Differential and coordinated expression of defensins and cytokines by gingival epithelial cells and dendritic cells in response to oral bacteria

BMC Immunology

Volumn 11, Issue , 2010, Pages

  Yin, Lei ^a   Chino, Takahiro ^a   Horst, Orapin V ^a   Hacker, Beth M ^a   Clark, Edward A ^b   Dale, Beverly A ^a,b   Chung, Whasun O ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA DEFENSIN; BETA DEFENSIN 1; BETA DEFENSIN 2; BETA DEFENSIN 3; CXCL2 CHEMOKINE; CYTOKINE; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; BIOLOGICAL MARKER; CHEMOKINE;

ACTINOMYCES NAESLUNDII; ARTICLE; BACTERIAL CELL WALL; BACTERIAL VIRULENCE; CELL TYPE; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; EPITHELIUM CELL; FUSOBACTERIUM NUCLEATUM; GINGIVAL EPITHELIAL CELL; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; MOUTH CAVITY; MOUTH FLORA; PORPHYROMONAS GINGIVALIS; PROTEIN EXPRESSION; STIMULATION; UPREGULATION; BACTERIUM; BIOLOGICAL MODEL; CELL CULTURE; CULTURE MEDIUM; CYTOLOGY; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GINGIVA; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY;

BACTERIA; BETA-DEFENSINS; BIOLOGICAL MARKERS; CELLS, CULTURED; CHEMOKINES; CULTURE MEDIA, CONDITIONED; CYTOKINES; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GINGIVA; HUMANS; IMMUNITY, INNATE; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; LIPOPOLYSACCHARIDES; MODELS, IMMUNOLOGICAL;

EID: 77954328580     PISSN: None     EISSN: 14712172     Source Type: Journal    
DOI: 10.1186/1471-2172-11-37     Document Type: Article

References (51)

