Complement and periodontitis

Biochemical Pharmacology

Volumn 80, Issue 12, 2010, Pages 1992-2001

  Hajishengallis, George ^a,b  

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

^b University of Louisville School of Medicine   (United States)

Author keywords

C5a; Complement; Inflammation; Innate immunity; Periodontitis

Indexed keywords

ANTIINFLAMMATORY AGENT; BETA2 INTEGRIN; COMPLEMENT; COMPLEMENT COMPONENT C5A; COMPLEMENT RECEPTOR; COMPLEMENT RECEPTOR 3; COMPLEMENT RECEPTOR C5AR; UNCLASSIFIED DRUG; XVA 143;

DISEASE PREDISPOSITION; DRUG MECHANISM; GENETIC POLYMORPHISM; HUMAN; IN VITRO STUDY; NONHUMAN; PATHOGENESIS; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW;

ANIMALS; COMPLEMENT ACTIVATION; COMPLEMENT C5A; COMPLEMENT INACTIVATING AGENTS; COMPLEMENT SYSTEM PROTEINS; GENETIC PREDISPOSITION TO DISEASE; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; MACROPHAGE-1 ANTIGEN; MOLECULAR TARGETED THERAPY; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; RECEPTOR, ANAPHYLATOXIN C5A; SIGNAL TRANSDUCTION;

EID: 78049417345     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2010.06.017     Document Type: Review

References (169)

1. Markiewski M.M., Lambris J.D. The role of complement in inflammatory diseases from behind the scenes into the spotlight. Am J Pathol 2007, 171:715-727.
2. Hajishengallis G., Lambris J.D. Crosstalk pathways between Toll-like receptors and the complement system. Trends Immunol 2010, 31:154-163.
3. Zhang X., Kimura Y., Fang C., Zhou L., Sfyroera G., Lambris J.D., et al. Regulation of Toll-like receptor-mediated inflammatory response by complement in vivo. Blood 2007, 110:228-236.
4. Guo R.F., Riedemann N.C., Ward P.A. Role of C5a-C5aR interaction in sepsis. Shock 2004, 21:1-7.
5. Fearon D.T., Carroll M.C. Regulation of B lymphocyte responses to foreign and self-antigens by the CD19/CD21 complex. Annu Rev Immunol 2000, 18:393-422.
6. Dunkelberger J.R., Song W.C. Complement and its role in innate and adaptive immune responses. Cell Res 2010, 20:34-50.
7. Strainic M.G., Liu J., Huang D., An F., Lalli P.N., Muqim N., et al. Locally produced complement fragments C5a and C3a provide both costimulatory and survival signals to naive CD4+ T cells. Immunity 2008, 28:425-435.
8. Weaver D.J., Reis E.S., Pandey M.K., Kohl G., Harris N., Gerard C., et al. C5a receptor-deficient dendritic cells promote induction of Treg and Th17 cells. Eur J Immunol 2010, 40:710-721.
9. Ricklin D., Lambris J.D. Complement-targeted therapeutics. Nat Biotechnol 2007, 25:1265-1275.
10. Ward P.A. The dark side of C5a in sepsis. Nat Rev Immunol 2004, 4:133-142.
11. Zipfel P.F., Skerka C. Complement regulators and inhibitory proteins. Nat Rev Immunol 2009, 9:729-740.
12. Pettigrew H.D., Teuber S.S., Gershwin M.E. Clinical significance of complement deficiencies. Ann N Y Acad Sci 2009, 1173:108-123.
13. Wagner E., Frank M.M. Therapeutic potential of complement modulation. Nat Rev Drug Discov 2010, 9:43-56.
14. Holers V.M. The spectrum of complement alternative pathway-mediated diseases. Immunol Rev 2008, 223:300-316.
15. Armitage G.C. Classifying periodontal diseases-a long-standing dilemma. Periodontol 2000 2002, 30:9-23.
16. Hajishengallis G. Toll gates to periodontal host modulation and vaccine therapy. Periodontol 2000 2009, 51:181-207.
17. Pihlstrom B.L., Michalowicz B.S., Johnson N.W. Periodontal diseases. Lancet 2005, 366:1809-1820.
18. Brown L.J., Johns B.A., Wall T.P. The economics of periodontal diseases. Periodontol 2000 2002, 29:223-234.
19. Xiong X., Buekens P., Fraser W.D., Beck J., Offenbacher S. Periodontal disease and adverse pregnancy outcomes: a systematic review. Bjog 2006, 113:135-143.
