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Pathogenic Microbes and Community Service Through Manipulation of Innate Immunity

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Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 946))

Abstract

The periodontal pathogen Porphyromonas gingivalis undermines major components of innate immunity, such as complement, Toll-like receptors (TLR), and their crosstalk pathways. At least in principle, these subversive activities could promote the adaptive fitness of the entire periodontal biofilm community. In this regard, the virulence factors responsible for complement and TLR exploitation (gingipain enzymes, atypical lipopolysaccharide molecules, and fimbriae) are released as components of readily diffusible membrane vesicles, which can thus become available to other biofilm organisms. This review summarizes important immune subversive tactics of P. gingivalis which might enable it to exert a supportive impact on the oral microbial community.

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References

  • Amano, A., Takeuchi, H. and Furuta, N. (2010) Outer membrane vesicles function as offensive weapons in host-parasite interactions. Microbes Infect. 12, 791-798

    Article  PubMed  CAS  Google Scholar 

  • Awano, S., Ansai, T., Takata, Y., Soh, I., Akifusa, S., Hamasaki, T., Yoshida, A., Sonoki, K., Fujisawa, K. and Takehara, T. (2008) Oral health and mortality risk from pneumonia in the elderly. J. Dent. Res. 87, 334-339

    Article  PubMed  CAS  Google Scholar 

  • Backhed, F., Ley, R.E., Sonnenburg, J.L., Peterson, D.A. and Gordon, J.I. (2005) Host-bacterial mutualism in the human intestine. Science 307, 1915-1920

    Article  PubMed  CAS  Google Scholar 

  • Beertsen, W., Willenborg, M., Everts, V., Zirogianni, A., Podschun, R., Schroder, B., Eskelinen, E.L. and Saftig, P. (2008) Impaired phagosomal maturation in neutrophils leads to periodontitis in lysosomal-associated membrane protein-2 knockout mice. J Immunol. 180, 475-482

    PubMed  CAS  Google Scholar 

  • Beutler, B., Jiang, Z., Georgel, P., Crozat, K., Croker, B., Rutschmann, S., Du, X. and Hoebe, K. (2006) Genetic analysis of host resistance: Toll-like receptor signaling and immunity at large. Annu. Rev. Immunol. 24, 353-389

    Article  PubMed  CAS  Google Scholar 

  • Coats, S.R., Jones, J.W., Do, C.T., Braham, P.H., Bainbridge, B.W., To, T.T., Goodlett, D.R., Ernst, R.K. and Darveau, R.P. (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

    Article  PubMed  CAS  Google Scholar 

  • Coats, S.R., Pham, T.T., Bainbridge, B.W., Reife, R.A. and Darveau, R.P. (2005) MD-2 mediates the ability of tetra-acylated and penta-acylated lipopolysaccharides to antagonize Escherichia coli lipopolysaccharide at the TLR4 signaling complex. J. Immunol. 175, 4490-4498

    PubMed  CAS  Google Scholar 

  • Darveau, R.P. (2009) The oral microbial consortium’s interaction with the periodontal innate defense system. DNA Cell Biol 28, 389-395

    Article  PubMed  CAS  Google Scholar 

  • Darveau, R.P. (2010) Periodontitis: a polymicrobial disruption of host homeostasis. Nat. Rev. Microbiol. 8, 481-490

    Article  PubMed  CAS  Google Scholar 

  • Darveau, R.P., Arbabi, S., Garcia, I., Bainbridge, B. and Maier, R.V. (2002) Porphyromonas gingivalis lipopolysaccharide is both agonist and antagonist for p38 mitogen-activated protein kinase activation. Infect. Immun. 70, 1867-1873

    Article  PubMed  CAS  Google Scholar 

  • Davey, M.E. and Costerton, J.W. (2006) Molecular genetics analyses of biofilm formation in oral isolates. Periodontol. 2000 42, 13-26

    Article  PubMed  Google Scholar 

  • de Pablo, P., Chapple, I.L., Buckley, C.D. and Dietrich, T. (2009) Periodontitis in systemic rheumatic diseases. Nat. Rev. Rheumatol. 5, 218-224

    Article  PubMed  Google Scholar 

  • Delima, A.J. and Van Dyke, T.E. (2003) Origin and function of the cellular components in gingival crevice fluid. Periodontol. 2000 31, 55-76

    Article  PubMed  Google Scholar 

  • Domon, H., Honda, T., Oda, T., Yoshie, H. and Yamazaki, K. (2008) Early and preferential induction of IL-1 receptor-associated kinase-M in THP-1 cells by LPS derived from Porphyromonas gingivalis. J. Leukoc. Biol. 83, 672-679

