent signaling via generation of reactive oxygen species. EMBO J 26: 4457-4466, 2007.
19. Kumar A, Wu H, Collier-Hyams LS, Kwon YM, Hanson JM, Neish AS. The bacterial fermentation product butyrate influences epithelial signaling via reactive oxygen species-mediated changes in cullin-1 neddylation. J Immunol 182: 538-546, 2009.
20. Kwon JH, Keates S, Simeonidis S, Grall F, Libermann TA, Keates AC. ESE-1, an enterocyte-specific Ets transcription factor, regulates MIP-3alpha gene expression in Caco-2 human colonic epithelial cells. J Biol Chem 278: 875-884, 2003.
21. 2 and tumor necrosis factor-alpha in endothelial and epithelial cells. J Biol Chem 272: 32910-32918, 1997.
22. Matzinger P. The danger model: a renewed sense of self. Science 296: 301-305, 2002.
23. Matzinger P. Tolerance, danger, and the extended family. Annu Rev Immunol 12: 991-1045, 1994.
24. Min K, Ebeler SE. Quercetin inhibits hydrogen peroxide-induced DNA damage and enhances DNA repair in Caco-2 cells. Food Chem Toxicol 47: 2716-2722, 2009.
25. Moodie FM, Marwick JA, Anderson CS, Szulakowski P, Biswas SK, Bauter MR, Kilty I, Rahman I. Oxidative stress and cigarette smoke alter chromatin remodeling but differentially regulate NF-kappaB activation and proinflammatory cytokine release in alveolar epithelial cells. FASEB J 18: 1897-1899, 2004.
26. Moussion C, Ortega N, Girard JP. The IL-1-like cytokine IL-33 is constitutively expressed in the nucleus of endothelial cells and epithelial cells in vivo: a novel 'alarmin'? PLoS One 10: e3331, 2008.
27. Nemeth E, Halasz A, Barath A, Domokos M, Galfi P. Effect of hydrogen peroxide on interleukin-8 synthesis and death of Caco-2 cells. Immunopharmacol Immunotoxicol 29: 297-310, 2007.
28. Ogushi K, Wada A, Niidome T, Okuda T, Llanes R, Nakayama M, Nishi Y, Kurazono H, Smith KD, Aderem A, Moss J, Hirayama T. Gangliosides act as co-receptors for Salmonella enteritidis FliC and promote FliC induction of human beta-defensin-2 expression in Caco-2 cells. J Biol Chem 279: 12213-12219, 2004.
29. Okusawa S, Dinarello CA, Yancey KB, Endres S, Lawley TJ, Frank MM, Burke JF, Gelfand JA. C5a induction of human interleukin 1. Synergistic effect with endotoxin or interferon-gamma. J Immunol 139: 2635-2640, 1987.
30. Oshima N, Ishihara S, Rumi MA, Aziz MM, Mishima Y, Kadota C, Moriyama I, Ishimura N, Amano Y, Kinoshita Y. A20 is an early responding negative regulator of Toll-like receptor 5 signalling in intestinal epithelial cells during inflammation. Clin Exp Immunol 159: 185-198, 2010.
31. Park JE, Kim YI, Yi AK. Protein kinase D1 is essential for MyD88- dependent TLR signaling pathway. J Immunol 182: 6316-6327, 2009.
32. Rahman I, Gilmour PS, Jimenez LA, MacNee W. Oxidative stress and TNF-alpha induce histone acetylation and NF-kappaB/AP-1 activation in alveolar epithelial cells: potential mechanism in gene transcription in lung inflammation. Mol Cell Biochem 234-235: 239-248, 2002.
33. Rao RK, Baker RD, Baker SS, Gupta A, Holycross M. Oxidant-induced disruption of intestinal epithelial barrier function: role of protein tyrosine phosphorylation. Am J Physiol Gastrointest Liver Physiol 273: G812-G823, 1997.
34. Rugtveit J, Haraldsen G, Hogasen AK, Bakka A, Brandtzaeg P, Scott H. Respiratory burst of intestinal macrophages in inflammatory bowel disease is mainly caused by CD14+L1+ monocyte derived cells. Gut 37: 367-373, 1995.
35. - exchange activity in human intestinal epithelial cells. Biochem J 416: 99-108, 2008.
