Serine lipids of porphyromonas gingivalis are human and mouse toll-like receptor 2 ligands

Infection and Immunity

Volumn 81, Issue 9, 2013, Pages 3479-3489

  Clark, Robert B ^a   Cervantes, Jorge L ^a   Maciejewski, Mark W ^b   Farrokhi, Vahid ^c   Nemati, Reza ^c   Yao, Xudong ^c   Anstadt, Emily ^a   Fujiwara, Mai ^a   Wright, Kyle T ^a   Riddle, Caroline ^a   La Vake, Carson J ^a   Salazar, Juan C ^a   Finegold, Sydney ^d   Nichols, Frank C ^e  

^a UNIVERSITY OF CONNECTICUT SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^c UNIVERSITY OF CONNECTICUT   (United States)

^d VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^e UNIVERSITY OF CONNECTICUT SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; LIPID; MONOCYTE CHEMOTACTIC PROTEIN 1; SERINE; TOLL LIKE RECEPTOR 2;

ANIMAL EXPERIMENT; ARTICLE; BIOLOGICAL ACTIVITY; CELL ASSAY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROCEDURES; PROTEIN BLOOD LEVEL; TANDEM MASS SPECTROMETRY;

EID: 84884267998     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00803-13     Document Type: Article

References (53)