1. Muller CA, Autenrieth IB, Peschel A. Innate defenses of the intestinal epithelial barrier. Cell Mol Life Sci 2005, 62:1297-307. 10.1007/s00018-005-5034-2, 15971105.
2. Ganz T. Defensins: antimicrobial peptides of innate immunity. Nat Rev Immunol 2003, 3:710-20. 10.1038/nri1180, 12949495.
3. Braff MH, Bardan A, Nizet V, Gallo RL. Cutaneous defense mechanisms by antimicrobial peptides. J Invest Dermatol 2005, 125:9-13. 10.1111/j.0022-202X.2004.23587.x, 15982297.
4. Chung WO, Dommisch H, Yin L, Dale BA. Expression of defensins in gingiva and their role in periodontal health and disease. Curr Pharm Des 2007, 13:3073-83. 10.2174/138161207782110435, 17979750.
5. Devine DA. Antimicrobial peptides in defence of the oral and respiratory tracts. Mol Immunol 2003, 40:431-43. 10.1016/S0161-5890(03)00162-7, 14568389.
6. Dale BA, Fredericks LP. Antimicrobial peptides in the oral environment: expression and function in health and disease. Curr Issues Mol Biol 2005, 7:119-33. 1479858, 16053246.
7. Diamond G, Beckloff N, Ryan LK. Host defense peptides in the oral cavity and the lung: similarities and differences. J Dent Res 2008, 87:915-27. 10.1177/154405910808701011, 2730219, 18809744.
8. Nuding S, Zabel LT, Enders C, Porter E, Fellermann K, Wehkamp J, Mueller HA, Stange EF. Antibacterial activity of human defensins on anaerobic intestinal bacterial species: a major role of HBD-3. Microbes Infect 2009, 11:384-93. 10.1016/j.micinf.2009.01.001, 19397883.
9. Yang D, Chertov O, Bykovskaia SN, Chen Q, Buffo MJ, Shogan J, Anderson M, Schroder JM, Wang JM, Howard OM, et al. Beta-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 1999, 286:525-8. 10.1126/science.286.5439.525, 10521347.
10. Yang D, Biragyn A, Hoover DM, Lubkowski J, Oppenheim JJ. Multiple roles of antimicrobial defensins, cathelicidins, and eosinophil-derived neurotoxin in host defense. Annu Rev Immunol 2004, 22:181-215. 10.1146/annurev.immunol.22.012703.104603, 15032578.
11. Brogden KA, Heidari M, Sacco RE, Palmquist D, Guthmiller JM, Johnson GK, Jia HP, Tack BF, McCray PB. Defensin-induced adaptive immunity in mice and its potential in preventing periodontal disease. Oral Microbiol Immunol 2003, 18:95-9. 10.1034/j.1399-302X.2003.00047.x, 12654098.
12. Vongsa RA, Zimmerman NP, Dwinell MB. CCR6 regulation of the actin cytoskeleton orchestrates human beta defensin-2- and CCL20-mediated restitution of colonic epithelial cells. J Biol Chem 2009, 284:10034-45. 10.1074/jbc.M805289200, 2665058, 19233848.
13. Mathews M, Jia HP, Guthmiller JM, Losh G, Graham S, Johnson GK, Tack BF, McCray PB. Production of beta-defensin antimicrobial peptides by the oral mucosa and salivary glands. Infect Immun 1999, 67:2740-5. 96577, 10338476.
14. Krisanaprakornkit S, Kimball JR, Weinberg A, Darveau RP, Bainbridge BW, Dale BA. Inducible expression of human beta-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 2000, 68:2907-15. 10.1128/IAI.68.5.2907-2915.2000, 97503, 10768988.
15. Liu AY, Destoumieux D, Wong AV, Park CH, Valore EV, Liu L, Ganz T. Human beta-defensin-2 production in keratinocytes is regulated by interleukin-1, bacteria, and the state of differentiation. J Invest Dermatol 2002, 118:275-81. 10.1046/j.0022-202x.2001.01651.x, 11841544.
16. Krisanaprakornkit S, Kimball JR, Dale BA. Regulation of human beta-defensin-2 in gingival epithelial cells: the involvement of mitogen-activated protein kinase pathways, but not the NF-kappaB transcription factor family. J Immunol 2002, 168:316-24.
17. Chung WO, Dale BA. Innate immune response of oral and foreskin keratinocytes: utilization of different signaling pathways by various bacterial species. Infect Immun 2004, 72:352-8. 10.1128/IAI.72.1.352-358.2004, 343965, 14688115.
