Tetra- and Penta-Acylated Lipid A Structures of Porphyromonas gingivalis LPS Differentially Activate TLR4-Mediated NF-κB Signal Transduction Cascade and Immuno-Inflammatory Response in Human Gingival Fibroblasts

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Herath, Thanuja D K ^a   Darveau, Richard P ^b   Seneviratne, Chaminda J ^a   Wang, Cun Yu ^c   Wang, Yu ^a   Jin, Lijian ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; LIPID A; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; TOLL LIKE RECEPTOR 4;

ARTICLE; CCL2 GENE; CONTROLLED STUDY; CXCL10 GENE; DOWN REGULATION; FIBROBLAST; G CSF GENE; GENE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR GENE; HUMAN; HUMAN CELL; IKBKB GENE; IMMUNE EVASION; IMMUNE RESPONSE; INNATE IMMUNITY; INTERLEUKIN 6 GENE; INTERLEUKIN 8 GENE; LIPID ANALYSIS; MAP2K4 GENE; MAPK8 GENE; NFKB1 GENE; NFKBIA GENE; NONHUMAN; PORPHYROMONAS GINGIVALIS; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UPREGULATION;

ACYLATION; CYTOKINES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLASTS; GINGIVA; HUMANS; LIPID A; MAP KINASE SIGNALING SYSTEM; NF-KAPPA B; PORPHYROMONAS GINGIVALIS; TOLL-LIKE RECEPTOR 4;

EID: 84874904949     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058496     Document Type: Article

References (78)

1. Pihlstrom BL, Michalowicz BS, Johnson NW, (2005) Periodontal diseases. Lancet 366: 1809-1820.
2. Socransky SS, Haffajee AD, (1992) The bacterial etiology of destructive periodontal disease: current concepts. J Periodontol 63: 322-331.
3. Darveau RP, (2010) Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol 8: 481-490.
4. Hajishengallis G, (2009) Porphyromonas gingivalis-host interactions: open war or intelligent guerilla tactics? Microbes Infect 11: 637-645.
5. Schwartz J, Stinson FL, Parker RB, (1972) The passage of tritiated bacterial endotoxin across intact gingival crevicular epithelium. J Periodontol 43: 270-276.
6. Curtis MA, Zenobia C, Darveau RP, (2011) The relationship of the oral microbiotia to periodontal health and disease. Cell Host Microbe 10: 302-306.
7. Beutler B, Rietschel ET, (2003) Innate immune sensing and its roots: the story of endotoxin. Nat Rev Immunol 3: 169-176.
8. Rietschel ET, Brade H, (1992) Bacterial endotoxins. Sci Am 267: 54-61.
9. Rietschel ET, Kirikae T, Schade FU, Mamat U, Schmidt G, et al. (1994) Bacterial endotoxin: molecular relationships of structure to activity and function. FASEB J 8: 217-225.
10. Dixon DR, Darveau RP, (2005) Lipopolysaccharide heterogeneity: innate host responses to bacterial modification of lipid a structure. J Dent Res 84: 584-595.
11. Grenier D, Mayrand D, (1987) Functional characterization of extracellular vesicles produced by Bacteroides gingivalis. Infect Immun 55: 111-117.
12. Uehara A, Takada H, (2007) Functional TLRs and NODs in human gingival fibroblasts. J Dent Res 86: 249-254.
13. Tamura M, Tokuda M, Nagaoka S, Takada H, (1992) Lipopolysaccharides of Bacteroides intermedius (Prevotella intermedia) and Bacteroides (Porphyromonas) gingivalis induce interleukin-8 gene expression in human gingival fibroblast cultures. Infect Immun 60: 4932-4937.
14. Tabeta K, Yamazaki K, Akashi S, Miyake K, Kumada H, et al. (2000) Toll-like receptors confer responsiveness to lipopolysaccharide from Porphyromonas gingivalis in human gingival fibroblasts. Infect Immun 68: 3731-3735.
