Scavenger receptor A is expressed by macrophages in response to Porphyromonas gingivalis, and participates in TNF-α expression

Oral Microbiology and Immunology

Volumn 24, Issue 6, 2009, Pages 456-463

  Baer, M T ^a   Huang, N ^a   Gibson III, F C ^a  

^a BOSTON UNIVERSITY   (United States)

Author keywords

Macrophage; Porphyromonas gingivalis; Scavenger receptor A; TNF

Indexed keywords

LOW DENSITY LIPOPROTEIN; POLYSACCHARIDE; SCAVENGER RECEPTOR A; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE; GENE EXPRESSION; IMMUNE RESPONSE; MACROPHAGE; MOUSE; MSR1 GENE; NONHUMAN; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION;

ANIMALS; CELLS, CULTURED; FIMBRIAE PROTEINS; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PORPHYROMONAS GINGIVALIS; SCAVENGER RECEPTORS, CLASS A; TUMOR NECROSIS FACTOR-ALPHA; VIRULENCE FACTORS;

EID: 70350026188     PISSN: 09020055     EISSN: 1399302X     Source Type: Journal    
DOI: 10.1111/j.1399-302X.2009.00538.x     Document Type: Article

References (76)

1. Areschoug T, Gordon S. Pattern recognition receptors and their role in innate immunity: focus on microbial protein ligands. Contrib Microbiol 2008 : 15 : 45 60.
2. Asai Y, Ohyama Y, Gen K, Ogawa T. Bacterial fimbriae and their peptides activate human gingival epithelial cells through Toll-like receptor 2. Infect Immun 2001 : 69 : 7387 7395.
3. Bainbridge BW, Coats SR, Darveau RP. Porphyromonas gingivalis lipopolysaccharide displays functionally diverse interactions with the innate host defense system. Ann Periodontol 2002 : 7 : 29 37.
4. Brown MS, Basu SK, Falck JR, Ho YK, Goldstein JL. The scavenger cell pathway for lipoprotein degradation: specificity of the binding site that mediates the uptake of negatively-charged LDL by macrophages. J Supramol Struct 1980 : 13 : 67 81.
5. Burns E, Bachrach G, Shapira L, Nussbaum G. 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 2006 : 177 : 8296 8300.
6. Califano JV, Schifferle RE, Gunsolley JC, Best AM, Schenkein HA, Tew JG. Antibody reactive with Porphyromonas gingivalis serotypes K1-6 in adult and generalized early-onset periodontitis. J Periodontol 1999 : 70 : 730 735.
7. Christie RH, Freeman M, Hyman BT. Expression of the macrophage scavenger receptor, a multifunctional lipoprotein receptor, in microglia associated with senile plaques in Alzheimer's disease. Am J Pathol 1996 : 148 : 399 403.
8. d'Empaire G, Baer MT, Gibson FC 3rd. K1 serotype capsular polysaccharide of Porphyromonas gingivalis elicits chemokine production from murine macrophages that facilitates cell migration. Infect Immun 2006 : 74 : 6236 6243.
9. Dasanayake AP. C-reactive protein levels are elevated in patients with periodontitis and their CRP levels may go down after periodontal therapy. J Evid Based Dent Pract 2009 : 9 : 21 22.
10. Davey M, Liu X, Ukai T et al. Bacterial fimbriae stimulate proinflammatory activation in the endothelium through distinct TLRs. J Immunol 2008 : 180 : 2187 2195.
11. Dunne DW, Resnick D, Greenberg J, Krieger M, Joiner KA. The type I macrophage scavenger receptor binds to gram-positive bacteria and recognizes lipoteichoic acid. Proc Natl Acad Sci U S A 1994 : 91 : 1863 1867.
12. Emingil G, Atilla G, Huseyinov A. Gingival crevicular fluid monocyte chemoattractant protein-1 and RANTES levels in patients with generalized aggressive periodontitis. J Clin Periodontol 2004 : 31 : 829 834.
