Salmonella typhimurium induces epithelial IL-8 expression via Ca2+- mediated activation of the NF-κb pathway

Journal of Clinical Investigation

Volumn 105, Issue 1, 2000, Pages 79-92

  Gewirtz, Andrew T ^a   Rao, Anjali S ^a   Simon Jr , Peter O ^a   Merlin, Didier ^a   Carnes, Denice ^a   Madara, James L ^a   Neish, Andrew S ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CARBACHOL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; IONOMYCIN; THAPSIGARGIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; EPITHELIUM CELL; INFLAMMATION; INTESTINE EPITHELIUM; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; SALMONELLA TYPHIMURIUM;

EID: 0033989283     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI8066     Document Type: Article

References (70)

1. Madara, J.L. 1990. Pathobiology of the intestinal epithelial barrier. Am. J. Pathol. 137:1273-1281.
2. Yamada, T., Alpers, D.H., Owyang, C., Powell, D.W., and Silverstein, F.E. 1995. Textbook of gastroenterology. J.B. Lippincott. Philadelphia, PA. 1606-1629.
3. Takeuchi, A. 1967. Electron microscope studies of experimental Salmonella infection. Am. J. Pathol. 50:109-119.
4. McCormick, B., Gerwirtz, A., and Madara, J.L. 1998. Epithelial crosstalk with bacteria and immune cells. Curr. Opin. Gastro. 14:492-497.
5. McCormick, B.A., Miller, S.I., and Madara, J.L. 1996. New insights on molecular pathways utilized by salmonella species in cell binding. Front. Biosci. 1:d131-d145.
6. Eckmann, L., et al. 1993. Differential cytokine expression by human intestinal epithelial cell lines: regulated expression of interleukin-8. Gastroenterology. 105:1689-1697.
7. Eckmann, L., Kagnoff, M., and Fierer, J. 1993. Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infect. Immun. 61:4569-4574.
8. McCormick, B.A., Colgan, S.P., Archer, C.D., Miller, S.I., and Madara, J.L. 1993. Salmonella typhimurium attachment to human intestinal epithelial monolayers: transcellular signalling to subepithelial neutrophils. J. Cell Biol. 123:895-907.
9. Jung, H C., et al. 1995. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J. Clin. Invest. 95:55-65.
10. Gewirtz, A.T., et al. 1998. Pathogen-induced chemokine secretion from model intestinal epithelium is inhibited by lipoxin A4 analogs. J. Clin. Invest. 101:1860-1869.
11. McCormick, B., et al. 1995. Surface attachment of Salmonella typhimurium to intestinal epithelia imprints the subepithelial matrix with gradients chemotoctic for neutrophils. J. Cell Biol. 131:1599-1608.
12. Kunsch, C., and Rosen, C.A. 1993. NF-kappa B subunit-specific regulation of ehe interleukin-8 promoter. Mol. Cell. Biol. 13:6137-6146.
13. Kunsch, C., Lang, R.K., Rosen, C.A., and Shannon, M.E 1994. Synergistic transcriptional activation of the IL-8 gene by NF-kappa B p65 (RelA) and NF-IL-6. J. Immunol. 153:153-164.
14. Mukaida, N., Shiroo, M., and Matsushima, K. 1989. Genomic structure of the human monocyte-derived neutrophil chemotactic factor IL-8. J. Immunol. 143:1366-1371.
15. Mukaida, N., Mahe, Y., and Matsushima, K. 1990. Cooperative interaction of nuclear factor-kappa B- and cis-regulatory enhancer binding protein-like factor binding elements in activating the interleukin-8 gene by pro-inflammatory cytokines. J. Biol. Chem. 265:21128-21133.
16. Mukaida, N., Okamoto, S., Ishikawa, Y., and Matsushima, K. 1994. Molecular mechanism of interleukin-8 gene expression. J. Leukoc. Biol. 56:554-558.
17. Ghosh, S., May, M.J., and Kopp, E.B. 1998. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16:225-260.
18. Bauerle, P. 1998. Pro-inflammatory signaling: last pieces in the NF-kB puzzle? Curr. Biol. 8:19-22.
19. Thanos, D., and Maniatis, T. 1995. NF-kappa B: a lesson in family values. Cell. 80:529-532.
20. Hobbie, S., Chen, L., Davis, R., and Galan, J.H. 1997. Involvement of mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal epithelial cells. J. Immunol. 159:5550-5559.
21. Pace, J., Hayman, M.J., and Galan, J.E. 1993. Signal transduction and invasion of epithelial cells by S. typhimurium. Cell. 72:505-514.
22. Ruschkowski, S., Rosenshine, I., and Finlay, B. 1992. Salmonella typhimurium induces an inositol phosphate flux in infected epithelial cells. FEMS Microbiol. Lett. 74:121-126.
23. Pahl, H.L., Sester, M., Burgert, H.G., and Baeuerle, P.A. 1996. Activation of transcription factor NF-kappaB by the adenovirus E3/19K protein requires its ER retention. J. Cell Biol. 132:511-522.
