β-defensin-2 expression is regulated by TLR signaling in intestinal epithelial cells

Journal of Immunology

Volumn 173, Issue 9, 2004, Pages 5398-5405

  Vora, Puja ^b   Youdim, Adrienne ^b   Thomas, Lisa S ^b   Fukata, Masayuki ^a   Tesfay, Samuel Y ^b   Lukasek, Katie ^b   Michelsen, Kathrin S ^b   Wada, Akihiro ^c   Hirayama, Toshiya ^c   Arditi, Moshe ^b   Abreu, Maria T ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b BURNS AND ALLEN RESEARCH INSTITUTE   (United States)

^c NAGASAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA DEFENSIN 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; PEPTIDOGLYCAN; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR AP 1;

ARTICLE; CELL INVASION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME INHIBITION; GENE MUTATION; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN SECRETION; REGULATORY MECHANISM; REPORTER GENE; SIGNAL TRANSDUCTION;

EID: 6344225825     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.173.9.5398     Document Type: Article

References (60)

1. Hecht, G. 1999. Innate mechanisms of epithelial host defense: spotlight on intestine. Am. J. Physiol. 277:C351.
2. Stadnyk, A. W. 2002. Intestinal epithelial cells as a source of inflammatory cytokines and chemokines. Can. J. Gastroenterol. 16:241.
3. Porter, E. M., C. L. Bevins, D. Ghosh, and T. Ganz. 2002. The multifaceted Paneth cell. Cell. Mol. Life Sci. 59:156.
4. Neutra, M. R., N. J. Mantis, and J. P. Kraehenbuhl. 2001. Collaboration of epithelial cells with organized mucosal lymphoid tissues. Nat. Immunol. 2:1004.
5. Surawicz, C. M., R. C. Haggitt, M. Husseman, and L. V. McFarland. 1994. Mucosal biopsy diagnosis of colitis: acute self-limited colitis and idiopathic inflammatory bowel disease. Gastroenterology 107:755.
6. Hershberg, R. M. 2002. The epithelial cell cytoskeleton and intracellular trafficking. V. Polarized compartmentalization of antigen processing and Toll-like receptor signaling in intestinal epithelial cells. Am. J. Physiol. 283:G833.
7. Gewirtz, A. T. 2003. Intestinal epithelial Toll-like receptors: to protect. And serve? Curr. Pharm. Des. 9:1.
8. Abreu, M. T. 2003. Immunologic regulation of Toll-like receptors in gut epithelium. Curr. Opin. Gastroenterol. 19:559.
9. Takeda, K., T. Kaisho, and S. Akira. 2003. Toll-like receptors. Annu. Rev. Immunol. 21:335.
10. Suzuki, M., T. Hisamatsu, and D. K. Podolsky. 2003. γ-Interferon augments the intracellular pathway for lipopolysaccharide (LPS) recognition in human intestinal epithelial cells through coordinated up-regulation of LPS uptake and expression of the intracellular Toll-like receptor 4-MD-2 complex. Infect. Immun. 71:3503.
11. Wang, Q., R. Dziarski, C. J. Kirschning, M. Muzio, and D. Gupta. 2001. Micrococci and peptidoglycan activate TLR2→MyD88→IRAK→TRAF→ NIK→IKK→ NF-κB signal transduction pathway that induces transcription of interleukin-8. Infect. Immun. 69:2270.
12. + fibroblasts primed with γ-interferon increase production of interleukin-8 in response to lipopolysaccharide through up-regulation of membrane CD14 and MyD88 mRNA expression. Infect. Immun. 70:1272.
13. Yang, H., D. W. Young, F. Gusovsky, and J. C. Chow. 2000. Cellular events mediated by lipopolysaccharide-stimulated Toll-like receptor 4: MD-2 is required for activation of mitogen-activated protein kinases and Elk-1. J. Biol. Chem. 275:20861.
14. Abreu, M. T., P. Vora, E. Faure, L. S. Thomas, E. T. Arnold, and M. Arditi. 2001. Decreased expression of Toll-like receptor-4 and MD-2 correlates with intestinal epithelial cell protection against dysregulated proinflammatory gene expression in response to bacterial lipopolysaccharide. J. Immunol. 167:1609.