    Article  PubMed  CAS  Google Scholar 

  • Feuille, F., Ebersole, J.L., Kesavalu, L., Stepfen, M.J. and Holt, S.C. (1996) Mixed infection with Porphyromonas gingivalis and Fusobacterium nucleatum in a murine lesion model: potential synergistic effects on virulence. Infect. Immun. 64, 2094-2100

    PubMed  CAS  Google Scholar 

  • Finegold, S.M. (1991) Aspiration pneumonia. Rev Infect Dis 13 Suppl 9, S737-742

    Article  PubMed  Google Scholar 

  • Flannagan, R.S., Cosio, G. and Grinstein, S. (2009) Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat. Rev. Microbiol. 7, 355-366

    Article  PubMed  CAS  Google Scholar 

  • Gaffen, S.L. and Hajishengallis, G. (2008) A new inflammatory cytokine on the block: re-thinking periodontal disease and the Th1/Th2 paradigm in the context of Th17 cells and IL-17. J. Dent. Res. 87, 817-828

    Article  PubMed  CAS  Google Scholar 

  • Graves, D.T., Fine, D., Teng, Y.-T.A., Van Dyke, T.E. and Hajishengallis, G. (2008) The use of rodent models to investigate host-bacteria interactions related to periodontal diseases. J. Clin. Periodontol. 35, 89-105

    Article  PubMed  Google Scholar 

  • Guenther, F., Stroh, P., Wagner, C., Obst, U. and Hansch, G.M. (2009) Phagocytosis of staphylococci biofilms by polymorphonuclear neutrophils: S. aureus and S. epidermidis differ with regard to their susceptibility towards the host defense. Int. J. Artif. Organs 32, 565-573

    PubMed  Google Scholar 

  • Gunther, F., Wabnitz, G.H., Stroh, P., Prior, B., Obst, U., Samstag, Y., Wagner, C. and Hansch, G.M. (2009) Host defence against Staphylococcus aureus biofilms infection: phagocytosis of biofilms by polymorphonuclear neutrophils (PMN). Mol. Immunol. 46, 1805-1813

    Article  PubMed  CAS  Google Scholar 

  • Guzik, K., Bzowska, M., Smagur, J., Krupa, O., Sieprawska, M., Travis, J. and Potempa, J. (2007) A new insight into phagocytosis of apoptotic cells: proteolytic enzymes divert the recognition and clearance of polymorphonuclear leukocytes by macrophages. Cell Death Differ. 14, 171-182

    Article  PubMed  CAS  Google Scholar 

  • Hajishengallis, G. (2007) Peptide mapping of a functionally versatile fimbrial adhesin from Porphyromonas gingivalis. Int. J. Pept. Res. Ther. 13, 533-546

    Article  CAS  Google Scholar 

  • Hajishengallis, G. (2009) Porphyromonas gingivalis-host interactions: open war or intelligent guerilla tactics? Microbes Infect. 11, 637-645

    Article  PubMed  CAS  Google Scholar 

  • Hajishengallis, G. (2010) Complement and periodontitis. Biochem Pharmacol 80 1992-2001

    Article  PubMed  CAS  Google Scholar 

  • Hajishengallis, G. and Harokopakis, E. (2007) Porphyromonas gingivalis interactions with complement receptor 3 (CR3): innate immunity or immune evasion? Front. Biosci. 12, 4547-4557

    Article  PubMed  CAS  Google Scholar 

  • Hajishengallis, G. and Lambris, J.D. (2010) Crosstalk pathways between Toll-like receptors and the complement system. Trends Immunol. 31, 154-163

    Article  PubMed  CAS  Google Scholar 

  • Hajishengallis, G. and Lambris, J.D. (2011) Microbial manipulation of receptor crosstalk in innate immunity. Nat. Rev. Immunol. 11, 187-200

    Article  PubMed  CAS  Google Scholar 

  • Hajishengallis, G., Martin, M., Schifferle, R.E. and Genco, R.J. (2002) Counteracting interactions between lipopolysaccharide molecules with differential activation of Toll-like receptors. Infect. Immun. 70, 6658-6664

    Article  PubMed  CAS  Google Scholar 

  • Hajishengallis, G., Shakhatreh, M.-A.K., Wang, M. and Liang, S. (2007) Complement receptor 3 blockade promotes IL-12-mediated clearance of Porphyromonas gingivalis and negates its virulence in vivo. J. Immunol. 179, 2359-2367

