Carrageenan-induced NFκB activation depends on distinct pathways mediated by reactive oxygen species and Hsp27 or by Bcl10

Biochimica et Biophysica Acta - General Subjects

Volumn 1780, Issue 7-8, 2008, Pages 973-982

  Bhattacharyya, Sumit ^a   Dudeja, Pradeep K ^a,b   Tobacman, Joanne K ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b JESSE BROWN VA MEDICAL CENTER   (United States)

Author keywords

Bcl10 (B cell CLL lymphoma 10); Carrageenan; Colonic epithelial cells; Hsp27; IL 8; MAPK; NF B; Reactive oxygen species (ROS); Sulfate assimilation pathway

Indexed keywords

CARRAGEENAN; HEAT SHOCK PROTEIN 27; I KAPPA B KINASE GAMMA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE 12; MITOGEN ACTIVATED PROTEIN KINASE 13; PROTEIN BCL 10; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; TEMPOL; BCL10 PROTEIN, HUMAN; HEAT SHOCK PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

AGED; ARTICLE; COLON MUCOSA; CYTOKINE RELEASE; ENZYME PHOSPHORYLATION; EPITHELIUM CELL; HUMAN; HUMAN CELL; MALE; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; BIOLOGICAL MODEL; CELL LINE; METABOLISM;

ANIMALIA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CARRAGEENAN; CELL LINE; EPITHELIAL CELLS; HEAT-SHOCK PROTEINS; HUMANS; MODELS, BIOLOGICAL; NF-KAPPA B; REACTIVE OXYGEN SPECIES;

EID: 44649175701     PISSN: 03044165     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagen.2008.03.019     Document Type: Article

References (57)