15. Ara T, Kurata K, Hirai K, Uchihashi T, Uematsu T, et al. (2009) Human gingival fibroblasts are critical in sustaining inflammation in periodontal disease. J Periodontal Res 44: 21-27.
16. Kocgozlu L, Elkaim R, Tenenbaum H, Werner S, (2009) Variable cell responses to P. gingivalis lipopolysaccharide. J Dent Res 88: 741-745.
17. Diya Z, Lili C, Shenglai L, Zhiyuan G, Jie Y, (2008) Lipopolysaccharide (LPS) of Porphyromonas gingivalis induces IL-1beta, TNF-alpha and IL-6 production by THP-1 cells in a way different from that of Escherichia coli LPS. Innate Immun 14: 99-107.
18. Darveau RP, Belton CM, Reife RA, Lamont RJ, (1998) Local chemokine paralysis, a novel pathogenic mechanism for Porphyromonas gingivalis. Infect Immun 66: 1660-1665.
19. Reife RA, Shapiro RA, Bamber BA, Berry KK, Mick GE, et al. (1995) Porphyromonas gingivalis lipopolysaccharide is poorly recognized by molecular components of innate host defense in a mouse model of early inflammation. Infect Immun 63: 4686-4694.
20. Heumann D, Roger T, (2002) Initial responses to endotoxins and Gram-negative bacteria. Clin Chim Acta 323: 59-72.
21. Triantafilou M, Triantafilou K, (2002) Lipopolysaccharide recognition: CD14, TLRs and the LPS-activation cluster. Trends Immunol 23: 301-304.
22. Lee HK, Lee J, Tobias PS, (2002) Two lipoproteins extracted from Escherichia coli K-12 LCD25 lipopolysaccharide are the major components responsible for Toll-like receptor 2-mediated signaling. J Immunol 168: 4012-4017.
23. Hirschfeld M, Weis JJ, Toshchakov V, Salkowski CA, Cody MJ, et al. (2001) Signaling by toll-like receptor 2 and 4 agonists results in differential gene expression in murine macrophages. Infect Immun 69: 1477-1482.
24. Martin M, Katz J, Vogel SN, Michalek SM, (2001) Differential induction of endotoxin tolerance by lipopolysaccharides derived from Porphyromonas gingivalis and Escherichia coli. J Immunol 167: 5278-5285.
25. Hajishengallis G, Martin M, Schifferle RE, Genco RJ, (2002) Counteracting interactions between lipopolysaccharide molecules with differential activation of toll-like receptors. Infect Immun 70: 6658-6664.
26. Lu Q, Darveau RP, Samaranayake LP, Wang CY, Jin L, (2009) Differential modulation of human {beta}-defensins expression in human gingival epithelia by Porphyromonas gingivalis lipopolysaccharide with tetra- and penta-acylated lipid A structures. Innate Immun 15: 325-335.
27. Kumada H, Haishima Y, Umemoto T, Tanamoto K, (1995) Structural study on the free lipid A isolated from lipopolysaccharide of Porphyromonas gingivalis. J Bacteriol 177: 2098-2106.
28. Darveau RP, Pham TT, Lemley K, Reife RA, Bainbridge BW, et al. (2004) Porphyromonas gingivalis lipopolysaccharide contains multiple lipid A species that functionally interact with both toll-like receptors 2 and 4. Infect Immun 72: 5041-5051.
29. Darveau RP, Arbabi S, Garcia I, Bainbridge B, Maier RV, (2002) Porphyromonas gingivalis lipopolysaccharide is both agonist and antagonist for p38 mitogen-activated protein kinase activation. Infect Immun 70: 1867-1873.
30. Bainbridge BW, Darveau RP, (2001) Porphyromonas gingivalis lipopolysaccharide: an unusual pattern recognition receptor ligand for the innate host defense system. Acta Odontol Scand 59: 131-138.
31. Reife RA, Coats SR, Al-Qutub M, Dixon DM, Braham PA, et al. (2006) Porphyromonas gingivalis lipopolysaccharide lipid A heterogeneity: differential activities of tetra- and penta-acylated lipid A structures on E-selectin expression and TLR4 recognition. Cell Microbiol 8: 857-868.