    PubMed  CAS  Google Scholar 

  • Hajishengallis, G., Tapping, R.I., Harokopakis, E., Nishiyama, S.-I., Ratti, P., Schifferle, R.E., Lyle, E.A., Triantafilou, M., Triantafilou, K. and 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

    Article  PubMed  CAS  Google Scholar 

  • Hajishengallis, G., Wang, M., Krauss, J.L., Domon, H., Hosur, K.B., Liang, S., Magotti, P., Triantafilou, M., Triantafilou, K. and Lambris, J.D. (2010) Pathogen-instigated subversive crosstalk between complement and Toll-like receptors. Mol Immunol 47, 2241

    Article  Google Scholar 

  • Hajishengallis, G., Wang, M., Liang, S., Triantafilou, M. and Triantafilou, K. (2008) Pathogen induction of CXCR4/TLR2 crosstalk impairs host defense function. Proc. Natl. Acad. Sci. U S A 105, 13532-13537

    Article  PubMed  Google Scholar 

  • Harokopakis, E. and Hajishengallis, G. (2005) Integrin activation by bacterial fimbriae through a pathway involving CD14, Toll-like receptor 2, and phosphatidylinositol-3-kinase. Eur. J. Immunol. 35, 1201-1210

    Article  PubMed  CAS  Google Scholar 

  • Hasturk, H., Kantarci, A., Goguet-Surmenian, E., Blackwood, A., Andry, C., Serhan, C.N. and Van Dyke, T.E. (2007) Resolvin E1 regulates inflammation at the cellular and tissue level and restores tissue homeostasis in vivo. J. Immunol. 179, 7021-7029

    PubMed  CAS  Google Scholar 

  • Hawlisch, H., Belkaid, Y., Baelder, R., Hildeman, D., Gerard, C. and Kohl, J. (2005) C5a negatively regulates toll-like receptor 4-induced immune responses. Immunity 22, 415-426

    Article  PubMed  CAS  Google Scholar 

  • Holt, S.C. and Ebersole, J.L. (2005) Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the "red complex", a prototype polybacterial pathogenic consortium in periodontitis. Periodontol. 2000 38, 72-122

    Article  PubMed  Google Scholar 

  • Janeway, C.A., Jr. and Medzhitov, R. (2002) Innate immune recognition. Annu. Rev. Immunol. 20, 197-216

    Article  PubMed  CAS  Google Scholar 

  • Jenkinson, H.F. and Lamont, R.J. (2005) Oral microbial communities in sickness and in health. Trends Microbiol. 13, 589-595

    Article  PubMed  CAS  Google Scholar 

  • Kebschull, M., Demmer, R.T. and Papapanou, P.N. (2010) “Gum bug leave my heart alone”–Epidemiologic and mechanistic evidence linking periodontal infections and atherosclerosis. J. Dent. Res. 89, 879-902

    Article  PubMed  CAS  Google Scholar 

  • Kesavalu, L., Holt, S.C. and Ebersole, J.L. (1998) Virulence of a polymicrobic complex, Treponema denticola and Porphyromonas gingivalis, in a murine model. Oral Microbiol. Immunol. 13, 373-377

    Article  PubMed  CAS  Google Scholar 

  • Kesavalu, L., Sathishkumar, S., Bakthavatchalu, V., Matthews, C., Dawson, D., Steffen, M. and Ebersole, J.L. (2007) Rat model of polymicrobial infection, immunity, and alveolar bone resorption in periodontal disease. Infect. Immun. 75, 1704-1712

    Article  PubMed  CAS  Google Scholar 

  • Kinane, D.F. and Hajishengallis, G. (2009) Polymicrobial infections, biofilms, and beyond. J Clin Periodontol 36, 404-405

    Article  PubMed  Google Scholar 

  • Kolenbrander, P.E., Palmer, R.J., Periasamy, S. and Jakubovics, N.S. (2010) Oral multispecies biofilm development and the key role of cell-cell distance. Nat Rev Microbiol 8, 471-480

    Article  PubMed  CAS  Google Scholar 

  • Kozarov, E.V., Dorn, B.R., Shelburne, C.E., Dunn, W.A., Jr. and Progulske-Fox, A. (2005) Human atherosclerotic plaque contains viable invasive Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. Arterioscler. Thromb. Vasc. Biol. 25, e17-e18