20. Awano S., Ansai T., Takata Y., Soh I., Akifusa S., Hamasaki T., et al. Oral health and mortality risk from pneumonia in the elderly. J Dent Res 2008, 87:334-339.
21. Desvarieux M., Demmer R.T., Rundek T., Boden-Albala B., Jacobs D.R., Sacco R.L., et al. Periodontal microbiota and carotid intima-media thickness: the Oral Infections and Vascular Disease Epidemiology Study (INVEST). Circulation 2005, 111:576-582.
22. Tonetti M.S., D'Aiuto F., Nibali L., Donald A., Storry C., Parkar M., et al. Treatment of periodontitis and endothelial function. N Engl J Med 2007, 356:911-920.
23. Paju S., Scannapieco F.A. Oral biofilms, periodontitis, and pulmonary infections. Oral Dis 2007, 13:508-512.
24. de Pablo P., Chapple I.L., Buckley C.D. Dietrich T. Periodontitis in systemic rheumatic diseases. Nat Rev Rheumatol 2009, 5:218-224.
25. Gaffen S.L., Hajishengallis G. 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 2008, 87:817-828.
26. Graves D. Cytokines that promote periodontal tissue destruction. J Periodontol 2008, 79:1585-1591.
27. Assuma R., Oates T., Cochran D., Amar S., Graves D.T. IL-1 and TNF antagonists inhibit the inflammatory response and bone loss in experimental periodontitis. J Immunol 1998, 160:403-409.
28. Ohyama H., Kato-Kogoe N., Kuhara A., Nishimura F., Nakasho K., Yamanegi K., et al. The involvement of IL-23 and the Th17 pathway in periodontitis. J Dent Res 2009, 88:633-638.
29. Dutzan N., Gamonal J., Silva A., Sanz M., Vernal R. Over-expression of forkhead box P3 and its association with receptor activator of nuclear factor-B ligand, interleukin (IL)-17, IL-10 and transforming growth factor-during the progression of chronic periodontitis. J Clin Periodontol 2009, 36:396-403.
30. Cardoso C.R., Garlet G.P., Crippa G.E., Rosa A.L., Junior W.M., Rossi M.A., et al. Evidence of the presence of T helper type 17 cells in chronic lesions of human periodontal disease. Oral Microbiol Immunol 2009, 24:1-6.
31. Vernal R., Dutzan N., Chaparro A., Puente J., Antonieta Valenzuela M., Gamonal J. Levels of interleukin-17 in gingival crevicular fluid and in supernatants of cellular cultures of gingival tissue from patients with chronic periodontitis. J Clin Periodontol 2005, 32:383-389.
32. Socransky S.S., Haffajee A.D., Cugini M.A., Smith C., Kent R.L. Microbial complexes in subgingival plaque. J Clin Periodontol 1998, 25:134-144.
33. Holt S.C., Ebersole J.L. Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the " red complex" , a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000 2005, 38:72-122.
34. Darveau R.P. Periodontitis: a polymicrobial bacterial-induced disruption of host homeostasis. Nat Rev Microbiol 2010, 8:481-490.
35. Hajishengallis G. Porphyromonas gingivalis-host interactions: open war or intelligent guerilla tactics?. Microbes Infect 2009, 11:637-645.
36. Darveau R.P. The oral microbial consortium's interaction with the periodontal innate defense system. DNA Cell Biol 2009, 28:389-395.
37. Spitzer D., Mitchell L.M., Atkinson J.P., Hourcade D.E. Properdin can initiate complement activation by binding specific target surfaces and providing a platform for de novo convertase assembly. J Immunol 2007, 179:2600-2608.
38. Kimura Y., Miwa T., Zhou L., Song W.-C. Activator-specific requirement of properdin in the initiation and amplification of the alternative pathway complement. Blood 2008, 111:732-740.
39. Harboe M., Mollnes T.E. The alternative complement pathway revisited. J Cell Mol Med 2008, 12:1074-1084.
40. Bamberg C.E., Mackay C.R., Lee H., Zahra D., Jackson J., Lim Y.S., et al. The C5a receptor (C5aR) C5L2 is a modulator of C5aR-mediated signal transduction. J Biol Chem 2010, 285:7633-7644.
41. Chen N.J., Mirtsos C., Suh D., Lu Y.C., Lin W.J., McKerlie C., et al. C5L2 is critical for the biological activities of the anaphylatoxins C5a and C3a. Nature 2007, 446:203-207.