32. Chen C, Coats SR, Bumgarner RE, Darveau RP, (2007) Hierarchical gene expression profiles of HUVEC stimulated by different lipid A structures obtained from Porphyromonas gingivalis and Escherichia coli. Cell Microbiol 9: 1028-1038.
33. Herath TD, Wang Y, Seneviratne CJ, Lu Q, Darveau RP, et al. (2011) Porphyromonas gingivalis lipopolysaccharide lipid A heterogeneity differentially modulates the expression of IL-6 and IL-8 in human gingival fibroblasts. J Clin Periodontol 38: 694-701.
34. Faria Morandini AC, Chaves Souza PP, Ramos-Junior ES, Brozoski DT, Sipert CR, et al. (2012) Toll-Like Receptor 2 Knockdown Modulates Interleukin (IL)-6 and IL-8 but not Stromal Derived Factor-1 (SDF-1/CXCL12) in Human Periodontal Ligament and Gingival Fibroblasts. J Periodontol.
35. Mahanonda R, Sa-Ard-Iam N, Montreekachon P, Pimkhaokham A, Yongvanichit K, et al. (2007) IL-8 and IDO expression by human gingival fibroblasts via TLRs. J Immunol 178: 1151-1157.
36. Hatakeyama J, Tamai R, Sugiyama A, Akashi S, Sugawara S, et al. (2003) Contrasting responses of human gingival and periodontal ligament fibroblasts to bacterial cell-surface components through the CD14/Toll-like receptor system. Oral Microbiol Immunol 18: 14-23.
37. Sugawara S, Sugiyama A, Nemoto E, Rikiishi H, Takada H, (1998) Heterogeneous expression and release of CD14 by human gingival fibroblasts: characterization and CD14-mediated interleukin-8 secretion in response to lipopolysaccharide. Infect Immun 66: 3043-3049.
38. Wang PL, Ohura K, (2002) Porphyromonas gingivalis lipopolysaccharide signaling in gingival fibroblasts-CD14 and Toll-like receptors. Crit Rev Oral Biol Med 13: 132-142.
39. Wang PL, Oido-Mori M, Fujii T, Kowashi Y, Kikuchi M, et al. (2001) Heterogeneous expression of Toll-like receptor 4 and downregulation of Toll-like receptor 4 expression on human gingival fibroblasts by Porphyromonas gingivalis lipopolysaccharide. Biochem Biophys Res Commun 288: 863-867.
40. Park BS, Song DH, Kim HM, Choi BS, Lee H, et al. (2009) The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458: 1191-1195.
41. Wang PL, Azuma Y, Shinohara M, Ohura K, (2000) Toll-like receptor 4-mediated signal pathway induced by Porphyromonas gingivalis lipopolysaccharide in human gingival fibroblasts. Biochem Biophys Res Commun 273: 1161-1167.
42. Ogawa T, Asai Y, Hashimoto M, Takeuchi O, Kurita T, et al. (2002) Cell activation by Porphyromonas gingivalis lipid A molecule through Toll-like receptor 4- and myeloid differentiation factor 88-dependent signaling pathway. Int Immunol 14: 1325-1332.
43. Berezow AB, Ernst RK, Coats SR, Braham PH, Karimi-Naser LM, et al. (2009) The structurally similar, penta-acylated lipopolysaccharides of Porphyromonas gingivalis and Bacteroides elicit strikingly different innate immune responses. Microb Pathog 47: 68-77.
44. Liu R, Desta T, Raptis M, Darveau RP, Graves DT, (2008) P. gingivalis and E. coli lipopolysaccharides exhibit different systemic but similar local induction of inflammatory markers. J Periodontol 79: 1241-1247.
45. Burns E, Eliyahu T, Uematsu S, Akira S, Nussbaum G, (2010) TLR2-dependent inflammatory response to Porphyromonas gingivalis is MyD88 independent, whereas MyD88 is required to clear infection. J Immunol 184: 1455-1462.