18. Chung WO, Hansen SR, Rao D, Dale BA. Protease-activated receptor signaling increases epithelial antimicrobial peptide expression. J Immunol 2004, 173:5165-70.
19. Chung WO, Dale BA. Differential utilization of nuclear factor-kappaB signaling pathways for gingival epithelial cell responses to oral commensal and pathogenic bacteria. Oral Microbiol Immunol 2008, 23:119-26. 10.1111/j.1399-302X.2007.00398.x, 2826319, 18279179.
20. Liu L, Roberts AA, Ganz T. By IL-1 signaling, monocyte-derived cells dramatically enhance the epidermal antimicrobial response to lipopolysaccharide. J Immunol 2003, 170:575-80.
21. Tsutsumi-Ishii Y, Nagaoka I. Modulation of human beta-defensin-2 transcription in pulmonary epithelial cells by lipopolysaccharide-stimulated mononuclear phagocytes via proinflammatory cytokine production. J Immunol 2003, 170:4226-36.
22. Zoumpopoulou G, Tsakalidou E, Dewulf J, Pot B, Grangette C. Differential crosstalk between epithelial cells, dendritic cells and bacteria in a co-culture model. Int J Food Microbiol 2009, 131:40-51. 10.1016/j.ijfoodmicro.2008.12.037, 19264370.
23. Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R, Granucci F, Kraehenbuhl JP, Ricciardi-Castagnoli P. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2001, 2:361-7. 10.1038/86373, 11276208.
24. Granucci F, Ricciardi-Castagnoli P. Interactions of bacterial pathogens with dendritic cells during invasion of mucosal surfaces. Curr Opin Microbiol 2003, 6:72-6. 10.1016/S1369-5274(03)00007-9, 12615223.
25. O'Mahony L, O'Callaghan L, McCarthy J, Shilling D, Scully P, Sibartie S, Kavanagh E, Kirwan WO, Redmond HP, Collins JK, et al. Differential cytokine response from dendritic cells to commensal and pathogenic bacteria in different lymphoid compartments in humans. Am J Physiol Gastrointest Liver Physiol 2005, 290:G839-G845. 10.1152/ajpgi.00112.2005, 16293657.
26. Jotwani R, Cutler CW. Multiple dendritic cell (DC) subpopulations in human gingiva and association of mature DCs with CD4+ T-cells in situ. J Dent Res 2003, 82:736-41. 10.1177/154405910308200915, 12939360.
27. Cutler CW, Jotwani R. Antigen-presentation and the role of dendritic cells in periodontitis. Periodontol 2000 2004, 35:135-57. 10.1111/j.0906-6713.2004.003560.x, 15107061.
28. Cutler CW, Teng YT. Oral mucosal dendritic cells and periodontitis: many sides of the same coin with new twists. Periodontol 2000 2007, 45:35-50. 10.1111/j.1600-0757.2007.00222.x, 2828688, 17850447.
29. Krisanaprakornkit S, Weinberg A, Perez CN, Dale BA. Expression of the peptide antibiotic human beta-defensin 1 in cultured gingival epithelial cells and gingival tissue. Infect Immun 1998, 66:4222-8. 108509, 9712771.
30. Giordano D, Magaletti DM, Clark EA, Beavo JA. Cyclic nucleotides promote monocyte differentiation toward a DC-SIGN+ (CD209) intermediate cell and impair differentiation into dendritic cells. J Immunol 2003, 171:6421-30.
31. Yin L, Dale BA. Activation of protective responses in oral epithelial cells by Fusobacterium nucleatum and human beta-defensin-2. J Med Microbiol 2007, 56:976-87. 10.1099/jmm.0.47198-0, 17577065.
32. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45. 10.1093/nar/29.9.e45, 55695, 11328886.
33. Chino T, Santer DM, Giordano D, Chen C, Li C, Chen CH, Darveau RP, Clark EA. Effects of oral commensal and pathogenic bacteria on human dendritic cells. Oral Microbiol Immunol 2009, 24:96-103. 2733846, 19239635.
34. Clark EA, Ledbetter JA. How B and T cells talk to each other. Nature 1994, 367:425-8. 10.1038/367425a0, 8107800.
35. Duits LA, Ravensbergen B, Rademaker M, Hiemstra PS, Nibbering PH. Expression of beta-defensin 1 and 2 mRNA by human monocytes, macrophages and dendritic cells. Immunology 2002, 106:517-25. 10.1046/j.1365-2567.2002.01430.x, 1782759, 12153515.