    Article  PubMed  CAS  Google Scholar 

  • Krauss, J.L., Potempa, J., Lambris, J.D. and Hajishengallis, G. (2010) Complementary Tolls in the periodontium: how periodontal bacteria modify complement and Toll-like receptor responses to prevail in the host. Periodontol. 2000 52, 141-162

    Article  PubMed  Google Scholar 

  • Lambris, J.D., Ricklin, D. and Geisbrecht, B.V. (2008) Complement evasion by human pathogens. Nat Rev Microbiol 6, 132-142

    Article  PubMed  CAS  Google Scholar 

  • Lamont, R.J. and Jenkinson, H.F. (1998) Life below the gum line: Pathogenic mechanisms of Porphyromonas gingivalis. Microbiol. Mol. Biol. Rev. 62, 1244-1263

    PubMed  CAS  Google Scholar 

  • Lange, D. and Schroeder, H.E. (1971) Cytochemistry and ultrastructure of gingival sulcus cells. Helv. Odontol. Acta 15, 65-86

    CAS  Google Scholar 

  • Liang, S., Krauss, J.L., Domon, H., McIntosh, M.L., Hosur, K.B., Qu, H., Li, F., Tzekou, A., Lambris, J.D. and Hajishengallis, G. (2010) The C5a receptor impairs IL-12-dependent clearance of Porphyromonas gingivalis and is required for induction of periodontal bone loss. J. Immunol. doi: 10.4049/jimmunol.1003252

    Google Scholar 

  • Lu, Q., Darveau, R.P., Samaranayake, L.P., Wang, C.Y. and Jin, L. (2009) Differential modulation of human β-defensins expression in human gingival epithelia by Porphyromonas gingivalis lipopolysaccharide with tetra- and penta-acylated lipid A structures. Innate Immun. 15, 325-335

    Article  PubMed  CAS  Google Scholar 

  • Lundberg, K., Wegner, N., Yucel-Lindberg, T. and Venables, P.J. (2010) Periodontitis in RA-the citrullinated enolase connection. Nat.Rev. Rheumatol. 6, 727-30

    Article  PubMed  CAS  Google Scholar 

  • Medzhitov, R. (2001) Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1, 135-145

    Article  PubMed  CAS  Google Scholar 

  • Medzhitov, R. (2007) Recognition of microorganisms and activation of the immune response. Nature 449, 819-826

    Article  PubMed  CAS  Google Scholar 

  • Meyle, E., Stroh, P., Gunther, F., Hoppy-Tichy, T., Wagner, C. and Hansch, G.M. (2010) Destruction of bacterial biofilms by polymorphonuclear neutrophils: relative contribution of phagocytosis, DNA release, and degranulation. Int. J. Artif. Organs 33, 608-620

    PubMed  CAS  Google Scholar 

  • Newman, H.N. (1980) Neutrophils and IgG at the host-plaque interface on children’s teeth. J. Periodontol. 51, 642-651

    Article  PubMed  CAS  Google Scholar 

  • Niederman, R., Westernoff, T., Lee, C., Mark, L.L., Kawashima, N., Ullman-Culler, M., Dewhirst, F.E., Paster, B.J., Wagner, D.D., Mayadas, T., Hynes, R.O. and Stashenko, P. (2001) Infection-mediated early-onset periodontal disease in P/E-selectin-deficient mice. J. Clin. Periodontol. 28, 569-575

    Article  PubMed  CAS  Google Scholar 

  • Okuda, K., Kimizuka, R., Abe, S., Kato, T. and Ishihara, K. (2005) Involvement of periodontopathic anaerobes in aspiration pneumonia. J. Periodontol. 76, 2154-2160

    Article  PubMed  Google Scholar 

  • Paine, R.T. (1969) The Pisaster-Tegula Interaction: Prey Patches, Predator Food Preference, and Intertidal Community Structure. Ecology 50, 950-961

    Article  Google Scholar 

  • Pfeiffer, A., Bottcher, A., Orso, E., Kapinsky, M., Nagy, P., Bodnar, A., Spreitzer, I., Liebisch, G., Drobnik, W., Gempel, K., Horn, M., Holmer, S., Hartung, T., Multhoff, G., Schutz, G., Schindle, r.H., Ulmer, A., Heine, H., Stelter, F., Schutt, C., Rothe, G., Szollosi, J., Damjanovich, S. and Schmitz, G. (2001) Lipopolysaccharide and ceramide docking to CD14 provokes ligand-specific receptor clustering in rafts. Eur. J. Immunol. 31, 3153-3164