13. Eskan MA, Hajishengallis G, Kinane DF. Differential activation of human gingival epithelial cells and monocytes by Porphyromonas gingivalis fimbriae. Infect Immun 2007 : 75 : 892 898.
14. Folwaczny M, Glas J, Torok HP, Limbersky O, Folwaczny C. Toll-like receptor (TLR) 2 and 4 mutations in periodontal disease. Clin Exp Immunol 2004 : 135 : 330 335.
15. Geivelis M, Turner DW, Pederson ED, Lamberts BL. Measurements of interleukin-6 in gingival crevicular fluid from adults with destructive periodontal disease. J Periodontol 1993 : 64 : 980 983.
16. Giacona MB, Papapanou PN, Lamster IB et al. Porphyromonas gingivalis induces its uptake by human macrophages and promotes foam cell formation in vitro. FEMS Microbiol Lett 2004 : 241 : 95 101.
17. Gibson FC 3rd., Ukai T, Genco CA. Engagement of specific innate immune signaling pathways during Porphyromonas gingivalis induced chronic inflammation and atherosclerosis. Front Biosci 2008 : 13 : 2041 2059.
18. Gonzalez D, Tzianabos AO, Genco CA, Gibson FC 3rd. Immunization with Porphyromonas gingivalis capsular polysaccharide prevents P. gingivalis-elicited oral bone loss in a murine model. Infect Immun 2003 : 71 : 2283 2287.
19. Gordon S. Pattern recognition receptors: doubling up for the innate immune response. Cell 2002 : 111 : 927 930.
20. Graves DT, Oskoui M, Volejnikova S et al. Tumor necrosis factor modulates fibroblast apoptosis, PMN recruitment, and osteoclast formation in response to P. gingivalis infection. J Dent Res 2001 : 80 : 1875 1879.
21. Greenberg JW, Fischer W, Joiner KA. Influence of lipoteichoic acid structure on recognition by the macrophage scavenger receptor. Infect Immun 1996 : 64 : 3318 3325.
22. Hajishengallis G, Wang M, Bagby GJ, 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.
23. Hampton RY, Golenbock DT, Penman M, Krieger M, Raetz CR. Recognition and plasma clearance of endotoxin by scavenger receptors. Nature 1991 : 352 : 342 344.
24. Harokopakis E, Albzreh MH, Martin MH, 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.
25. Haworth R, Platt N, Keshav S et al. The macrophage scavenger receptor type A is expressed by activated macrophages and protects the host against lethal endotoxic shock. J Exp Med 1997 : 186 : 1431 1439.
26. Heine H, Lien E. Toll-like receptors and their function in innate and adaptive immunity. Int Arch Allergy Immunol 2003 : 130 : 180 192.
27. Hiramine H, Watanabe K, Hamada N, Umemoto T. Porphyromonas gingivalis 67-kDa fimbriae induced cytokine production and osteoclast differentiation utilizing TLR2. FEMS Microbiol Lett 2003 : 229 : 49 55.
28. Hirschfeld M, Weis JJ, Toshchakov V et al. Signaling by toll-like receptor 2 and 4 agonists results in differential gene expression in murine macrophages. Infect Immun 2001 : 69 : 1477 1482.
29. Hughes DA, Fraser IP, Gordon S. Murine macrophage scavenger receptor: in vivo expression and function as receptor for macrophage adhesion in lymphoid and non-lymphoid organs. Eur J Immunol 1995 : 25 : 466 473.
30. Janeway CA Jr., Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002 : 20 : 197 216.
31. Kato T, Kawai S, Nakano K et al. Virulence of Porphyromonas gingivalis is altered by substitution of fimbria gene with different genotype. Cell Microbiol 2007 : 9 : 753 765.
32. Kinane DF, Shiba H, Stathopoulou PG et al. Gingival epithelial cells heterozygous for Toll-like receptor 4 polymorphisms Asp299Gly and Thr399ile are hypo-responsive to Porphyromonas gingivalis. Genes Immun 2006 : 7 : 190 200.