36. 2+ through two distinct mechanisms in rat hepatocytes. Acta Pharmacol Sin 30: 78-89, 2009.
37. Schutyser E, Struyf S, Van Damme J. The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev 14: 409-426, 2003.
38. 2-induced apoptosis via NF-kappaB and p38 MAPK in RIE-1 cells. Biochem Biophys Res Commun 378: 610-614, 2009.
39. Storz P, Doppler H, Johannes FJ, Toker A. Tyrosine phosphorylation of protein kinase D in the pleckstrin homology domain leads to activation. J Biol Chem 278: 17969-17976, 2003.
40. Storz P, Doppler H, Toker A. Protein kinase Cdelta selectively regulates protein kinase D-dependent activation of NF-kappaB in oxidative stress signaling. Mol Cell Biol 24: 2614-2626, 2004.
41. Storz P, Toker A. Protein kinase D mediates a stress-induced NF-kappaB activation and survival pathway. EMBO J 22: 109-120, 2003.
42. Stubberfield CR, Cohen GM. Interconversion of NAD(H) to NADP(H). A cellular response to quinone-induced oxidative stress in isolated hepatocytes. Biochem Pharmacol 38: 2631-2637, 1989.
43. Takada Y, Mukhopadhyay A, Kundu GC, Mahabeleshwar GH, Singh S, Aggarwal BB. Hydrogen peroxide activates NF-kappa B through tyrosine phosphorylation of I kappa B alpha and serine phosphorylation of p65: evidence for the involvement of I kappa B alpha kinase and Syk protein-tyrosine kinase. J Biol Chem 278: 24233-24241, 2003.
44. 2? Eur J Gastroenterol Hepatol 20: 555-560, 2008.
45. Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, Frazier A, Yang H, Ivanova S, Borovikova L, Manogue KR, Faist E, Abraham E, Andersson J, Andersson U, Molina PE, Abumrad NN, Sama A, Tracey KJ. HMG-1 as a late mediator of endotoxin lethality in mice. Science 285: 248-251, 1999.
46. Williams IR. CCR6 and CCL20: partners in intestinal immunity and lymphorganogenesis. Ann NY Acad Sci 1072: 52-61, 2006.
47. Yamada T, Grisham MB. Role of neutrophil-derived oxidants in the pathogenesis of intestinal inflammation. Klin Wochenschr 69: 988-994, 1991.
48. Yamamoto K, Fujiyama Y, Andoh A, Bamba T, Okabe H. Oxidative stress increases MICA and MICB gene expression in the human colon carcinoma cell line (CaCo-2). Biochim Biophys Acta 1526: 10-12, 2001.
49. Yamamoto K, Kushima R, Kisaki O, Fujiyama Y, Okabe H. Combined effect of hydrogen peroxide induced oxidative stress and IL-1 alpha on IL-8 production in CaCo-2 cells (a human colon carcinoma cell line) and normal intestinal epithelial cells. Inflammation 27: 123-128, 2003.
50. Yamazaki T, Yang XO, Chung Y, Fukunaga A, Nurieva R, Pappu B, Martin-Orozco N, Kang HS, Ma L, Panopoulos AD, Craig S, Watowich SS, Jetten AM, Tian Q, Dong C. CCR6 regulates the migration of inflammatory and regulatory T cells. J Immunol 181: 8391-8401, 2008.
51. Yanagisawa S, Koarai A, Sugiura H, Ichikawa T, Kanda M, Tanaka R, Akamatsu K, Hirano T, Matsunaga K, Minakata Y, Ichinose M. Oxidative stress augments toll-like receptor 8 mediated neutrophilic responses in healthy subjects. Respir Res 10: 50, 2009.
52. Zhou Y, Wang Q, Evers BM, Chung DH. Signal transduction pathways involved in oxidative stress-induced intestinal epithelial cell apoptosis. Pediatr Res 58: 1192-1197, 2005.
53. Zmijewski JW, Lorne E, Zhao X, Tsuruta Y, Sha Y, Liu G, Abraham E. Antiinflammatory effects of hydrogen peroxide in neutrophil activation and acute lung injury. Am J Respir Crit Care Med 179: 694-704, 2009.