Original Article

You have full text access to this OnlineOpen article

ROS, Hsp27, and IKKβ mediate dextran sodium sulfate (DSS) activation of IκBa, NFκB, and IL-8

  1. Sumit Bhattacharyya PhD1,
  2. Pradeep K. Dudeja PhD1,2,
  3. Joanne K. Tobacman MD1,2,*

Article first published online: 11 DEC 2008

DOI: 10.1002/ibd.20821

Issue

Inflammatory Bowel Diseases

Inflammatory Bowel Diseases

Volume 15, Issue 5, pages 673–683, May 2009

Additional Information

How to Cite

Bhattacharyya, S., Dudeja, P. K. and Tobacman, J. K. (2009), ROS, Hsp27, and IKKβ mediate dextran sodium sulfate (DSS) activation of IκBa, NFκB, and IL-8. Inflamm Bowel Dis, 15: 673–683. doi: 10.1002/ibd.20821

Author Information

  1. 1

    Department of Medicine, University of Illinois at Chicago

  2. 2

    Jesse Brown VAMC, Chicago, Illinois

*Department of Medicine, University of Illinois at Chicago, 840 S. Wood St. M/C 718, CSN 440, Chicago, IL 60612

Publication History

  1. Issue published online: 7 APR 2009
  2. Article first published online: 11 DEC 2008
  3. Manuscript Accepted: 14 OCT 2008
  4. Manuscript Received: 23 SEP 2008

Funded by

  • Department of Veterans Affairs
  • NIDDK. Grant Numbers: DK54016, DK68324

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (392K)