1. Galili U. The alpha-gal epitope and the anti-Gal antibody in xenotransplantation and in cancer immunotherapy. Immunol. Cell Biol. 83 (2005) 674-686
2. Sandrin M.S., Osman N., and McKenzie I.F.C. Transgenic approaches for the reduction in expression of GALα(1,3)GAL for xenotransplantation. Front. Biosci. 2 (1997) e1-e11
3. Osman N., McKenzie I.F.C., Ostenried K., Ioannou Y.A., Desnick R.J., and Sandrin M.S. Combined transgenic expression of alpha-galactosidase and alpha 1,2 fucosyltransferase leads to optimal reduction in the major xenoepitope Gal-alpha(1,3)Gal. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 14677-14682
4. Baumann B.C., Stussi G., Huggel K., Rieben R., and Seebach J.D. Reactivity of human natural antibodies to endothelial cells from Galpha(1,3)Gal-deficient pigs. Transplantation 83 (2007) 193-201
5. Borthakur A., Bhattacharyya S., Dudeja P.K., and Tobacman J.K. Carrageenan induces NFκB activation and interleukin-8 production in normal human colonic epithelial cells. Am. J. Physiol.: Gastrointest. Liver Physiol. 292 (2007) G829-G838
6. Bhattacharyya S., Gill R., Chen M.-L., Zhang F., Linhardt R.J., Dudeja P.K., and Tobacman J.K. Toll-like receptor 4 mediates induction of Bcl10-NFκB-IL-8 inflammatory pathway by carrageenan in human intestinal epithelial cells. J. Biol. Chem. (2008) Feb 5 [Electronic publication ahead of print]
7. Moyer M.P., Manzano L.A., Merriman R.L., Stauffer J.S., and Tanzer L.R. NCM460, a normal human colon mucosal epithelial cell line. In Vitro Cell. Dev. Biol., Anim. 32 (1996) 315-317
8. Ndengele M.M., Muscoli C.W., Zhi Q., Doyle T.M., Matuschak G.M., and Salvemini D. Superoxide potentiates NFκB activation and modulates endotoxin-induced cytokine production in alveolar macrophages. Shock 23 (2005) 186-193
9. Bhattacharyya S., Borthakur A., Pant N., Dudeja P.K., and Tobacman J.K. BCL-10 induces lipopolysaccharide induced activation of NF-κB and IL-8 in human intestinal epithelial cells. Am. J. Physiol.: Gastrointest. Liver Physiol. 293 (2007) G429-G437
10. Affymetrix. Products and Applications. Gene Chip System. Gene Chip Arrays. Human Genome U133 Plus2.0.NetAffx™ Analysis Center. https://www.affymetrix.com.
11. Bhattacharyya S., Dudeja P.K., and Tobacman J.K. Cell cycle arrest in human intestinal epithelial cells following exposure to carrageenan. J. Nutr. 138 (2008) 469-475
12. Whitehead Institute for Medical Research. Primer 3. Cambridge, MA. http://frodo. wi.mit.edu.
13. Park K.J., Gaynor R.B., and Kwak Y.T. 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. 278 (2003) 35272-35278
14. Kammanadiminti S.J., and Chadee K. Suppression of NF-kappaB activation by Entamoeba histolytica in intestinal epithelial cells is mediated by heat shock protein 27. J. Biol. Chem. 281 (2006) 26112-26120
15. Sur R., Lyte P.A., and Southall M.D. Hsp27 regulates pro-inflammatory mediator release in keratinocytes by modulating NF-kappaB signaling. J. Invest. Dermatol. (2007) Nov 15; [Electronic publication ahead of print]
16. Lucas P.C., McAllister-Lucas L.M., and Nunez G. NF-kappa B signaling in lymphocytes: a new cast of characters. J. Cell. Sci. 117 (2004) 31-39
17. Liu Y., Dong W., Chen L., Xiang R., Xiao H., De G., Wang Z., and Qi Y. Bcl10 mediates lipopolysaccharide/Toll-like receptor-4 signaling through interaction with Pellino2. J. Biol. Chem. 279 (2004) 37436-37444
18. Dong W., Liu Y., Peng J., Chen L., Zou T., Xiao H., Liu Z., Li W., Bu Y., and Qi Y. The IRAK-1-BCL10-MALT1-TRAF6-TAK1 cascade mediates signaling to NFκB from Toll-like Receptor 4. J. Biol. Chem. 281 (2006) 26029-26040
19. Sun L., Deng L., Ea C.K., Xia Z.P., and Chen Z.J. The TRAF6 ubiquitin ligase and TAK1 kinase mediate IKK activation by BCL10 and MALT1 in T lymphocytes. Mol. Cell 14 (2004) 289-301