1. Medzhitov R. 2001. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1:135-145.
2. Medzhitov R, Preston-Hurlburt P, Janeway CA, Jr. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388:394-397.
3. Zahringer U, Lindner B, Inamura S, Heine H, Alexander C. 2008. TLR2: promiscuous or specific? A critical re-evaluation of a receptor expressing apparent broad specificity. Immunobiology 213:205-224.
4. Hashimoto M, Asai Y, Ogawa T. 2004. Separation and structural analysis of lipoprotein in a lipopolysaccharide preparation from Porphyromonas gingivalis. Int. Immunol. 16:1431-1437.
5. Bainbridge BW, Coats SR, Darveau RP. 2002. Porphyromonas gingivalis lipopolysaccharide displays functionally diverse interactions with the innate host defense system. Ann. Periodontol. 7:29-37.
6. 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.
7. Triantafilou M, Gamper FG, Lepper PM, Mouratis MA, Schumann C, Harokopakis E, Schifferle RE, Hajishengallis G, Triantafilou K. 2007. Lipopolysaccharides from atherosclerosis-associated bacteria antagonize TLR4, induce formation of TLR2/1/CD36 complexes in lipid rafts and trigger TLR2-induced inflammatory responses in human vascular endothelial cells. Cell, Microbiol. 9:2030-2039.
8. Davey M, Liu X, Ukai T, Jain V, Gudino C, Gibson FC, III, Golenbock D, Visintin A, Genco CA. 2008. Bacterial fimbriae stimulate proinflammatory activation in the endothelium through distinct TLRs. J. Immunol. 180:2187-2195.
9. Hajishengallis G, Tapping RI, Harokopakis E, Nishiyama S, Ratti P, Schifferle RE, Lyle EA, Triantafilou M, Triantafilou K, Yoshimura F. 2006. Differential interactions of fimbriae and lipopolysaccharide from Porphyromonas gingivalis with the Toll-like receptor 2-centred pattern recognition apparatus. Cell, Microbiol. 8:1557-1570.
10. Ogawa T, Asai Y, Hashimoto M, Uchida H. 2002. Bacterial fimbriae activate human peripheral blood monocytes utilizing TLR2, CD14 and CD11a/CD18 as cellular receptors. Eur. J. Immunol. 32:2543-2550.
11. Jain S, Coats SR, Chang AM, Darveau RP. 2013. A novel class of lipoprotein lipase-sensitive molecules mediates Toll-like receptor 2 activation by Porphyromonas gingivalis. Infect. Immun. 81:1277-1286.
12. Nichols FC, Bajrami B, Clark RB, Housley W, Yao X. 2012. Free lipid A isolated from Porphyromonas gingivalis lipopolysaccharide is contaminated with phosphorylated dihydroceramide lipids: recovery in diseased dental samples. Infect. Immun. 80:860-874.
13. Nichols FC, Housley WJ, O'Conor CA, Manning T, Wu S, Clark RB. 2009. Unique lipids from a common human bacterium represent a new class of Toll-like receptor 2 ligands capable of enhancing autoimmunity. Am. J. Pathol. 175:2430-2438.
14. Wang YH, Jiang J, Zhu Q, Alanezi AZ, Clark RB, Jiang X, Rowe DW, Nichols FC. 2010. Porphyromonas gingivalis lipids inhibit osteoblastic differentiation and function. Infect. Immun. 78:3726-3735.
15. Gibson FC, III, Genco CA. 2007. Porphyromonas gingivalis mediated periodontal disease and atherosclerosis: disparate diseases with commonalities in pathogenesis through TLRs. Curr. Pharm. Des. 13:3665-3675.
16. Ukai T, Yumoto H, Gibson FC, III, Genco CA. 2008. Macrophageelicited osteoclastogenesis in response to bacterial stimulation requires Toll-like receptor 2-dependent tumor necrosis factor-alpha production. Infect. Immun. 76:812-819.
17. Papadopoulos G, Weinberg EO, Massari P, Gibson FC, III, Wetzler LM, Morgan EF, Genco CA. 2013. Macrophage-specific TLR2 signaling mediates pathogen-induced TNF-dependent inflammatory oral bone loss. J. Immunol. 190:1148-1157.
18. Aoki Y, Tabeta K, Murakami Y, Yoshimura F, Yamazaki K. 2010. Analysis of immunostimulatory activity of Porphyromonas gingivalis fimbriae conferred by Toll-like receptor 2. Biochem. Biophys. Res. Commun. 398:86-91.
19. Nichols FC, Riep B, Mun J, Morton MD, Bojarski MT, Dewhirst FE, Smith MB. 2004. Structures and biological activity of phosphorylated dihydroceramides of Porphyromonas gingivalis. J. Lipid Res. 45:2317-2330.
20. Aliprantis AO, Yang RB, Mark MR, Suggett S, Devaux B, Radolf JD, Klimpel GR, Godowski P, Zychlinsky A. 1999. Cell activation and apoptosis by bacterial lipoproteins through toll-like receptor-2. Science 285:736-739.
21. Nichols FC. 1994. Distribution of 3-hydroxy iC17:0 in subgingival plaque and gingival tissue samples: relationship to adult periodontitis. Infect. Immun. 62:3753-3760.
22. Chiou SH, Wang KT. 1989. Peptide and protein hydrolysis by microwave irradiation. J. Chromatogr. 491:424-431.
23. Fuchs SA, De Sain-van der Velden MG, de Barse MM, Roeleveld MW, Hendriks M, Dorland L, Klomp LW, Berger R, de Koning TJ. 2008. Two mass-spectrometric techniques for quantifying serine enantiomers and glycine in cerebrospinal fluid: potential confounders and age-dependent ranges. Clin. Chem. 54:1443-1450.
24. 13C 1D spectrum of straight baseline free of hump, dip and roll. Magn. Reson. Chem. 46:432-435.
25. Fulton DB, Hrabal R, Ni F. 1996. Gradient-enhanced TOCSY experiments with improved sensitivity and solvent suppression. J. Biomol. NMR 8:213-218.
26. Piantini U, Sorenson OW, Ernst RR. 1982. Multiple quantum filters for elucidating NMR coupling networks. J. Am. Chem. Soc. 104:6800-6801.