    Article  PubMed  CAS  Google Scholar 

  • Pihlstrom, B.L., Michalowicz, B.S. and Johnson, N.W. (2005) Periodontal diseases. Lancet 366, 1809-1820

    Article  PubMed  Google Scholar 

  • Polak, D., Wilensky, A., Shapira, L., Halabi, A., Goldstein, D., Weiss, E.I. and Houri-Haddad, Y. (2009) Mouse model of experimental periodontitis induced by P. gingivalis/F. nucleatum infection: Bone loss and host response. J. Clin. Periodontol. 36, 406-410

    Article  PubMed  Google Scholar 

  • Popadiak, K., Potempa, J., Riesbeck, K. and Blom, A.M. (2007) Biphasic effect of gingipains from Porphyromonas gingivalis on the human complement system. J. Immunol. 178, 7242-7250

    PubMed  CAS  Google Scholar 

  • Potempa, J. and Pike, R.N. (2009) Corruption of innate immunity by bacterial proteases. J. Innate Immun. 1, 70-87

    Article  PubMed  CAS  Google Scholar 

  • Potempa, M., Potempa, J., Kantyka, T., Nguyen, K.A., Wawrzonek, K., Manandhar, S.P., Popadiak, K., Riesbeck, K., Eick, S. and Blom, A.M. (2009) Interpain A, a cysteine proteinase from Prevotella intermedia, inhibits complement by degrading complement factor C3. PLoS Pathog. 5, e1000316

    Article  PubMed  CAS  Google Scholar 

  • Potempa, M., Potempa, J., Okroj, M., Popadiak, K., Eick, S., Nguyen, K.A., Riesbeck, K. and Blom, A.M. (2008) Binding of complement inhibitor C4b-binding protein contributes to serum resistance of Porphyromonas gingivalis. J. Immunol. 181, 5537-5544

    PubMed  CAS  Google Scholar 

  • Rangarajan, M., Aduse-Opoku, J., Paramonov, N., Hashim, A., Bostanci, N., Fraser, O.P., Tarelli, E. and Curtis, M.A. (2008) Identification of a second lipopolysaccharide in Porphyromonas gingivalis W50. J. Bacteriol. 190, 2920-2932

    Article  PubMed  CAS  Google Scholar 

  • Ricklin, D., Hajishengallis, G., Yang, K. and Lambris, J.D. (2010) Complement: a key system for immune surveillance and homeostasis. Nat. Immunol. 11, 785-797

    Article  PubMed  CAS  Google Scholar 

  • Rosenberger, C.M. and Finlay, B.B. (2003) Phagocyte sabotage: disruption of macrophage signalling by bacterial pathogens. Nat. Rev. Mol. Cell Biol. 4, 385-396

    Article  PubMed  CAS  Google Scholar 

  • Roy, C.R. and Mocarski, E.S. (2007) Pathogen subversion of cell-intrinsic innate immunity. Nat. Immunol. 8, 1179-1187

    Article  PubMed  CAS  Google Scholar 

  • Ryder, M.I. (2010) Comparison of neutrophil functions in aggressive and chronic periodontitis. Periodontol. 2000 53, 124-137

    Article  PubMed  Google Scholar 

  • Schroeder, H.E. and Listgarten, M.A. (1997) The gingival tissues: the architecture of periodontal protection. Periodontol. 2000 13, 91-120

    Article  PubMed  CAS  Google Scholar 

  • Slaney, J.M., Gallagher, A., Aduse-Opoku, J., Pell, K. and Curtis, M.A. (2006) Mechanisms of resistance of Porphyromonas gingivalis to killing by serum complement. Infect. Immun. 74, 5352-5361

    Article  PubMed  CAS  Google Scholar 

  • Socransky, S.S., Haffajee, A.D., Cugini, M.A., Smith, C. and Kent, R.L., Jr. (1998) Microbial complexes in subgingival plaque. J. Clin. Periodontol. 25, 134-144

    Article  PubMed  CAS  Google Scholar 

  • Tonetti, M.S., D’Aiuto, F., Nibali, L., Donald, A., Storry, C., Parkar, M., Suvan, J., Hingorani, A.D., Vallance, P. and Deanfield, J. (2007) Treatment of periodontitis and endothelial function. N. Engl. J. Med. 356, 911-920

    Article  PubMed  CAS  Google Scholar 

  • Tonetti, M.S., Imboden, M.A., Gerber, L., Lang, N.P., Laissue, J. and Mueller, C. (1994) Localized expression of mRNA for phagocyte-specific chemotactic cytokines in human periodontal infections. Infect. Immun. 62, 4005-4014