36. Funderburg N, Lederman MM, Feng Z, Drage MG, Jadlowsky J, Harding CV, Weinberg A, Sieg SF. Human-defensin-3 activates professional antigen-presenting cells via Toll-like receptors 1 and 2. Proc Natl Acad Sci USA 2007, 104:18631-5. 10.1073/pnas.0702130104, 2141828, 18006661.
37. Presicce P, Giannelli S, Taddeo A, Villa ML, Della Bella S. Human defensins activate monocyte-derived dendritic cells, promote the production of proinflammatory cytokines, and up-regulate the surface expression of CD91. J Leukoc Biol 2009, 86(4):941-948. 10.1189/jlb.0708412, 19477909.
38. Roberts FA, Darveau RP. Beneficial bacteria of the periodontium. Periodontol 2000 2002, 30:40-50. 10.1034/j.1600-0757.2002.03004.x, 12236894.
39. Tonetti MS, Imboden MA, Gerber L, Lang NP, Laissue J, Mueller C. Localized expression of mRNA for phagocyte-specific chemotactic cytokines in human periodontal infections. Infect Immun 1994, 62:4005-14. 303060, 8063420.
40. Darveau RP, Belton CM, Reife RA, Lamont RJ. Local chemokine paralysis, a novel pathogenic mechanism for Porphyromonas gingivalis. Infect Immun 1998, 66:1660-5. 108102, 9529095.
41. Lamont RJ, Jenkinson HF. Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol Mol Biol Rev 1998, 62:1244-63. 98945, 9841671.
42. Imai T, Nagira M, Takagi S, Kakizaki M, Nishimura M, Wang J, Gray PW, Matsushima K, Yoshie O. Selective recruitment of CCR4-bearing Th2 cells toward antigen-presenting cells by the CC chemokines thymus and activation-regulated chemokine and macrophage-derived chemokine. Int Immunol 1999, 11:81-8. 10.1093/intimm/11.1.81, 10050676.
43. Jotwani R, Pulendran B, Agrawal S, Cutler CW. Human dendritic cells respond to Porphyromonas gingivalis LPS by promoting a Th2 effector response in vitro. Eur J Immunol 2003, 33:2980-6. 10.1002/eji.200324392, 14579266.
44. Kusumoto Y, Hirano H, Saitoh K, Yamada S, Takedachi M, Nozaki T, Ozawa Y, Nakahira Y, Saho T, Ogo H, et al. Human gingival epithelial cells produce chemotactic factors interleukin-8 and monocyte chemoattractant protein-1 after stimulation with Porphyromonas gingivalis via toll-like receptor 2. J Periodontol 2004, 75:370-9. 10.1902/jop.2004.75.3.370, 15088874.
45. Boniotto M, Jordan WJ, Eskdale J, Tossi A, Antcheva N, Crovella S, Connell ND, Gallagher G. Human beta-defensin 2 induces a vigorous cytokine response in peripheral blood mononuclear cells. Antimicrob Agents Chemother 2006, 50:1433-41. 10.1128/AAC.50.4.1433-1441.2006, 1426918, 16569862.
46. Zhou L, Spolski R, Min R, Shenderov K, Egawa T, Levy DE, Leonard WJ, Littman DR. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol 2007, 8:967-74. 10.1038/ni1488, 17581537.
47. Yang D, Chen Q, Hoover DM, Staley P, Tucker KD, Lubkowski J, Oppenheim JJ. Many chemokines including CCL20/MIP-3alpha display antimicrobial activity. J Leukoc Biol 2003, 74:448-55. 10.1189/jlb.0103024, 12949249.
48. Goulvestre C, Batteux F, Charreire J. Chemokines modulate experimental autoimmune thyroiditis through attraction of autoreactive or regulatory T cells. Eur J Immunol 2002, 32:3435-42.
49. Biragyn A, Ruffini PA, Leifer CA, Klyushnenkova E, Shakhov A, Chertov O, Shirakawa AK, Farber JM, Segal DM, Oppenheim JJ, et al. Toll-like receptor 4-dependent activation of dendritic cells by beta-defensin 2. Science 2002, 298:1025-9. 10.1126/science.1075565, 12411706.
50. Rimoldi M, Chieppa M, Salucci V, Avogadri F, Sonzogni A, Sampietro GM, Nespoli A, Viale G, Allavena P, Rescigno M. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat Immunol 2005, 6:507-14. 10.1038/ni1192, 15821737.
51. Rimoldi M, Chieppa M, Larghi P, Vulcano M, Allavena P, Rescigno M. Monocyte-derived dendritic cells activated by bacteria or by bacteria-stimulated epithelial cells are functionally different. Blood 2005, 106:2818-26. 10.1182/blood-2004-11-4321, 16030185.