24. Lieb, K., Fiebich, B.L., Berger, M., Bauer, J., and Schulze-Osthoff, K. 1997. The neuropeptide substance P activates transcription factor NF-kappa B and kappa B-dependent gene expression in human astrocytoma cells. J. Immunol. 159:4952-4958.
25. Dharmsathaphorn, K., and Madara, J.L. 1990. Established intestinal cell lines as model systems for electrolyte transport studies. Methods Enzymol. 192:354-389.
26. Seeroo, K.F., et al. 1997. A cytosolic calcium transient is not necessary for degranulation or oxidative burst in immune complex-stimulated neurrophils. J. Leukoc. Biol. 62:329-340.
27. Gewirtz, A.T., Siber, A.M., Madara, J.L., and McCormick, B.A. 1999. Orchestration of neutrophil movement by intestinal epithelial cells in response to salmonella typhimurium can be uncoupled from bacterial internalization. Infect. Immun. 67:608-617.
28. Neish, A.S., et al. 1995. Endothelial interferon regulatory factor 1 cooperates with NF-kappa B as a transcriptional activator of vascular cell adhesion molecule 1. Mol. Cell. Biol. 15:2558-2569.
29. Fiedler, M.A. Wernke-Dollries, K. and Stark, J.M. 1998. Inhibition of TNF-alpha-induced NF-kappaB activation and IL-8 release in A549 cells with the proteasome inhibitor MG-132. Am. J. Respir. Cell Mol Biol. 19:259-268.
30. Read, M. A., et al. 1995. The proteasome pathway is required for cytokine-induced Endothelial-leukocyte adhesion molecule expression. Immunity. 2:493-506.
31. Dickinson, K.E., Frizzell, R.A., and Sekar, M.C. 1992. Activation of T84 cell chloride channels by carbachol involves a phosphoinositide-coupled muscarinic M3 receptor. Eur. J. Pharmacol. 225:291-298.
32. Fischer, H., Illek, B., Negulescu, P.A. Clauss, W., and Machen, T.E. 1992. Carbachol-activated calcium entry into HT-29 cells is regulated by both membrane potential and cell volume. Proc. Natl. Acad. Sci. USA. 89:1438-1442.
33. Kuznetsov, G., Brostrom, M.A., and Brostrom, C.O. 1992. Demonstration of a calcium requirement for secretory protein processing and export. Differencial effects of calcium and dithiothreitol. J. Biol. Chem. 267:3932-3939.
34. Takemura, H., Hughes, A.R., Thastrup, O., and Putney, J.W., Jr. 1989. Activation of calcium entry by the tumor promoter thapsigargin in parotid acinar cells. Evidence that an intracellular calcium pool and not an inositol phosphate regulates calcium fluxes at the plasma membrane. J. Biol. Chem. 264:12266-12271.
35. Henderson, R.M., Ashford, M.L., MacVinish, L.J., and Cuthbert, A.W. 1992. Chloride channels and anion fluxes in a human colonic epithelium (HCA-7). Br. J. Pharmacol. 106:109-114.
36. McCormick, B., Miller, S., Carnes, D., and Madara, J. 1995. Transepithelial signaling to neutrophils by Salmonellae: a novel virulence mechanism for gastroenteritis. Infect. Immun. 63:2302-2309.
37. Bajaj, V., Hwang, C., and Lee, C.A. 1995. hilA is a novel ompR/toxR family member that activates the expression of Salmonella typhimurium invasion genes. Mol. Microbiol. 18:715-727.
38. Garcia Vescovi, E., Soncini, F.C., and Groisman, E.A. Mg2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell. 1996, 84:165-174.
39. Miller, S., and Mekalanos, J. 1990. Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages. J. Bacteriol. 172:2485-2490.
40. Eaves-Pyles, T., Szabo, C., and Salzman, A.L. 1999. Bacterial invasion is not required for activation of NF-kappaB in enterocytes. Infect. Immun. 67:800-804.
41. Daig, R., et al. 1996. Increased interleukin 8 expression in the colon mucosa of patients with inflammatory bowel disease. Gut. 38:216-222.
42. Funakoshi, K., et al. 1995. Study of cytokines in ulcerative colitis. J. Gastroenterol. 30(Suppl. 8):61-63.
43. Mazzucchelli, L., et al. 1994. Expression of interleukin-8 gene in inflammatory bowel disease is related to the histological grade of active inflammation. Am. J. Pathol. 144:997-1007.
44. Nielsen, O.H., Rudiger, N., Gaustadnes, M., and Horn, T. 1997. Intestinal interleukin-8 concentration and gene expression in inflammatory bowel disease. Scand. J. Gastroenterol. 32:1028-1034.
45. Foubister, V., Rosenshine, I., and Finlay, B.B. 1994. A diarrheal pathogen, enteropathogenic Escherichia coli (EPEC), triggers a flux of inositol phosphates in infected epithelial cells. J. Exp. Med. 179:993-998.