42. Rittirsch D., Flierl M.A., Nadeau B.A., Day D.E., Huber-Lang M., Mackay C.R., et al. Functional roles for C5a receptors in sepsis. Nat Med 2008, 14:551-557.
43. Scola A.M., Johswich K.O., Morgan B.P., Klos A., Monk P.N. The human complement fragment receptor, C5L2, is a recycling decoy receptor. Mol Immunol 2009, 46:1149-1162.
44. Monk P.N., Scola A.M., Madala P., Fairlie D.P. Function, structure and therapeutic potential of complement C5a receptors. Br J Pharmacol 2007, 152:429-448.
45. Kim D.D., Song W.C. Membrane complement regulatory proteins. Clin Immunol 2006, 118:127-136.
46. Heinen S., Hartmann A., Lauer N., Wiehl U., Dahse H.-M., Schirmer S., et al. Factor H-related protein 1 (CFHR-1) inhibits complement C5 convertase activity and terminal complex formation. Blood 2009, 114:2439-2447.
47. Markiewski M.M., Nilsson B., Ekdahl K.N., Mollnes T.E., Lambris J.D. Complement and coagulation: strangers or partners in crime?. Trends Immunol 2007, 28:184-192.
48. Jalili A., Shirvaikar N., Marquez-Curtis L., Qiu Y., Korol C., Lee H., et al. Fifth complement cascade protein (C5) cleavage fragments disrupt the SDF-1/CXCR4 axis: Further evidence that innate immunity orchestrates the mobilization of hematopoietic stem/progenitor cells. Exp Hematol 2010, 38:321-332.
49. Lee H.M., Wysoczynski M., Liu R., Shin D.M., Kucia M., Botto M., et al. Mobilization studies in complement-deficient mice reveal that optimal AMD3100 mobilization of hematopoietic stem cells depends on complement cascade activation by AMD3100-stimulated granulocytes. Leukemia 2009, 24:573-582.
50. Longhi M.P., Harris C.L., Morgan B.P., Gallimore A. Holding T cells in check-a new role for complement regulators?. Trends Immunol 2006, 27:102-108.
51. Wagner C., Ochmann C., Schoels M., Giese T., Stegmaier S., Richter R., et al. The complement receptor 1, CR1 (CD35), mediates inhibitory signals in human T-lymphocytes. Mol Immunol 2006, 43:643-651.
52. Klos A., Tenner A.J., Johswich K.O., Ager R.R., Reis E.S., Kohl J. The role of the anaphylatoxins in health and disease. Mol Immunol 2009, 46:2753-2766.
53. Lambris J.D., Ricklin D., Geisbrecht B.V. Complement evasion by human pathogens. Nat Rev Microbiol 2008, 6:132-142.
54. Attstrom R., Laurel A.B., Lahsson U., Sjoholm A. Complement factors in gingival crevice material from healthy and inflamed gingiva in humans. J Periodont Res 1975, 10:19-27.
55. Schenkein H.A., Genco R.J. Gingival fluid and serum in periodontal diseases. II. Evidence for cleavage of complement components C3, C3 proactivator (factor B) and C4 in gingival fluid. J Periodontol 1977, 48:778-784.
56. Schenkein H.A., Genco R.J. Gingival fluid and serum in periodontal diseases. I. Quantitative study of immunoglobulins, complement components, and other plasma proteins. J Periodontol 1977, 48:772-777.
57. Challacombe S.J., Shirlaw P.J. Immunology of diseases of the oral cavity. Mucosal immunology 2005, 1517-1546. Elsevier Academic Press. J. Mestecky, M.E. Lamm, W. Strober, J. Bienenstock, J.R. McGhee, L. Mayer (Eds.).
58. Patters M.R., Niekrash C.E., Lang N.P. Assessment of complement cleavage in gingival fluid during experimental gingivitis in man. J Clin Periodontol 1989, 16:33-37.
59. Lamster I.B., Ahlo J.K. Analysis of gingival crevicular fluid as applied to the diagnosis of oral and systemic diseases. Ann N Y Acad Sci 2007, 1098:216-229.
60. Popadiak K., Potempa J., Riesbeck K., Blom A.M. Biphasic effect of gingipains from Porphyromonas gingivalis on the human complement system. J Immunol 2007, 178:7242-7250.
61. Schenkein H.A., Genco R.J. Complement cleavage products in inflammatory exudates from patients with periodontal diseases. J Immunol 1978, 120:1796.
62. Lally E.T., McArthur W.P., Baehni P.C. Biosynthesis of complement components in chronically inflamed gingiva. J Periodontal Res 1982, 17:257-262.