15. Melmed, G., L. S. Thomas, N. Lee, S. Y. Tesfay, K. Lukasek, K. S. Michelsen, Y. Zhou, B. Hu, M. Arditi, and M. T. Abreu. 2003. Human intestinal epithelial cells are broadly unresponsive to Toll-like receptor 2-dependent bacterial ligands: implications for host-microbial interactions in the gut. J. Immunol. 170:1406.
16. Abreu, M. T., E. T. Arnold, L. S. Thomas, R. Gonsky, Y. Zhou, B. Hu, and M. Arditi. 2002. TLR4 and MD-2 expression is regulated by immune-mediated signals in human intestinal epithelial cells. J. Biol. Chem. 277:20431.
17. Cario, E., and D. K. Podolsky. 2000. Differential alteration in intestinal epithelial cell expression of Toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect. Immun. 68:7010.
18. Ganz, T. 2003. Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 3:710.
19. Yang, D., O. Chertov, S. N. Bykovskaia, Q. Chen, M. J. Buffo, J. Shogan, M. Anderson, J. M. Schroder, J. M. Wang, O. M. Howard, and J. J. Oppenheim. 1999. β-Defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 286:525.
20. Wehkamp, J., B. Schwind, K. R. Herrlinger, S. Baxmann, K. Schmidt, M. Duchrow, C. Wohlschlager, A. C. Feller, E. F. Stange, and K. Fellermann. 2002. Innate immunity and colonic inflammation: enhanced expression of epithelial α-defensins. Dig. Dis. Sci. 47:1349.
21. Fahlgren, A., S. Hammarstrom, A. Danielsson, and M. L. Hammarstrom. 2003. Increased expression of antimicrobial peptides and lysozyme in colonic epithelial cells of patients with ulcerative colitis. Clin. Exp. Immunol. 131:90.
22. Lawrance, I. C., C. Fiocchi, and S. Chakravarti. 2001. Ulcerative colitis and Crohn's disease: distinctive gene expression profiles and novel susceptibility candidate genes. Hum. Mol. Gen. 10:445.
23. Cunliffe, R. N., F. R. Rose, J. Keyte, L. Abberley, W. C. Chan, and Y. R. Mahida. 2001. Human defensin 5 is stored in precursor form in normal Paneth cells and is expressed by some villous epithelial cells and by metaplastic Paneth cells in the colon in inflammatory bowel disease. Gut 48:176.
24. O'Neil, D. A., E. M. Porter, D. Elewaut, G. M. Anderson, L. Eckmann, T. Ganz, and M. F. Kagnoff. 1999. Expression and regulation of the human β-defensins hBD-1 and hBD-2 in intestinal epithelium. J. Immunol. 163:6718.
25. Frye, M., J. Bargon, B. Lembcke, T. O. Wagner, and R. Gropp. 2000. Differential expression of human α- and β-defensins mRNA in gastrointestinal epithelia. Eur. J. Clin. Invest. 30:695.
26. Takahashi, A., A. Wada, K. Ogushi, K. Maeda, T. Kawahara, K. Mawatari, H. Kurazono, J. Moss, T. Hirayama, and Y. Nakaya. 2001. Production of β-defensin-2 by human colonic epithelial cells induced by Salmonella enteritidis flagella filament structural protein. FEBS Lett. 508:484.
27. Krisanaprakornkit, S., J. R. Kimball, A. Weinberg, R. P. Darveau, B. W. Bainbridge, and B. A. Dale. 2000. Inducible expression of human β-defensin 2 by Fusobacterium nucleatum in oral epithelial cells: multiple signaling pathways and role of commensal bacteria in innate immunity and the epithelial barrier. Infect. Immun. 68:2907.
28. Wehkamp, J., K. Fellermann, K. R. Herrlinger, S. Baxmann, K. Schmidt, B. Schwind, M. Duchrow, C. Wohlschlager, A. C. Feller, and E. F. Stange. 2002. Human β-defensin 2 but not β-defensin 1 is expressed preferentially in colonic mucosa of inflammatory bowel disease. Eur. J. Gastroenterol. Hepatol. 14:745.