33. Kodama T, Freeman M, Rohrer L, Zabrecky J, Matsudaira P, Krieger M. Type I macrophage scavenger receptor contains alpha-helical and collagen-like coiled coils. Nature 1990 : 343 : 531 535.
34. Kunjathoor VV, Febbraio M, Podrez EA et al. Scavenger receptors class A-I/II and CD36 are the principal receptors responsible for the uptake of modified low density lipoprotein leading to lipid loading in macrophages. J Biol Chem 2002 : 277 : 49982 49988.
35. Laine ML, van Winkelhoff AJ. Virulence of six capsular serotypes of Porphyromonas gingivalis in a mouse model. Oral Microbiol Immunol 1998 : 13 : 322 325.
36. Lamont RJ, Jenkinson HF. Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol Mol Biol Rev 1998 : 62 : 1244 1263.
37. Lin YL, de Villiers WJ, Garvy B et al. The effect of class a scavenger receptor deficiency in bone. J Biol Chem 2007 : 282 : 4653 4660.
38. Malek R, Fisher JG, Caleca A et al. Inactivation of the Porphyromonas gingivalis fimA gene blocks periodontal damage in gnotobiotic rats. J Bacteriol 1994 : 176 : 1052 1059.
39. Martin M, Katz J, Vogel SN, Michalek SM. Differential induction of endotoxin tolerance by lipopolysaccharides derived from Porphyromonas gingivalis and Escherichia coli. J Immunol 2001 : 167 : 5278 5285.
40. Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature 2007 : 449 : 819 826.
41. Medzhitov R. Toll-like receptors and innate immunity. Nat Rev Immunol 2001 : 1 : 135 145.
42. Murphy JE, Tedbury PR, Homer-Vanniasinkam S, Walker JH, Ponnambalam S. Biochemistry and cell biology of mammalian scavenger receptors. Atherosclerosis 2005 : 182 : 1 15.
43. Naito M, Suzuki H, Mori T, Matsumoto A, Kodama T, Takahashi K. Coexpression of type I and type II human macrophage scavenger receptors in macrophages of various organs and foam cells in atherosclerotic lesions. Am J Pathol 1992 : 141 : 591 599.
44. Njoroge T, Genco RJ, Sojar HT, Hamada N, Genco CA. A role for fimbriae in Porphyromonas gingivalis invasion of oral epithelial cells. Infect Immun 1997 : 65 : 1980 1984.
45. Peiser L, Gordon S. The function of scavenger receptors expressed by macrophages and their role in the regulation of inflammation. Microbes Infect 2001 : 3 : 149 159.
46. Peiser L, Gough PJ, Kodama T, Gordon S. Macrophage class A scavenger receptor-mediated phagocytosis of Escherichia coli: role of cell heterogeneity, microbial strain, and culture conditions in vitro. Infect Immun 2000 : 68 : 1953 1963.
47. Peiser L, Makepeace K, Pluddemann A et al. Identification of Neisseria meningitidis nonlipopolysaccharide ligands for class A macrophage scavenger receptor by using a novel assay. Infect Immun 2006 : 74 : 5191 5199.
48. Platt N, Haworth R, Darley L, Gordon S. The many roles of the class A macrophage scavenger receptor. Int Rev Cytol 2002 : 212 : 1 40.
49. Pluddemann A, Hoe JC, Makepeace K, Moxon ER, Gordon S. The macrophage scavenger receptor a is host-protective in experimental meningococcal septicaemia. PLoS Pathog 2009 : 5 : e1000297.
50. Potempa J, Sroka A, Imamura T, Travis J. Gingipains, the major cysteine proteinases and virulence factors of Porphyromonas gingivalis: structure, function and assembly of multidomain protein complexes. Curr Protein Pept Sci 2003 : 4 : 397 407.
51. Qi M, Miyakawa H, Kuramitsu HK. Porphyromonas gingivalis induces murine macrophage foam cell formation. Microb Pathog 2003 : 35 : 259 267.