46. Gibson FC, 3rd, Genco CA (2007) Porphyromonas gingivalis mediated periodontal disease and atherosclerosis: disparate diseases with commonalities in pathogenesis through TLRs. Curr Pharm Des 13: 3665-3675.
47. Hajishengallis G, (2011) Immune evasion strategies of Porphyromonas gingivalis. J Oral Biosci 53: 233-240.
48. Baldwin AS Jr, (2001) Series introduction: the transcription factor NF-kappaB and human disease. J Clin Invest 107: 3-6.
49. Golenbock DT, Hampton RY, Qureshi N, Takayama K, Raetz CR, (1991) Lipid A-like molecules that antagonize the effects of endotoxins on human monocytes. J Biol Chem 266: 19490-19498.
50. Coats SR, Reife RA, Bainbridge BW, Pham TT, Darveau RP, (2003) Porphyromonas gingivalis lipopolysaccharide antagonizes Escherichia coli lipopolysaccharide at toll-like receptor 4 in human endothelial cells. Infect Immun 71: 6799-6807.
51. Nemoto E, Darveau RP, Foster BL, Nogueira-Filho GR, Somerman MJ, (2006) Regulation of cementoblast function by P. gingivalis lipopolysaccharide via TLR2. J Dent Res 85: 733-738.
52. Burns E, Bachrach G, Shapira L, Nussbaum G, (2006) Cutting Edge: TLR2 is required for the innate response to Porphyromonas gingivalis: activation leads to bacterial persistence and TLR2 deficiency attenuates induced alveolar bone resorption. J Immunol 177: 8296-8300.
53. Yamagishi VT, Torneck CD, Friedman S, Huang GT, Glogauer M, (2011) Blockade of TLR2 inhibits Porphyromonas gingivalis suppression of mineralized matrix formation by human dental pulp stem cells. J Endod 37: 812-818.
54. Erridge C, Pridmore A, Eley A, Stewart J, Poxton IR, (2004) Lipopolysaccharides of Bacteroides fragilis, Chlamydia trachomatis and Pseudomonas aeruginosa signal via toll-like receptor 2. J Med Microbiol 53: 735-740.
55. Erridge C, Spickett CM, Webb DJ, (2007) Non-enterobacterial endotoxins stimulate human coronary artery but not venous endothelial cell activation via Toll-like receptor 2. Cardiovasc Res 73: 181-189.
56. Coats SR, Jones JW, Do CT, Braham PH, Bainbridge BW, et al. (2009) Human Toll-like receptor 4 responses to P. gingivalis are regulated by lipid A 1- and 4′-phosphatase activities. Cell Microbiol 11: 1587-1599.
57. Rangarajan M, Aduse-Opoku J, Paramonov N, Hashim A, Bostanci N, et al. (2008) Identification of a second lipopolysaccharide in Porphyromonas gingivalis W50. J Bacteriol 190: 2920-2932.
58. Hayashi J, Masaka T, Saito I, Ishikawa I, (1996) Soluble CD14 mediates lipopolysaccharide-induced intercellular adhesion molecule 1 expression in cultured human gingival fibroblasts. Infect Immun 64: 4946-4951.
59. Ren L, Jiang ZQ, Fu Y, Leung WK, Jin L, (2009) The interplay of lipopolysaccharide-binding protein and cytokines in periodontal health and disease. J Clin Periodontol 36: 619-626.
60. Ren L, Leung WK, Loo TW, Jin L, (2005) Lipopolysaccharide-binding protein down-regulates the expression of interleukin-6 by human gingival fibroblast. J Periodontal Res 40: 407-416.
61. Miyake K, (2004) Innate recognition of lipopolysaccharide by Toll-like receptor 4-MD-2. Trends Microbiol 12: 186-192.
62. Bainbridge BW, Coats SR, Pham TT, Reife RA, Darveau RP, (2006) Expression of a Porphyromonas gingivalis lipid A palmitylacyltransferase in Escherichia coli yields a chimeric lipid A with altered ability to stimulate interleukin-8 secretion. Cell Microbiol 8: 120-129.