20. McAllister-Lucas L.M., Ruland J., Siu K., Jin X., Gu S., Kim D.S., Kuffa P., Kohrt D., Mak T.W., Nuñez G., and Lucas P.C. CARMA3/Bcl10/MALT1-dependent NFkappaB activation mediates angiotensin II-responsive inflammatory signaling in nonimmune cells. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 139-144
21. Klemm S., Zimmermann S., Peschel C., Mak T.W., and Ruland J. Bcl10 and Malt1 control lysophosphatidic acid-induced NFkappaB activation and cytokine production. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 134-138
22. Wang D., You Y., Lin P.-C., Xue L., Morris S.W., Zeng H., Wen R., and Lin X. Bcl10 plays a critical role in NF-κB activation induced by G protein-coupled receptors. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 145-150
23. Zhang Q., Siebert R., Yan M., Hinzmann B., Cui X., Xue L., Rakestraw K.M., Naeve C.W., Beckmann G., Weisenburger D.D., Sanger W.G., Nowotny H., Vesely M., Callet-Bauchu E., Salles G., Xisit V.M., Rosenthal A., Schlegelberger B., and Morris S.W. Inactivating mutations and overexpression of BCL10, a caspase recruitment domain-containing gene, in MALT lymphoma with t(1;14)(p22;q32). Nat. Gen. 22 (1999) 63-68
24. Willis T.G., Jadayel D.M., Du M.-Q., Peng H., Perry A.R., Abdul-Rauf M., Price H., Karran L., Majekodunmi O., Wlodarska I., Pan L., Crook T., Hamoudi R., Isaacson P.G., and Dyer J.F. Bcl10 is involved in t(1;14)(p22;q32) of MALT B Cell lymphoma and mutated in multiple tumor types. Cell 96 (1999) 46-56
25. Isaacson P.G., and Du M.Q. MALT lymphoma: from morphology to molecules. Nat. Rev., Cancer 4 (2004) 644-654
26. Burns K.A., and Martinon F. Inflammatory diseases: is ubiquitinated NEMO at the Hub?. Curr. Biol. 14 (2004) R1040-R1042
27. Zhou H., Wertz I., O'Rourke K., Ultsch M., Seshagiri S., Eby M., Xiao W., and Dixit V.M. Bcl10 activates the NFκB pathway through ubiquitination of NEMO. Nature 427 (2004) 167-171
28. Cairns J., Qin S., Philp R., Tan Y.H., and Guy G.R. Dephosphorylation of the small heat shock protein Hsp27 in vivo by protein phosphatase 2A. J. Biol. Chem. 269 (2003) 9176-9183
29. Kray A.E., Carter R.S., Pennington K.N., Gomez R.J., Sanders L.E., Llanes J.M., Khan W.N., Ballard D.W., and Wadzinski B.E. Positive regulation of IkappaB kinase signaling by protein serine/threonine phosphatase 2A. J. Biol. Chem. 280 (2005) 35974-35982
30. Tar K., Csortos C., Czikora I., Olah G., Ma S.F., Wadgaonkar R., Gergely P., Garcia J.G., and Verin A.D. Role of protein phosphatase 2A in the regulation of endothelial cell cytoskeleton structure. J. Cell. Biochem. 98 (2006) 931-953
31. Li S., Wang L., Berman M.A., Zhang Y., and Dorf M.E. RNAi screen in mouse astrocytes identifies phosphatases that regulate NF-kappaB signaling. Mol. Cell 24 (2006) 497-509
32. Bhattacharyya S., Borthakur A., Dudeja P.K., and Tobacman J.K. Carrageenan reduces bone morphogenetic protein-4 (BMP4) and activates wnt/β-catenin pathway in normal human colonic epithelial cells. Dig. Dis. Sci. 52 (2007) 2766-2774
33. Woods J.S., Kavanagh T.J., Corral J., Reese A.W., Diaz D., and Ellis M.E. 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. 160 (1999) 207-216
34. Dalton T.P., Chen Y., Schneider S.N., Nebert D.W., and Shertzer H.G. Genetically altered mice to evaluate glutathione homeostasis in health and disease. Free Radic. Biol. Med. 37 (2004) 1511-1526
35. Ray S., Watkins D.N., Misso N.L., and Thompson P.J. Oxidant stress induces gamma-glutamylcysteine synthetase and glutathione synthesis in human bronchial epithelial NCI-H292 cells. Clin. Exp. Allergy 32 (2002) 571-577
36. Jacob C., Holme A.L., and Fry F.H. The sulfinic acid switch in proteins. Org. Biomol. Chem. 2 (2004) 1953-1956
37. Chang T.S., Jeong W., Woo H.A., Lee S.M., Park S., and Rhee S.G. 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. 279 (2004) 50994-51001