63. Courts F.J., Boackle R.J., Fudenberg H.H., Silverman M.S. Detection of functional complement components in gingival crevicular fluid from humans with periodontal diseases. J Dent Res 1977, 56:327-331.
64. Toto P.D., Lin L., Gargiulo A. Identification of C3a, IgG, IgM in inflamed human gingiva. J Dent Res 1978, 57:696.
65. Nikolopoulou-Papaconstantinou A.A., Johannessen A.C., Kristoffersen T. Deposits of immunoglobulins, complement, and immune complexes in inflamed human gingiva. Acta Odontol Scand 1987, 45:187-193.
66. Rautemaa R., Meri S. Protection of gingival epithelium against complement-mediated damage by strong expression of the membrane attack complex inhibitor protectin (CD59). J Dent Res 1996, 75:568-574.
67. Boackle R.J. The interaction of salivary secretions with the human complement system-a model for the study of host defense systems on inflamed mucosal surfaces. Crit Rev Oral Biol Med 1991, 2:355-367.
68. Beikler T., Peters U., Prior K., Eisenacher M., Flemmig T.F. Gene expression in periodontal tissues following treatment. BMC Med Genomics 2008, 1:30.
69. Niekrash C.E., Patters M.R. Simultaneous assessment of complement components C3, C4, and B and their cleavage products in human gingival fluid. II. Longitudinal changes during periodontal therapy. J Periodontal Res 1985, 20:268-275.
70. Snyderman R. Role for endotoxin and complement in periodontal tissue destruction. J Dent Res 1972, 51:356-361.
71. Krauss J.L., Potempa J., Lambris J.D., Hajishengallis G. Complementary Tolls in the periodontium: how periodontal bacteria modify complement and Toll-like receptor responses to prevail in the host. Periodontol 2000 2010, 52:141-162.
72. Van Dyke T.E., Serhan C.N. Resolution of inflammation: a new paradigm for the pathogenesis of periodontal diseases. J Dent Res 2003, 82:82-90.
73. Delima A.J., Van Dyke T.E. Origin and function of the cellular components in gingival crevice fluid. Periodontol 2000 2003, 31:55-76.
74. Schroeder H.E. Transmigration and infiltration of leucocytes in human junctional epithelium. Helv Odontol Acta 1973, 17:6-18.
75. Roberts A., Shah M., Chapple I.L. C-1 esterase inhibitor dysfunction localised to the periodontal tissues: clues to the role of stress in the pathogenesis of chronic periodontitis?. J Clin Periodontol 2003, 30:271-277.
76. Hillebrandt S., Wasmuth H.E., Weiskirchen R., Hellerbrand C., Keppeler H., Werth A., et al. Complement factor 5 is a quantitative trait gene that modifies liver fibrogenesis in mice and humans. Nat Genet 2005, 37:835-843.
77. Chai L., Song Y.-Q., Zee K.-Y., Leung W.K. Single nucleotide polymorphisms of complement component 5 and periodontitis. J Periodont Res 2010, 45:301-308.
78. Niculescu F., Rus H. Mechanisms of signal transduction activated by sublytic assembly of terminal complement complexes on nucleated cells. Immunol Res 2001, 24:191-199.
79. Cybulsky A.V., Takano T., Papillon J., McTavish A.J. Complement-induced phospholipase A2 activation in experimental membranous nephropathy. Kidney Int 2000, 57:1052-1062.
80. Daniels R.H., Houston W.A., Petersen M.M., Williams J.D., Williams B.D., Morgan B.P. Stimulation of human rheumatoid synovial cells by non-lethal complement membrane attack. Immunology 1990, 69:237-242.
81. Raisz L.G., Sandberg A.L., Goodson J.M., Simmons H.A., Mergenhagen S.E. Complement-dependent stimulation of prostaglandin synthesis and bone resorption. Science 1974, 185:789-791.
82. Seppanen M., Lokki M.L., Notkola I.L., Mattila K., Valtonen V., Nieminen A., et al. Complement and c4 null alleles in severe chronic adult periodontitis. Scand J Immunol 2007, 65:176-181.
83. Slaney J.M., Gallagher A., Aduse-Opoku J., Pell K., Curtis M.A. Mechanisms of resistance of Porphyromonas gingivalis to killing by serum complement. Infect Immun 2006, 74:5352-5361.