REFERENCES

  • 1
    Onderdonk AB. The carrageenan model for experimental ulcerative colitis. Prog Clin Biol Res. 1985; 186: 237–245.
  • 2
    Kitano A, Matsumoto T, Oshitani N, et al. Distribution and anti-inflammatory effect of mesalazine on carrageenan-induced colitis in the rabbit. Clin Exp Pharmacol Physiol. 1996; 23: 305–309.
    Direct Link:
  • 3
    Murano M, Maemura K, Hirata I, et al. Therapeutic effect of intracolonically administered nuclear factor kappa B (p65) antisense oligonucleotide on mouse dextran sulphate sodium (DSS)-induced colitis. Clin Exp Immunol. 2000; 120: 51–58.
    Direct Link:
  • 4
    Herfarth H, Brand K, Rath HC, et al. Nuclear factor-kappa B activity and intestinal inflammation in dextran sulphate sodium (DSS)-induced colitis in mice is suppressed by gliotoxin. Clin Exp Immunol. 2000; 120: 59–65.
    Direct Link:
  • 5
    Venkatraman A, Ramakrishna B, Shaji RV, et al. Amelioration of dextran sulfate colitis by butyrate: role of heat shock protein 70 and NF-κB. Am J Physiol Gastrointest Liver Physiol. 2003; 285: G177–G184.
  • 6
    Jaysekhar P, Rao SB, Santhakumari G. Effect of 5-substituted benxylideneaminosalicylic acid on carrageenan-induced ulcerative colitis. Boll Chim Farm. 2004; 143: 309–313.
  • 7
    Oh PS, Lim KT. Plant originated glycoprotein has anti-oxidative and anti-inflammatory effects on dextran sulfate sodium-induced colitis in mouse. J Biomed Sci. 2006; 13: 549–560.
  • 8
    Oz HS, Chen TS, McClain CJ, et al. Antioxidants as novel therapy in a murine model of colitis. J Nutr Biochem. 2005; 16: 297–304.
  • 9
    Egger B, Bajaj-Elliott M, MacDonald TT, et al. Characterisation of acute murine dextran sodium sulphate colitis: cytokine profile and dose dependency. Digestion. 2000; 62: 240–248.
  • 10
    Camuesco D, Gálvez J, Nieto A, et al. Dietary olive oil supplemented with fish oil, rich in EPA and DHA (n-3) polyunsaturated fatty acids, attenuates colonic inflammation in rats with DSS-induced colitis. J Nutr. 2005; 135: 687–694.
  • 11
    Borthakur A, Bhattacharyya S, Dudeja PK, et al. Carrageenan induces Interleukin-8 production through distinct Bcl10 pathway in normal human colonic epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2007; 292: G829–838.
  • 12
    Bhattacharyya S, Borthakur A, Pant N, et al. Bcl10 mediates lipopolysaccharide (LPS)-induced activation of NFκB and IL-8 in human intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2007; 293: G429–437.
  • 13
    McAllister-Lucas LM, Ruland J, Siu K, et al. CARMA3/Bcl10/MALT1-dependent NFkappaB activation mediates angiotensin II-responsive inflammatory signaling in nonimmune cells. Proc Natl Acad Sci U S A. 2007; 104: 139–144.
  • 14
    Klemm S, Zimmermann S, Peschel C, et al. Bcl10 and Malt1 control lysophosphatidic acid-induced NF-kappa B activation and cytokine production. Proc Natl Acad Sci U S A. 2007; 104: 134–138.
  • 15
    Wang D, You Y, Lin PC, et al. Bcl10 plays a critical role in NF-κB activation induced by G protein-coupled receptors. Proc Natl Acad Sci U S A. 2007; 104: 145–150.
  • 16
    Zhang Q, Siebert R, Yan M, et al. Inactivating mutations and overexpression of BCL10, a caspase recruitment domain-containing gene, in MALT lymphoma with t(1;14)(p22;q32). Nat Genet. 1999; 22: 63–68.
  • 17
    Isaacson PG, Du MQ. MALT lymphoma: from morphology to molecules. Nat Rev Cancer. 2004; 4: 644–653.
  • 18
    Willis TG, Jadayel DM, Du MQ, et al. Bcl10 is involved in t(1;14)(p22;q32) of MALT B cell lymphoma and mutated in multiple tumor types. Cell. 1999; 96: 335–345.
  • 19
    Keshavarzian A, Fusunyan RD, Jacyno M, et al. Increased interleukin-8 (IL-8) in rectal dialysate from patients with ulcerative colitis: evidence for a biological role for IL-8 in inflammation of the colon. Am J Gastroenterol. 1999; 94: 704–712.
    Direct Link:
  • 20
    Kankuri E, Hämäläinen M, Hukkanen M, et al. Suppression of pro-inflammatory cytokine release by selective inhibition of inducible nitric oxide synthase in mucosal explants from patients with ulcerative colitis. Scand J Gastroenterol. 2003; 38: 186–192.
  • 21
    Levine JJ, Pettei MJ, Valderrama E, et al. Nitric oxide and inflammatory bowel disease: evidence for local intestinal production in children with active colonic disease. J Pediatr Gastroenterol. Nutr. 1998; 26: 34–38.
  • 22
    Park KJ, Gaynor RB, Kwak YT. Heat shock protein 27 association with the I kappa B kinase complex regulates tumor necrosis factor alpha-induced NF-kappa B activation. J Biol Chem. 2003; 278: 35272–35278.
  • 23
    Kammanadiminti SJ, Chadee K. Suppression of NF-kappa B activation by Entamoeba histolytica in intestinal epithelial cells is mediated by heat shock protein 27. J Biol Chem. 2006; 281: 26112–26120.
  • 24
    Sur R, Lyte PA, Southall MD. Hsp27 regulates pro-inflammatory mediator release in keratinocytes by modulating NF-kappaB signaling. J Invest Dermatol. 2008; 128: 1116–1122.
  • 25
    Jobin C, Sartor RB. The I kappa B/NF-kappa B system: a key determinant of mucosal inflammation and protection. Am J Physiol Cell Physiol. 2000; 278: C451–C462.
  • 26
    Jung HC, Eckmann L, Yang SK, et al. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest. 1995; 95: 55–65.
  • 27
    Moyer MP, Manzano LA, Merriman RL, et al. NCM460, a normal human colon mucosal epithelial cell line. In Vitro Cell Dev Biol Anim. 1996; 32: 315–317.
  • 28
    Li ZW, Chu W, Hu Y, et al. The IKKbeta subunit of IkappaB kinase (IKK) is essential for nuclear factor kappaB activation and prevention of apoptosis. J Exp Med. 1999; 189: 1839–1845.
  • 29
    Ndengele MM, Muscoli C, Wang ZQ, et al. Superoxide potentiates NF-kappaB activation and modulates endotoxin-induced cytokine production in alveolar macrophages. Shock. 2005; 23: 186–193.