29. Ogushi, K., A. Wada, T. Niidome, N. Mori, K. Oishi, T. Nagatake, A. Takahashi, H. Asakura, S. Makino, H. Hojo, et al. 2001. Salmonella enteritidis FliC (flagella filament protein) induces human β-defensin-2 mRNA production by Caco-2 cells. J. Biol. Chem. 276:30521.
30. Becker, M. N., G. Diamond, M. W. Verghese, and S. H. Randell. 2000. CD14-dependent lipopolysaccharide-induced β-defensin-2 expression in human tracheobronchial epithelium. J. Biol. Chem. 275:29731.
31. Birchler, T., R. Seibl, K. Buchner, S. Loeliger, R. Seger, J. P. Hossle, A. Aguzzi, and R. P. Lauener. 2001. Human Toll-like receptor 2 mediates induction of the antimicrobial peptide human β-defensin 2 in response to bacterial lipoprotein. Eur. J. Immunol. 31:3131.
32. Wang, X., Z. Zhang, J. P. Louboutin, C. Moser, D. J. Weiner, and J. M. Wilson. 2003. Airway epithelia regulate expression of human β-defensin 2 through Toll-like receptor 2. FASEB J. 17:1727.
33. Kawai, K., H. Shimura, M. Minagawa, A. Ito, K. Tomiyama, and M. Ito. 2002. Expression of functional Toll-like receptor 2 on human epidermal keratinocytes. J. Dematol. Sci. 30:185.
34. Hertz, C. J., Q. Wu, E. M. Porter, Y. J. Zhang, K. H. Weismuller, P. J. Godowski, T. Ganz, S. H. Randell, and R. L. Modlin. 2003. Activation of Toll-like receptor 2 on human tracheobronchial epithelial cells induces the antimicrobial peptide human β-defensin-2. J. Immunol. 171:6820.
35. Abreu, M. T., A. A. Palladino, E. T. Arnold, R. S. Kwon, and J. A. McRoberts. 2000. Modulation of barrier function during Fas-mediated apoptosis in human intestinal epithelial cells. Gastroenterology 119:1524.
36. Dharmsathaphorn, K., J. A. McRoberts, K. G. Mandel, L. D. Tisdale, and H. Masui. 1984. A human colonic tumor cell line that maintains vectorial electrolyte transport. Am. J. Physiol. 246:G204.
37. Ades, E. W., F. J. Candal, R. A. Swerlick, V. G. George, S. Summers, D. C. Bosse, and T. J. Lawley. 1992. HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J. Invest. Dermatol. 99:683.
38. Zhang, F. X., C. J. Kirschning, R. Mancinelli, X. P. Xu, Y. Jin, E. Faure, A. Mantovani, M. Rothe, M. Muzio, and M. Arditi. 1999. Bacterial lipopolysaccharide activates nuclear factor-κB through interleukin-1 signaling mediators in cultured human dermal endothelial cells and mononuclear phagocytes. J. Biol. Chem. 274:7611.
39. Faure, E., O. Equils, P. A. Sieling, L. Thomas, F. X. Zhang, C. J. Kirschning, N. Polentarutti, M. Muzio, and M. Arditi. 2000. Bacterial lipopolysaccharide activates NF-κB through Toll-like receptor 4 (TLR-4) in cultured human dermal endothelial cells: differential expression of TLR-4 and TLR-2 in endothelial cells. J. Biol. Chem. 275:11058.
40. McIntire, F., H. Sievert, G. Barlow, R. Finley, and A. Lee. 1967. Chemical, physical, biological properties of a lipopolysaccharide from Escherichia coli K-235. Biochemistry. 6:2363.
41. Takeuchi, O., K. Hoshino, and S. Akira. 2000. Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J Immunol. 165:5392.
42. Ozinsky, A., K. D. Smith, D. Hume, and D. M. Underhill. 2000. Co-operative induction of pro-inflammatory signaling by Toll-like receptors. J. Endotoxin Res. 6:393.
43. Hajjar, A. M., D. S. O'Mahony, A. Ozinsky, D. M. Underhill, A. Aderem, S. J. Klebanoff, and C. B. Wilson. 2001. Cutting edge: functional interactions between Toll-like receptor (TLR) 2 and TLR1 or TLR6 in response to phenol-soluble modulin. J. Immunol. 166:15.
44. Means, T. K., S. Wang, E. Lien, A. Yoshimura, D. T. Golenbock, and M. J. Fenton. 1999. Human Toll-like receptors mediate cellular activation by Mycobacterium tuberculosis. J. Immunol. 163:3920.