84. Potempa M., Potempa J., Kantyka T., Nguyen K.A., Wawrzonek K., Manandhar S.P., et al. Interpain A, a cysteine proteinase from Prevotella intermedia, inhibits complement by degrading complement factor C3. PLoS Pathog 2009, 5:e1000316.
85. Hajishengallis G., Wang M., Liang S., Shakhatreh M.A., James D., Nishiyama S., et al. Subversion of innate immunity by periodontopathic bacteria via exploitation of complement receptor-3. Adv Exp Med Biol 2008, 632:203-219.
86. McDowell J.V., Huang B., Fenno J.C., Marconi R.T. Analysis of a unique interaction between the complement regulatory protein factor H and the periodontal pathogen Treponema denticola. Infect Immun 2009, 77:1417-1425.
87. Wang M., Krauss J.L., Domon H., Hosur K.B., Liang S., Magotti P., et al. Microbial hijacking of complement-Toll-like receptor crosstalk. Sci Signal 2010, 3:ra11.
88. Potempa J., Pike R.N. Corruption of innate immunity by bacterial proteases. J Innate Immun 2009, 1:70-87.
89. Slaney J.M., Curtis M.A. Mechanisms of evasion of complement by Porphyromonas gingivalis. Front Biosci 2008, 13:188-196.
90. Kamaguchi A., Ohyama T., Sakai E., Nakamura R., Watanabe T., Baba H., et al. Adhesins encoded by the gingipain genes of Porphyromonas gingivalis are responsible for co-aggregation with Prevotella intermedia. Microbiology 2003, 149:1257-1264.
91. Potempa M., Potempa J., Okroj M., Popadiak K., Eick S., Nguyen K.A., et al. Binding of complement inhibitor C4b-binding protein contributes to serum resistance of Porphyromonas gingivalis. J Immunol 2008, 181:5537-5544.
92. Yamazaki T., Miyamoto M., Yamada S., Okuda K., Ishihara K. Surface protease of Treponema denticola hydrolyzes C3 and influences function of polymorphonuclear leukocytes. Microbes Infect 2006, 8:1758-1763.
93. Mahtout H., Chandad F., Rojo J.M., Grenier D. Porphyromonas gingivalis mediates the shedding and proteolysis of complement regulatory protein CD46 expressed by oral epithelial cells. Oral Microbiol Immunol 2009, 24:396-400.
94. Graves D.T., Fine D., Teng Y-TA, Van Dyke T.E., Hajishengallis G. The use of rodent models to investigate host-bacteria interactions related to periodontal diseases. J Clin Periodontol 2008, 35:89-105.
95. Friec G.L., Kemper C. Complement: coming full circle. Arch Immunol Ther Exp (Warsz) 2009, 57:393-407.
96. Markiewski M.M., DeAngelis R.A., Benencia F., Ricklin-Lichtsteiner S.K., Koutoulaki A., Gerard C., et al. Modulation of the antitumor immune response by complement. Nat Immunol 2008, 9:1225-1235.
97. Griselli M., Herbert J., Hutchinson W.L., Taylor K.M., Sohail M., Krausz T., et al. C-reactive protein and complement are important mediators of tissue damage in acute myocardial infarction. J Exp Med 1999, 190:1733-1740.
98. Garcia-Laorden M.I., Sole-Violan J., Rodriguez de Castro F., Aspa J., Briones M.L., Garcia-Saavedra A., et al. Mannose-binding lectin and mannose-binding lectin-associated serine protease 2 in susceptibility, severity, and outcome of pneumonia in adults. J Allergy Clin Immunol 2008, 122:368-374. 74 e1-2.
99. Roos A., Nauta A.J., Broers D., Faber-Krol M.C., Trouw L.A., Drijfhout J.W., et al. Specific inhibition of the classical complement pathway by C1q-binding peptides. J Immunol 2001, 167:7052-7059.
100. Frakking F.N., Brouwer N., van Eijkelenburg N.K., Merkus M.P., Kuijpers T.W., Offringa M., et al. Low mannose-binding lectin (MBL) levels in neonates with pneumonia and sepsis. Clin Exp Immunol 2007, 150:255-262.
101. Butko P., Nicholson-Weller A., Wessels M.R. Role of complement component C1q in the IgG-Independent opsonophagocytosis of Group B Streptococcus. J Immunol 1999, 163:2761-2768.
102. Yuste J., Ali S., Sriskandan S., Hyams C., Botto M., Brown J.S. Roles of the alternative complement pathway and C1q during innate immunity to Streptococcus pyogenes. J Immunol 2006, 176:6112-6120.