38. Rhee S.G., Jeong W., Chang T.S., and Woo H.A. Sulfiredoxin, the cysteine sulfinic acid reductase specific to 2-Cys peroxiredoxin: its discovery, mechanism of action, and biological significance. Kidney Inter., Suppl. 106 (2007) S3-S8
39. Mendoza-Cózatl D., Loza-Tavera H., Hernández-Navarro A., and Moreno-Sánchez R. Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants. FEMS Microbiol. Rev. 29 (2005) 653-671
40. Höfgen R., Kreft O., Willmitzer L., and Hesse H. Manipulation of thiol contents in plants. Amino Acids 20 (2001) 291-299
41. Kopriva S. Regulation of sulfate assimilation in Arabidopsis and beyond. Ann. Bot. (Lond) 97 (2006) 479-495
42. Mougous J.D., Lee D.H., Hubbard S.C., Schelle M.W., Vocadlo D.J., Berger J.M., and Bertozzi C.R. Molecular basis for G protein control of the prokaryotic ATP sulfurylase. Mol. Cell. 21 (2006) 109-122
43. Sun M., Andreassi 2nd J.L., Liu S., Pinto R., Triccas J.A., and Leyh T.S. The trifunctional sulfate-activating complex (SAC) of Mycobacterium tuberculosis. J. Biol. Chem. 280 (2005) 7861-7866
44. Gavel O.Y., Bursakov S.A., Calvete J.J., George G.N., Moura J.J., and Moura I. ATP sulfurylases from sulfate-reducing bacteria of the genus Desulfovibrio. A novel metalloprotein containing cobalt and zinc. Biochemistry 37 (1998) 16225-16232
45. Dhia Thabet O.B., Fardeau M.L., Suarez-Nuñez C., Hamdi M., Thomas P., Ollivier B., and Alazard D. Desulfovibrio marinus sp. nov., a moderately halophilic sulfate-reducing bacterium isolated from marine sediments in Tunisia. Int. J. Syst. Evol. Microbiol. 57 (2007) 2167-2170
46. Meng Z. Oxidative damage of sulfur dioxide on various organs of mice: sulfur dioxide is a systemic oxidative damage agent. Inhal. Toxicol. 15 (2003) 281-295
47. Meng Z., Liu Y., and Wu D. Effect of sulfur dioxide inhalation on cytokine levels in lungs and serum of mice. Inhal. Toxciol. 17 (2005) 303-307
48. Langley-Evans S.C., Phillips G.J., and Jackson A.A. Sulphur dioxide: a potent glutathione depleting agent. Comp. Biochem. Physiol., C Pharmacol. Toxicol. Endocrinol. 114 (1996) 89-98
49. 3) in vitro. Hum. Exp. Toxicol. 17 (1998) 600-605
50. Okumura T., Sakakibara A., Murata Y., and Kita Y. Mathematical analysis of involvement ratio between central and peripheral COX-2 in rat pain models with two types of COX-2 inhibitors with different distribution, celecoxib and CIAA. Eur. J. Pharmacol. 578 (2008) 97-99
51. Albertini R., Aimbire F., Villaverde A.B., Silva Jr. J.A., and Costa M.S. COX-2 mRNA expression decreases in the subplantar muscle of rat paw subjected to carrageenan-induced inflammation after low level laser therapy. Inflamm. Res. 56 (2007) 228-229
52. Zhang Y., Shaffer A., Portanova J., Seibert K., and Isakson P.C. Inhibition of cyclooxygenase-2 rapidly reverses inflammatory hyperalgesia and prostaglandin E2 production. J. Pharmacol. Exp. Ther. 283 (1997) 1069-1075
53. Cuzzocrea S., Mazzon E., Calabro G., Dugo L., De Sarro A., van De Loo F.A., and Caputi A.P. Inducible nitric oxide synthase-knockout mice exhibit resistance to pleurisy and lung injury caused by carrageenan. Am. J. Respir. Crit. Care Med. 162 (2000) 1859-1866
54. Rossi A., Cuzzocrea S., Mazzon E., Serraino I., De Sarro A., Dugo L., and Felice M.R. Regulation of prostaglandin generation in carrageenan-induced pleurisy by inducible nitric oxide synthase in knockout mice. Life Sci. 72 (2003) 1199-1208
55. Di Paola R., Mazzon E., Muià C., Genovese T., Menegazzi M., Zaffini R., Suzuki H., and Cuzzocrea S. Green tea polyphenol extract attenuates lung injury. Respir. Res. 6 (2005) 66-79
56. Roberts P., Riley G.P., Morgan K., Miller R., Hunter J.O., and Middleton S.J. The physiological expression of inducible nitric oxide synthase (iNOS) in the human colon. J. Clin. Pathol. 54 (2001) 293-297
57. Kankuri E., Hamalainen M., Hukkanen M., Salmenpera P.K., Kivilaakso E., Vapaatalo H., and Moilanen E. 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. 38 (2003) 186-193