27. Bodenhausen G, Ruben DJ. 1980. Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy. Chem. Phys. Lett. 69:185-189.
28. Bax A, Summers M. 1986. 1H and 13C assignments form sensitivityenhanced detection of heteronuclear multiple-bond connectivity by 2D multiple quantum NMR. J. Am. Chem. Soc. 108:2093-2094.
29. Nyberg NT, Duus JO, Sorenson OW. 2005. Heteronuclear two-bond correlation: suppressing heteronuclear three-bond or higher NMR correlations while enhancing two-bond correlations even for vanishing 2J(CH). J. Am. Chem. Soc. 127:6154-6155.
30. Takeuchi O, Hoshino K, Kawai T, Sanjo H, Takada H, Ogawa T, Takeda K, Akira S. 1999. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 11:443-451.
31. Yi EC, Hackett M. 2000. Rapid isolation method for lipopolysaccharide and lipid A from gram-negative bacteria. Analyst 125:651-656.
32. Nichols FC, Yao X, Bajrami B, Downes J, Finegold SM, Knee E, Gallagher JJ, Housley WJ, Clark RB. 2011. Phosphorylated dihydroceramides from common human bacteria are recovered in human tissues. PLoS One 6(2):e16771. doi:10.1371/journal.pone.0016771.
33. Kawai Y, Yano I, Kaneda K. 1988. Various kinds of lipoamino acids including a novel serine-containing lipid in an opportunistic pathogen Flavobacterium. Their structures and biological activities on erythrocytes. Eur. J. Biochem. 171:73-80.
34. Shiozaki M, Degucki N, Mochizuki T, Wakabayashi T, Ishikawa T, Haruyama H, Kawai Y, Nishijima M. 1998. Revised structure of flavolipin and synthesis of its isomers. Tetrahedron Lett. 39:4497-4500.
35. Gomi K, Kawasaki K, Kawai Y, Shiozaki M, Nishijima M. 2002. Toll-like receptor 4-MD-2 complex mediates the signal transduction induced by flavolipin, an amino acid-containing lipid unique to Flavobacterium meningosepticum. J. Immunol. 168:2939-2943.
36. Kawasaki K, Gomi K, Kawai Y, Shiozaki M, Nishijima M. 2003. Molecular basis for lipopolysaccharide mimetic action of Taxol and flavolipin. J. Endotoxin Res. 9:301-307.
37. Nichols FC, Riep B, Mun J, Morton MD, Kawai T, Dewhirst FE, Smith MB. 2006. Structures and biological activities of novel phosphatidylethanolamine lipids of Porphyromonas gingivalis. J. Lipid Res. 47:844-853.
38. Garrison SW, Holt SC, Nichols FC. 1988. Lipopolysaccharidestimulated PGE2 release from human monocytes. Comparison of lipopolysaccharides prepared from suspected periodontal pathogens. J. Periodontol. 59:684-687.
39. Shi C, Jia T, Mendez-Ferrer S, Hohl TM, Serbina NV, Lipuma L, Leiner I, Li MO, Frenette PS, Pamer EG. 2011. Bone marrow mesenchymal stem and progenitor cells induce monocyte emigration in response to circulating toll-like receptor ligands. Immunity 34:590-601.
40. Fife BT, Huffnagle GB, Kuziel WA, Karpus WJ. 2000. CC chemokine receptor 2 is critical for induction of experimental autoimmune encephalomyelitis. J. Exp. Med. 192:899-905.
41. Izikson L, Klein RS, Charo IF, Weiner HL, Luster AD. 2000. Resistance to experimental autoimmune encephalomyelitis in mice lacking the CC chemokine receptor (CCR)2. J. Exp. Med. 192:1075-1080.
42. Simpson J, Rezaie P, Newcombe J, Cuzner ML, Male D, Woodroofe MN. 2000. Expression of the beta-chemokine receptors CCR2, CCR3 and CCR5 in multiple sclerosis central nervous system tissue. J. Neuroimmunol. 108:192-200.
43. Sorensen TL, RansohoffRM, Strieter RM, Sellebjerg F. 2004. Chemokine CCL2 and chemokine receptor CCR2 in early active multiple sclerosis. Eur. J. Neurol. 11:445-449.
44. Shiori T, Terao Y, Irako N, Aoyama T. 1998. Synthesis of topostins B567 and D654 (WB-3559D, flavolipin), DNAtoposimerase I inhibitors of bacterial origin. Tetrahedron 54:15701-15710.
45. Cann-Moisan C, CaroffJ, Girin E. 1988. Determination of flavin adenine dinucleotide in biological tissues by high-performance liquid chromatography with electrochemical detection. J. Chromatogr. 442:441-443.
46. Darveau RP, Pham TT, Lemley K, Reife RA, Bainbridge BW, Coats SR, Howald WN, Way SS, Hajjar AM. 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.
47. Bligh EG, Dyer WJ. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911-917.
48. Garbus J, DeLuca HF, Loomas ME, Strong FM. 1963. The rapid incorporation of phosphate into mitochondrial lipids. J. Biol. Chem. 238:59-63.
49. Makimura Y, Asai Y, Taiji Y, Sugiyama A, Tamai R, Ogawa T. 2006. Correlation between chemical structure and biological activities of Porphyromonas gingivalis synthetic lipopeptide derivatives. Clin. Exp. Immunol. 146:159-168.
50. Gibson FC, III, Hong C, Chou HH, Yumoto H, Chen J, Lien E, Wong J, Genco CA. 2004. Innate immune recognition of invasive bacteria accelerates atherosclerosis in apolipoprotein E-deficient mice. Circulation 109:2801-2806.
51. Nichols FC, Rojanasomsith K. 2006. Porphyromonas gingivalis lipids and diseased dental tissues. Oral Microbiol. Immunol. 21:84-92.
52. Gibson FC, III, Ukai T, Genco CA. 2008. Engagement of specific innate immune signaling pathways during Porphyromonas gingivalis induced chronic inflammation and atherosclerosis. Front. Biosci. 13:2041-2059.
53. Liang S, Krauss JL, Domon H, McIntosh ML, Hosur KB, Qu H, Li F, Tzekou A, Lambris JD, Hajishengallis G. 2011. The C5a receptor impairs IL-12-dependent clearance of Porphyromonas gingivalis and is required for induction of periodontal bone loss. J. Immunol. 186:869-877.