103. Roos A., Ramwadhdoebe T.H., Nauta A.J., Hack C.E., Daha M.R. Therapeutic inhibition of the early phase of complement activation. Immunobiology 2002, 205:595-609.
104. Ehlers M.R.W. CR3: a general purpose adhesion-recognition receptor essential for innate immunity. Microbes Infect 2000, 2:289-294.
105. Triantafilou M., Brandenburg K., Kusumoto S., Fukase K., Mackie A., Seydel U., et al. Combinational clustering of receptors following stimulation by bacterial products determines lipopolysaccharide responses. Biochem J 2004, 381:527-536.
106. Hajishengallis G., Tapping R.I., Harokopakis E., Nishiyama S.-I., Ratti P., Schifferle R.E., et al. Differential interactions of fimbriae and lipopolysaccharide from Porphyromonas gingivalis with the Toll-like receptor 2-centred pattern recognition apparatus. Cell Microbiol 2006, 8:1557-1570.
107. Diamond M.S., Garcia-Aguilar J., Bickford J.K., Corbi A.L., Springer T.A. The I domain is a major recognition site on the leukocyte integrin Mac-1 (CD11b/CD18) for four distinct adhesion ligands. J Cell Biol 1993, 120:1031-1043.
108. McGuirk P., Mills K.H. Direct anti-inflammatory effect of a bacterial virulence factor: IL-10-dependent suppression of IL-12 production by filamentous hemagglutinin from Bordetella pertussis. Eur J Immunol 2000, 30:415-422.
109. Russell D.G., Wright S.D. Complement receptor type 3 (CR3) binds to an Arg-Gly-Asp-containing region of the major surface glycoprotein, gp63, of Leishmania promastigotes. J Exp Med 1988, 168:279-292.
110. Hajishengallis G., Ratti P., Harokopakis E. Peptide mapping of bacterial fimbrial epitopes interacting with pattern recognition receptors. J Biol Chem 2005, 280:38902-38913.
111. Ingalls R.R., Arnaout M.A., Golenbock D.T. Outside-in signaling by lipopolysaccharide through a tailless integrin. J Immunol 1997, 159:433-438.
112. Laudanna C., Kim J.Y., Constantin G., Butcher E.C. Rapid leukocyte integrin activation by chemokines. Immunol Rev 2002, 186:37-46.
113. Harokopakis E., Hajishengallis G. Integrin activation by bacterial fimbriae through a pathway involving CD14 Toll-like receptor 2, and phosphatidylinositol-3-kinase. Eur J Immunol 2005, 35:1201-1210.
114. 2 integrin adhesive activity and promote binding to and internalization by macrophages. Infect Immun 2006, 74:5658-5666.
115. Hajishengallis G., Sojar H., Genco R.J., DeNardin E. Intracellular signaling and cytokine induction upon interactions of Porphyromonas gingivalis fimbriae with pattern-recognition receptors. Immunol Invest 2004, 33:157-172.
116. Harokopakis E., Albzreh M.H., Martin M.H., Hajishengallis G. TLR2 transmodulates monocyte adhesion and transmigration via Rac1- and PI3K-mediated inside-out signaling in response to Porphyromonas gingivalis fimbriae. J Immunol 2006, 176:7645-7656.
117. Luster A.D., Alon R., von Andrian U.H. Immune cell migration in inflammation: present and future therapeutic targets. Nat Immunol 2005, 6:1182-1190.
118. Issekutz A.C., Rowter D., Springer T.A. Role of ICAM-1 and ICAM-2 and alternate CD11/CD18 ligands in neutrophil transendothelial migration. J Leukoc Biol 1999, 65:117-126.
119. Hajishengallis G., Shakhatreh M-AK, Wang M., Liang S. Complement receptor 3 blockade promotes IL-12-mediated clearance of Porphyromonas gingivalis and negates its virulence in vivo. J Immunol 2007, 179:2359-2367.
120. Wang M., Shakhatreh M-AK, James D., Liang S., Nishiyama S-i, Yoshimura F., et al. Fimbrial proteins of Porphyromonas gingivalis mediate in vivo virulence and exploit TLR2 and complement receptor 3 to persist in macrophages. J Immunol 2007, 179:2349-2358.
121. Lowell C.A. Rewiring phagocytic signal transduction. Immunity 2006, 24:243-245.
122. Wright S.D., Silverstein S.C. Receptors for C3b and C3bi promote phagocytosis but not the release of toxic oxygen from human phagocytes. J Exp Med 1983, 158:2016-2023.