    PubMed  CAS  Google Scholar 

  • Triantafilou, M., Brandenburg, K., Gutsmann, T., Seydel, U. and Triantafilou, K. (2002) Innate recognition of bacteria: engagement of multiple receptors. Crit. Rev. Immunol. 22, 251-268

    Article  PubMed  CAS  Google Scholar 

  • Triantafilou, K., Triantafilou, M. and Dedrick, R.L. (2001) A CD14-independent LPS receptor cluster. Nat. Immunol. 2, 338-345

    Article  PubMed  CAS  Google Scholar 

  • Trinchieri, G. (2003) Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3, 133-146

    Article  PubMed  CAS  Google Scholar 

  • Uematsu, S. and Akira, S. (2008) Toll-Like receptors (TLRs) and their ligands. Handb. Exp. Pharmacol. 183, 1-20

    Article  PubMed  CAS  Google Scholar 

  • Vitkov, L., Klappacher, M., Hannig, M. and Krautgartner, W.D. (2010) Neutrophil fate in gingival crevicular fluid. Ultrastruct. Pathol. 34, 25-30

    Article  PubMed  Google Scholar 

  • Wagner, C., Zimmermann, S., Brenner-Weiss, G., Hug, F., Prior, B., Obst, U. and Hansch, G.M. (2007) The quorum-sensing molecule N-3-oxododecanoyl homoserine lactone (3OC12-HSL) enhances the host defence by activating human polymorphonuclear neutrophils (PMN). Anal. Bioanal. Chem. 387, 481-487

    Article  PubMed  CAS  Google Scholar 

  • Wang, M. and Hajishengallis, G. (2008) Lipid raft-dependent uptake, signalling and intracellular fate of Porphyromonas gingivalis in mouse macrophages. Cell. Microbiol. 10, 2029-2042

    Article  PubMed  CAS  Google Scholar 

  • Wang, M., Krauss, J.L., Domon, H., Hosur, K.B., Liang, S., Magotti, P., Triantafilou, M., Triantafilou, K., Lambris, J.D. and Hajishengallis, G. (2010) Microbial hijacking of complement-Toll-like receptor crosstalk. Sci. Signal. 3, ra11

    Article  PubMed  CAS  Google Scholar 

  • Wang, M., Shakhatreh, M.-A.K., James, D., Liang, S., Nishiyama, S.-i., Yoshimura, F., Demuth, D.R. and Hajishengallis, G. (2007) Fimbrial proteins of Porphyromonas gingivalis mediate in vivo virulence and exploit TLR2 and complement receptor 3 to persist in macrophages. J. Immunol. 179, 2349-2358

    PubMed  CAS  Google Scholar 

  • Wingrove, J.A., DiScipio, R.G., Chen, Z., Potempa, J., Travis, J. and Hugli, T.E. (1992) Activation of complement components C3 and C5 by a cysteine proteinase (gingipain-1) from Porphyromonas (Bacteroides) gingivalis. J. Biol. Chem. 267, 18902-18907

    PubMed  CAS  Google Scholar 

  • Xiong, X., Buekens, P., Fraser, W.D., Beck, J. and Offenbacher, S. (2006) Periodontal disease and adverse pregnancy outcomes: a systematic review. BJOG 113, 135-143

    Article  PubMed  CAS  Google Scholar 

  • Yilmaz, O. (2008) The chronicles of Porphyromonas gingivalis: the microbium, the human oral epithelium and their interplay. Microbiology 154, 2897-2903

    Article  PubMed  CAS  Google Scholar 

  • Zhang, X., Kimura, Y., Fang, C., Zhou, L., Sfyroera, G., Lambris, J.D., Wetsel, R.A., Miwa, T. and Song, W.C. (2007) Regulation of Toll-like receptor-mediated inflammatory response by complement in vivo. Blood 110, 228-236

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors acknowledge support by US Public Health Service Grants DE015254, DE018292, DE017138, DE021580 (GH) and GM062134, AI030040, AI072106, AI068730 (JDL).

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Hajishengallis, G., Krauss, J.L., Liang, S., McIntosh, M.L., Lambris, J. (2012). Pathogenic Microbes and Community Service Through Manipulation of Innate Immunity. In: Lambris, J., Hajishengallis, G. (eds) Current Topics in Innate Immunity II. Advances in Experimental Medicine and Biology, vol 946. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-0106-3_5

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