45. Mori, N., Y. Yamada, S. Ikeda, Y. Yamasaki, K. Tsukasaki, Y. Tanaka, M. Tomonaga, N. Yamamoto, and M. Fujii. 2002. Bay 11-7082 inhibits transcription factor NF-κB and induces apoptosis of HTLV-I-infected T-cell lines and primary adult T-cell leukemia cells. Blood 100:1828.
46. Scaife, C. L., J. Kuang, J. C. Wills, D. B. Trowbridge, P. Gray, B. M. Manning, E. J. Eichwald, R. A. Daynes, and S. K. Kuwada. 2002. Nuclear factor κB inhibitors induce adhesion-dependent colon cancer apoptosis: implications for metastasis. Cancer Res. 62:6870.
47. Bogoyevitch, M. A., I. Boehm, A. Oakley, A. J. Ketterman, and R. K. Barr. 2004. Targeting the JNK MAPK cascade for inhibition: basic science and therapeutic potential. Biochim. Biophys. Acta 1697:89.
48. Wada, A., K. Ogushi, T. Kimura, H. Hojo, N. Mon, S. Suzuki, A. Kumatori, M. Se, Y. Nakahara, M. Nakamura, et al. 2001. Helicobacter pylori-mediated transcriptional regulation of the human β-defensin 2 gene requires NF-κB. Cell. Microbiol. 3:115.
49. Ogushi, K., A. Wada, T. Niidome, T. Okuda, R. Llanes, M. Nakayama, Y. Nishi, H. Kurazono, K. D. Smith, A. Aderem, et al. 2004. Gangliosides act as coreceptors for Salmonella enteritidis FliC and promote FliC induction of human β-defensin-2 expression in Caco-2 cells. J. Biol. Chem. 279:12213.
50. Cario, E., I. M. Rosenberg, S. L. Brandwein, P. L. Beck, H. C. Reinecker, and D. K. Podolsky. 2000. Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing-Toll-like receptors. J. Immunol. 164:966.
51. Yang, D., A. Biragyn, L. W. Kwak, and J. J. Oppenheim. 2002. Mammalian defensins in immunity: more than just microbicidal. Trends Immunol. 23:291.
52. Biragyn, A., P. A. Ruffini, C. A. Leiter, E. Klyushnenkova, A. Shakhov, O. Chertov, A. K. Shirakawa, J. M. Farber, D. M. Segal, J. J. Oppenheim, and L. W. Kwak. 2002. Toll-like receptor 4-dependent activation of dendritic cells by β-defensin 2. Science 298:1025.
53. Hommes, D., B. van den Blink, T. Plasse, J. Bartelsman, C. Xu, B. Macpherson, G. Tytgat, M. Peppelenbosch, and S. Van Deventer. 2002. Inhibition of stress-activated MAP kinases induces clinical improvement in moderate to severe Crohn's disease. Gastroenterology 122:7.
54. Ogura, Y., D. K. Bonen, N. Inohara, D. L. Nicolae, F. F. Chen, R. Ramos, H. Britton, T. Moran, R. Karaliuskas, R. H. Duerr, et al. 2001. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411:603.
55. Hugot, J. P., M. Chamaillard, H. Zouali, S. Lesage, J. P. Cezard, J. Belaiche, S. Almer, C. Tysk, C. A. O'Morain, M. Gassull, et al. 2001. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411:599.
56. Chamaillard, M., D. Philpott, S. E. Girardin, H. Zouali, S. Lesage, F. Chareyre, T. H. Bui, M. Giovannini, U. Zaehringer, V. Penard-Lacronique, et al. 2003. Gene-environment interaction modulated by allelic heterogeneity in inflammatory diseases. Proc. Natl. Acad. Sci. U.S.A. 100:3455.
57. Girardin, S. E., I. G. Boneca, J. Viala, M. Chamaillard, A. Labigne, G. Thomas, D. J. Philpott, and P. J. Sansonetti. 2003. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem. 278:8869.
58. Lala, S., Y. Ogura, C. Osborne, S. Y. Hor, A. Bromfield, S. Davies, O. Ogunbiyi, G. Nunez, and S. Keshav. 2003. Crohn's disease and the NOD2 gene: a role for Paneth cells. Gastroenterology 125:47.
59. Hisamatsu, T., M. Suzuki, H. C. Reinecker, W. J. Nadeau, B. A. McCormick, and D. K. Podolsky. 2003. CARD15/NOD2 functions as an antibacterial factor in human intestinal epithelial cells. Gastroenterology 124:993.
60. Fellermann, K., J. Wehkamp, K. R. Herrlinger, and E. F. Stange. 2003. Crohn's disease: a defensin deficiency syndrome? Eur. J. Gastroenterol. Hepatol. 15:627.