123. Caron E., Hall A. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 1998, 282:1717-1721.
124. Rosenberger C.M., Finlay B.B. Phagocyte sabotage: disruption of macrophage signalling by bacterial pathogens. Nat Rev Mol Cell Biol 2003, 4:385-396.
125. Hellwig S.M., van Oirschot H.F., Hazenbos W.L., van Spriel A.B., Mooi F.R., van De Winkel J.G. Targeting to Fcγ receptors, but not CR3 (CD11b/CD18), increases clearance of Bordetella pertussis. J Infect Dis 2001, 183:871-879.
126. Vieira O.V., Botelho R.J., Grinstein S. Phagosome maturation: aging gracefully. Biochem J 2002, 366:689-704.
127. Kim S., Elkon K.B., Ma X. Transcriptional suppression of interleukin-12 gene expression following phagocytosis of apoptotic cells. Immunity 2004, 21:643-653.
128. Mevorach D., Mascarenhas J.O., Gershov D., Elkon K.B. Complement-dependent clearance of apoptotic cells by human macrophages. J Exp Med 1998, 188:2313-2320.
129. Hawlisch H., Belkaid Y., Baelder R., Hildeman D., Gerard C., Kohl J. C5a negatively regulates toll-like receptor 4-induced immune responses. Immunity 2005, 22:415-426.
130. Marth T., Kelsall B.L. Regulation of interleukin-12 by complement receptor 3 signaling. J Exp Med 1997, 185:1987-1995.
131. Hajishengallis G. Too old to fight? Aging and its toll on innate immunity. Mol Oral Microbiol 2010, 25:25-37.
132. Sebastian C., Espia M., Serra M., Celada A., Lloberas J. MacrophAging: a cellular and molecular review. Immunobiology 2005, 210:121-126.
133. Butcher S., Chahel H., Lord J.M. Ageing and the neutrophil: no appetite for killing?. Immunology 2000, 100:411-416.
134. Butcher S.K., Chahal H., Nayak L., Sinclair A., Henriquez N.V., Sapey E., et al. Senescence in innate immune responses: reduced neutrophil phagocytic capacity and CD16 expression in elderly humans. J Leukoc Biol 2001, 70:881-886.
135. Liang S., Hosur K.B., Domon H., Hajishengallis G. Periodontal inflammation and bone loss in aged mice. J Periodont Res 2010, 45:574-578.
136. Guo R.F., Ward P.A. Role of C5a in inflammatory responses. Annu Rev Immunol 2005, 23:821-852.
137. Okroj M., Heinegard D., Holmdahl R., Blom A.M. Rheumatoid arthritis and the complement system. Ann Med 2007, 39:517-530.
138. Kasama T., Miwa Y., Isozaki T., Odai T., Adachi M., Kunkel S.L. Neutrophil-derived cytokines: potential therapeutic targets in inflammation. Curr Drug Targets Inflamm Allergy 2005, 4:273-279.
139. Kanazawa N., Furukawa F. Autoinflammatory syndromes with a dermatological perspective. J Dermatol 2007, 34:601-618.
140. Simpson J.L., Phipps S., Gibson P.G. Inflammatory mechanisms and treatment of obstructive airway diseases with neutrophilic bronchitis. Pharmacol Ther 2009, 124:86-95.
141. Kitsis E., Weissmann G. The role of the neutrophil in rheumatoid arthritis. Clin Orthop Relat Res 1991, 63-72.
142. Lange D., Schroeder H.E. Cytochemistry and ultrastructure of gingival sulcus cells. Helv Odontol Acta 1971, 15:65-86.
143. Newman H.N. Neutrophils and IgG at the host-plaque interface on children's teeth. J Periodontol 1980, 51:642-651.
144. Schroeder H.E., Listgarten M.A. The gingival tissues: the architecture of periodontal protection. Periodontol 2000 1997, 13:91-120.
145. Vitkov L., Klappacher M., Hannig M., Krautgartner W.D. Neutrophil fate in gingival crevicular fluid. Ultrastruct Pathol 2010, 34:25-30.
146. Nathan C. Points of control in inflammation. Nature 2002, 420:846-852.
147. Van Dyke T.E. The management of inflammation in periodontal disease. J Periodontol 2008, 79:1601-1608.
148. Chapple I.L., Matthews J.B. The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontol 2000 2007, 43:160-232.
149. Mydel P., Takahashi Y., Yumoto H., Sztukowska M., Kubica M., Gibson F.C., et al. Roles of the host oxidative immune response and bacterial antioxidant rubrerythrin during Porphyromonas gingivalis infection. PLoS Pathog 2006, 2:e76. (712-25).