  • 30
    Araki Y, Sugihara H, Hattori T. The free radical scavengers edaravone and tempol suppress experimental dextran sulfate sodium-induced colitis in mice. Int J Mol Med. 2006; 17: 331–334.
  • 31
    Lejeune D, Hasanuzzaman M, Pitcock A, et al. The superoxide scavenger TEMPOL induces urokinase receptor (uPAR) expression in human prostate cancer cells. Mol Cancer. 2006; 5: 21.
  • 32
    Cuzzocrea S, McDonald MC, Mazzon E, et al. Tempol, a membrane-permeable radical scavenger, reduces dinitrobenezene sulfonic acid-induced colitis. Eur J Pharmacol. 2000; 406: 127–137.
  • 33
    Yang J, Su Y, Richmond A. Antioxidants tiron and N-acetyl-L-cysteine differentially mediate apoptosis in melanoma cells via a reactive oxygen species-independent NF-kappaB pathway. Free Radic Biol Med. 2007; 42: 1369–1380.
  • 34
    Bhattacharyya S, Pant N, Dudeja PK, et al. Development, evaluation, and application of a highly sensitive microtiter plate ELISA for human Bcl10 protein. J Immunoassay Immunochem. 2007; 28: 173–188.
  • 35
    Bhattacharyya S, Dudeja PK, Tobacman JK. Carrageenan-induced NFkappaB activation depends on distinct pathways mediated by reactive oxygen species and Hsp27 or by Bcl10. Biochim Biophys Acta. 2008; 1780: 973–982.
  • 36
    Bhattacharyya S, Gill R, Chen M-L, et al. Toll-like receptor 4 mediates induction of Bcl10-NFκB-IL-8 inflammatory pathway by carrageenan in human intestinal epithelial cells. J Biol Chem. 2008; 283: 10550–10558.
  • 37
    Zughaier SM, Zimmer SM, Datta A, et al. Differential induction of the toll-like receptor 4-MyD88-dependent and -independent signaling pathways by endotoxins. Infect Immun. 2005; 73: 2940–2950.
  • 38
    Guillot L, Medjane S, Le-Barillec K, et al. Response of human pulmonary epithelial cells to lipopolysaccharide involves Toll-like receptor 4 (TLR4)-dependent signaling pathways. J Biol Chem. 2004; 279: 2712–2718.
  • 39
    Powers JP, Li S, Jaen JC, et al. Discovery and initial SAR of inhibitors of interleukin-1 receptor-associated kinase-4. Bioorg Med Chem Lett. 2006; 16: 2842–2845.
  • 40
    Krieglstein CF, Cerwinka WH, Laroux FS, et al. Regulation of murine intestinal inflammation by reactive metabolites of oxygen and nitrogen: divergent roles of superoxide and nitric oxide. J Exp Med. 2001; 94: 1207–1218.
  • 41
    Kolios G, Rooney N, Murphy CT, et al. Expression of inducible nitric oxide synthase activity in human colon epithelial cells: modulation by T lymphocyte derived cytokines. Gut. 1998; 43: 56–63.
  • 42
    Roberts PJ, Riley GP, Morgan K, et al. The physiological expression of inducible nitric oxide synthase (iNOS) in the human colon. J Clin Pathol. 2001; 54: 293–297.
  • 43
    Menconi MJ, Unno N, Smith M, et al. Nitric oxide donor-induced hyperpermeability of cultured intestinal epithelial monolayers: role of superoxide radical, hydroxyl radical, and peroxynitrite. Biochim Biophys Acta. 1998; 1425: 189–203.
  • 44
    Kruidenier L, van Meeteren ME, Kuiper I, et al. Attenuated mild colonic inflammation and improved survival from severe DSS-colitis of transgenic Cu/Zn-SOD mice. Free Radic Biol Med. 2003; 34: 753–765.
  • 45
    Kopriva S. Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot (Lond). 2006; 97: 479–495.
  • 46
    Höfgen R, Kreft O, Willmitzer L, et al. Manipulation of thiol contents in plants. Amino Acids. 2001; 20: 291–299.
  • 47
    Meng Z. Oxidative damage of sulfur dioxide on various organs of mice: sulfur dioxide is a systemic oxidative damage agent. Inhal Toxicol. 2003; 15: 181–195.
  • 48
    Dhia Thabet OB, Fardeau ML, Suarez-Nuñez C, et al. Desulfovibrio marinus sp. nov., a moderately halophilic sulfate-reducing bacterium isolated from marine sediments in Tunisia. Int J Syst Evol Microbiol. 2007; 57: 2167–2170.
  • 49
    Jacob C, Holme AL, Fry FH. The sulfinic acid switch in proteins. Org Biomol Chem. 2004; 2: 1953–1956.
  • 50
    Chang TS, Jeong W, Woo HA, et al. Characterization of mammalian sulfiredoxin and its reactivation of hyperoxidized peroxiredoxin through reduction of cysteine sulfinic acid in the active site to cysteine. J Biol Chem. 2004; 279: 50994–51001.
  • 51
    Woods JS, Kavanagh TJ, Corral J, et al. The role of glutathione in chronic adaptation to oxidative stress: studies in a normal rat kidney epithelial (NRK52E) cell model of sustained upregulation of glutathione biosynthesis. Toxicol Appl Pharmacol. 1999; 160: 207–216.
  • 52
    Dalton TP, Chen Y, Schneider SN, et al. Genetically altered mice to evaluate glutathione homeostasis in health and disease. Free Radic Biol Med. 2004; 37: 1511–1526.
  • 53
    Jowett SL, Seal CJ, Pearce MS, et al. Influence of dietary factors on the clinical course of ulcerative colitis: a prospective cohort study. Gut. 2004; 53: 1479–1484.
  • 54
    Cairns J, Qin S, Philp R, et al. Dephosphorylation of the small heat shock protein Hsp27 in vivo by protein phosphatase 2A. J Biol Chem. 1994; 69: 9176–9183.
  • 55
    Kray AE, Carter RS, Pennington KN, et al. Positive regulation of IkappaB kinase signaling by protein serine/threonine phosphatase 2A. J Biol Chem. 2005; 280: 35974–35982.
  • 56
    Tar K, Csortos C, Czikora I, et al. Role of protein phosphatase 2A in the regulation of endothelial cell cytoskeleton structure. J Cell Biochem. 2006; 98: 931–953.
    Direct Link:
  • 57
    Arrigo AP. The cellular “networking” of mammalian Hsp27 and its functions in the control of protein folding, redox state and apoptosis. Adv Exp Med Biol. 2007; 594: 14–26.
  • 58
    Landry J, Huot J. Modulation of actin dynamics during stress and physiological stimulation by a signaling pathway involving p38 MAP kinase and heat-shock protein 27. Biochem Cell Biol. 1995; 73: 703–707.
View Full Article (HTML) Get PDF (392K)