46. Baldwin, T.J., Ward, W., Aitken, A., Knutton. S., and Williams, P.H. 1991. Elevation of in tracellular free calcium levels in HEp-2 cells infected with enteropathogenic Escherichia coli. Infect. Immun. 59:1599-1604.
47. Savkovic, S.D., Koutsouris, A., and Hecht, G. 1997. Activation of NF-kappaB in intestinal epithelial cells by enteropathogenic Escherichia coli. Am. J. Physiol. 273:C1160-C1167.
48. Miller, S. 1991. PhoP/PhoQ: macrophage-specific modulators of Salmonella virulence? Mol. Microbiol. 5:2073-2078.
49. Guo, L., et al. 1997. Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ. Science. 276:250-253.
50. Woods, J.S., Ellis, M.E. Diegez-Acuna, F.J., and Corral, J. 1999. Activation of NF-κB in normal rat kidney epithelial (NRK52E) cells is mediated via a redox-insensitive, calcium-dependent pathway. Toxicol. Appl. Pharmacol. 154:219-227.
51. Hsuan, S.L., et al. 1999. Pasteurella haemolytica leukotoxin and endotoxin induced cytokine gene expression in bovine alveolar macrophages requires NF-kappaB activation and calcium elevation. Microb. Pathog. 26:263-273.
52. Fischer, C., et al. 1999. Differential effects of lipopolysaccharide and tumor necrosis factor on monocytic IkappaB kinase signal some activation and IkappaB proteolysis. J. Biol. Chem. 274:24625-24632.
53. Henkel, T., et al. 1993. Rapid proteolysis of I kappa B-alpha is necessary for activation of transcription factor NF-kappa B. Nature. 365:182-185.
54. Brunkhorst, B.A., et al. 1992. Differential roles of FcγRII and FcγRIII in immune complex stimulation of human neutrophils. J. Biol. Chem. 267:20659-20666.
55. Strohmeier, G.R., et al. 1995. Role of the Fc gamma R subclasses Fc gamma RII and Fc gamma RIII in the activation of human neutrophils by low and high valency immune complexes. J. Leukoc. Biol. 58:415-422.
56. DiMango, E., Ratner, A.J., Bryan, R., Tabibi, S., and Prince, A. 1998. Activation of NF-kappaB by adherent Pseudamonas aeruginosa in normal and cystic fibrosis respiratory epithelial cells. J. Clin. Invest. 101:2598-2605.
57. Rosales, C., and Brown, E.J. 1992. Signal transduction by neutrophil immunoglobulin G Fc receptors. Dissociation of intracytoplasmic calcium concentration rise from inositol 1,4,5-trisphosphate. J. Biol. Chem. 267:5265-5271.
58. Muller, A., et al. 1999. Neisserial porin (PorB) causes rapid calcium influx in target cells and induces apoptosis by the activation of cysteine proteases. EMBO J. 18:339-352.
59. Cornelis, G.R., and Wolf-Watz, H. 1997. The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol. Microbiol. 23:861-867.
60. Kenny, B., et al. 1997. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell. 91:511-520.
61. Wood, M., Rosqvist, R., Mullan, P., Edwards, M., and Galyov, E. 1996. SopE, a secreted protein of Salmonella dublin, is translocated into the target eukaryotic cell via a sip-dependent mechanism and promotes bacterial entry. Mol. Microbiol. 22:327-338.
62. Norris, F.A., Wilson, M.P., Wallis, T.S., Galyov, E.E., and Majerus, P.W. 1998. SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc. Natl. Acad. Sci. USA. 95:14057-14059.
63. Hardt, W.D., Chen, L.M., Schuebel, K.E., Bustelo, X.R., and Galan, J.E. 1998. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell. 93:815-826.
64. Stancovski, I., and Baltimore, D. 1997. NF-kappaB activation: the I kappaB kinase revealed? Cell. 91:299-302.
65. Jobin, C., et al. 1999. TNF receptor-associated factor-2 is involved in both IL-1 beta and TNF-alpha signaling cascades leading to NF-kappa B activation and IL-8 expression in human intestinal epithelial cells. J. Immunol. 162:4447-4454.
66. Chen, Z.J., Parent, L., and Maniatis, T. 1996. Site-specific phosphorylation of IkappaBalpha by a novel ubiquitmation-dependent protein kinase activity. Cell. 84:853-862.
67. Maniatis, T. 1997 Catalysis by a multiprotein IkappaB kinase complex. Science, 278:818-819.
68. Lee, F.S., Hagler, J., Chen, Z.J., and Maniatis, T. 1997. Activation of the IkappaB alpha kinase complex by MEKK1, a kinase of the JNK pathway. Cell. 88:213-22.
69. Kuhn, R., Lohler, J., Rennick, D., Rajewsky, K., and Muller, W. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 75:263-274.
70. Panwala, C.M., Jones, J.C. and Viney, J.L. 1998. A novel model of inflammatory bowel disease: mice deficient for the multiple drug resistance gene, mdr1a, spontaneously develop colitis. J. Immunol. 161:5733-5744.