150. Wingrove J.A., DiScipio R.G., Chen Z., Potempa J., Travis J., Hugli T.E. Activation of complement components C3 and C5 by a cysteine proteinase (gingipain-1) from Porphyromonas (Bacteroides) gingivalis. J Biol Chem 1992, 267:18902-18907.
151. de Haas C.J.C., Veldkamp K.E., Peschel A., Weerkamp F., Van Wamel W.J.B., Heezius E.C.J.M., et al. Chemotaxis inhibitory protein of Staphylococcus aureus, a bacterial antiinflammatory agent. J Exp Med 2004, 199:687-695.
152. Huber-Lang M.S., Younkin E.M., Sarma J.V., McGuire S.R., Lu K.T., Guo R.F., et al. Complement-induced impairment of innate immunity during sepsis. J Immunol 2002, 169:3223-3231.
153. Riedemann N.C., Guo R.F., Bernacki K.D., Reuben J.S., Laudes I.J., Neff T.A., et al. Regulation by C5a of neutrophil activation during sepsis. Immunity 2003, 19:193-202.
154. Gibson F.C., Hong C., Chou H.H., Yumoto H., Chen J., Lien E., et al. Innate immune recognition of invasive bacteria accelerates atherosclerosis in apolipoprotein E-deficient mice. Circulation 2004, 109:2801-2806.
155. Gibson F.C., Yumoto H., Takahashi Y., Chou H.H., Genco C.A. Innate immune signaling and Porphyromonas gingivalis-accelerated atherosclerosis. J Dent Res 2006, 85:106-121.
156. Okuda K., Kimizuka R., Abe S., Kato T., Ishihara K. Involvement of periodontopathic anaerobes in aspiration pneumonia. J Periodontol 2005, 76:2154-2160.
157. Liang S., Domon H., Hosur K.B., Wang M., Hajishengallis G. Age-related alterations in innate immune receptor expression and ability of macrophages to respond to pathogen challenge in vitro. Mech Ageing Dev 2009, 130:538-546.
158. Hajishengallis G., Wang M., Bagby G.J., Nelson S. Importance of TLR2 in early innate immune response to acute pulmonary infection with Porphyromonas gingivalis in mice. J Immunol 2008, 181:4141-4149.
159. Grant E.P., Picarella D., Burwell T., Delaney T., Croci A., Avitahl N., et al. Essential role for the C5a receptor in regulating the effector phase of synovial infiltration and joint destruction in experimental arthritis. J Exp Med 2002, 196:1461-1471.
160. Ricklin D., Hajishengallis G., Yang K., Lambris J.D. A new perspective on complement: a keystone biological system for immune surveillance and homeostasis. Nat Immunol 2010, 11.
161. Hopken U.E., Lu B., Gerard N.P., Gerard C. The C5a chemoattractant receptor mediates mucosal defence to infection. Nature 1996, 383:86-89.
162. Stevens B., Allen N.J., Vazquez L.E., Howell G.R., Christopherson K.S., Nouri N., et al. The classical complement cascade mediates CNS synapse elimination. Cell 2007, 131:1164-1178.
163. Drouin S.M., Sinha M., Sfyroera G., Lambris J.D., Wetsel R.A. A protective role for the fifth complement component (c5) in allergic airway disease. Am J Respir Crit Care Med 2006, 173:852-857.
164. Baker P.J., DuFour L., Dixon M., Roopenian D.C. Adhesion molecule deficiencies increase Porphyromonas gingivalis-induced alveolar bone loss in mice. Infect Immun 2000, 68:3103-3107.
165. Genco C.A., Van Dyke T., Amar S. Animal models for Porphyromonas gingivalis-mediated periodontal disease. Trends Microbiol 1998, 6:444-449.
166. Ebersole J.L. Humoral immune responses in gingival crevice fluid: local and systemic implications. Periodontol 2000 2003, 31:135-166.
167. Niekrash C.E., Patters M.R. Assessment of complement cleavage in gingival fluid in humans with and without periodontal disease. J Periodontal Res 1986, 21:233-242.
168. Bohana-Kashtan O., Ziporen L., Donin N., Kraus S., Fishelson Z. Cell signals transduced by complement. Mol Immunol 2004, 41:583-597.
169. Hajishengallis G., Harokopakis E. Porphyromonas gingivalis interactions with complement receptor 3 (CR3): innate immunity or immune evasion?. Front Biosci 2007, 12:4547-4557.