63. Coats SR, Berezow AB, To TT, Jain S, Bainbridge BW, et al. (2011) The lipid A phosphate position determines differential host Toll-like receptor 4 responses to phylogenetically related symbiotic and pathogenic bacteria. Infect Immun 79: 203-210.
64. Erridge C, Bennett-Guerrero E, Poxton IR, (2002) Structure and function of lipopolysaccharides. Microbes Infect 4: 837-851.
65. Seydel U, Schromm AB, Blunck R, Brandenburg K, (2000) Chemical structure, molecular conformation, and bioactivity of endotoxins. Chem Immunol 74: 5-24.
66. Schromm AB, Brandenburg K, Loppnow H, Moran AP, Koch MH, et al. (2000) Biological activities of lipopolysaccharides are determined by the shape of their lipid A portion. Eur J Biochem 267: 2008-2013.
67. Netea MG, van Deuren M, Kullberg BJ, Cavaillon JM, Van der Meer JW, (2002) Does the shape of lipid A determine the interaction of LPS with Toll-like receptors? Trends Immunol 23: 135-139.
68. Al-Qutub MN, Braham PH, Karimi-Naser LM, Liu X, Genco CA, et al. (2006) Hemin-dependent modulation of the lipid A structure of Porphyromonas gingivalis lipopolysaccharide. Infect Immun 74: 4474-4485.
69. Kawahara K, Tsukano H, Watanabe H, Lindner B, Matsuura M, (2002) Modification of the structure and activity of lipid A in Yersinia pestis lipopolysaccharide by growth temperature. Infect Immun 70: 4092-4098.
70. Hajjar AM, Ernst RK, Tsai JH, Wilson CB, Miller SI, (2002) Human Toll-like receptor 4 recognizes host-specific LPS modifications. Nat Immunol 3: 354-359.
71. Sawada N, Ogawa T, Asai Y, Makimura Y, Sugiyama A, (2007) Toll-like receptor 4-dependent recognition of structurally different forms of chemically synthesized lipid As of Porphyromonas gingivalis. Clin Exp Immunol 148: 529-536.
72. Kumada H, Haishima Y, Watanabe K, Hasegawa C, Tsuchiya T, et al. (2008) Biological properties of the native and synthetic lipid A of Porphyromonas gingivalis lipopolysaccharide. Oral Microbiol Immunol 23: 60-69.
73. Zhang Y, Gaekwad J, Wolfert MA, Boons GJ, (2008) Synthetic tetra-acylated derivatives of lipid A from Porphyromonas gingivalis are antagonists of human TLR4. Org Biomol Chem 6: 3371-3381.
74. Yi EC, Hackett M, (2000) Rapid isolation method for lipopolysaccharide and lipid A from gram-negative bacteria. Analyst 125: 651-656.
75. Caroff M, Tacken A, Szabo L, (1988) Detergent-accelerated hydrolysis of bacterial endotoxins and determination of the anomeric configuration of the glycosyl phosphate present in the "isolated lipid A" fragment of the Bordetella pertussis endotoxin. Carbohydr Res 175: 273-282.
76. Di Domenico G, Del Vecchio L, Postiglione L, Ramaglia L (2003) Immunophenotypic analysis of human gingival fibroblasts and its regulation by Granulocyte-Macrophage Colony-Stimulating Factor (GM-CSF). Minerva Stomatol 52: 81-87, 87-91.
77. Baluchamy S, Zhang Y, Ravichandran P, Ramesh V, Sodipe A, et al. (2010) Differential oxidative stress gene expression profile in mouse brain after proton exposure. In Vitro Cell Dev Biol Anim 46: 718-725.
78. Ardeshna KM, Pizzey AR, Devereux S, Khwaja A, (2000) The PI3 kinase, p38 SAP kinase, and NF-kappaB signal transduction pathways are involved in the survival and maturation of lipopolysaccharide-stimulated human monocyte-derived dendritic cells. Blood 96: 1039-1046.