52. Reife RA, Coats SR, Al-Qutub M et al. 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 2006 : 8 : 857 868.
53. Ren L, Leung WK, Darveau RP, Jin L. The expression profile of lipopolysaccharide-binding protein, membrane-bound CD14, and toll-like receptors 2 and 4 in chronic periodontitis. J Periodontol 2005 : 76 : 1950 1959.
54. Roberts FA, McCaffery KA, Michalek SM. Profile of cytokine mRNA expression in chronic adult periodontitis. J Dent Res 1997 : 76 : 1833 1839.
55. Salvi GW, Brown CE, Fujihashi K et al. Inflammatory mediators of the terminal dentition in adult and early onset periodontitis. J Periodontal Res 1998 : 33 : 212 225.
56. Salzberg TN, Overstreet BT, Rogers JD, Califano JV, Best AM, Schenkein HA. C-reactive protein levels in patients with aggressive periodontitis. J Periodontol 2006 : 77 : 933 939.
57. Sawada N, Ogawa T, Asai Y, Makimura Y, Sugiyama A. Toll-like receptor 4-dependent recognition of structurally different forms of chemically synthesized lipid As of Porphyromonas gingivalis. Clin Exp Immunol 2007 : 148 : 529 536.
58. Schifferle RE, Reddy MS, Zambon JJ, Genco RJ, Levine MJ. Characterization of a polysaccharide antigen from Bacteroides gingivalis. J Immunol 1989 : 143 : 3035 3042.
59. Schroder NW, Meister D, Wolff V et al. Chronic periodontal disease is associated with single-nucleotide polymorphisms of the human TLR-4 gene. Genes Immun 2005 : 6 : 448 451.
60. Shashkin P, Dragulev B, Ley K. Macrophage differentiation to foam cells. Curr Pharm Des 2005 : 11 : 3061 3072.
61. Sheets SM, Robles-Price AG, McKenzie RM, Casiano CA, Fletcher HM. Gingipain-dependent interactions with the host are important for survival of Porphyromonas gingivalis. Front Biosci 2008 : 13 : 3215 3238.
62. Slade GD, Beck JD. Plausibility of periodontal disease estimates from NHANES III. J Public Health Dent 1999 : 59 : 67 72.
63. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr. Microbial complexes in subgingival plaque. J Clin Periodontol 1998 : 25 : 134 144.
64. Stary HC, Chandler AB, Glagov S et al. A definition of initial, fatty streak, and intermediate lesions of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation 1994 : 89 : 2462 2478. (Pubitemid 24142837)
65. Suzuki H, Kurihara Y, Takeya M et al. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature 1997 : 386 : 292 296.
66. Suzuki Y, Aoki K, Saito H et al. A tumor necrosis factor-alpha antagonist inhibits inflammatory bone resorption induced by Porphyromonas gingivalis infection in mice. J Periodontal Res 2006 : 41 : 81 91.
67. Thomas CA, Li Y, Kodama T, Suzuki H, Silverstein SC, El Khoury J. Protection from lethal gram-positive infection by macrophage scavenger receptor-dependent phagocytosis. J Exp Med 2000 : 191 : 147 156.
68. Triantafilou M, Gamper FG, Lepper PM et al. 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 2007 : 9 : 2030 2039.
69. Tsai CC, Ho YP, Chen CC. Levels of interleukin-1 beta and interleukin-8 in gingival crevicular fluids in adult periodontitis. J Periodontol 1995 : 66 : 852 859.
70. Ukai T, Yumoto H, Gibson FC 3rd., Genco CA. Macrophage-elicited osteoclastogenesis in response to bacterial stimulation requires Toll-like receptor 2-dependent tumor necrosis factor-alpha production. Infect Immun 2008 : 76 : 812 819.
71. van Winkelhoff AJ, Appelmelk BJ, Kippuw N, de Graaff J. K-antigens in Porphyromonas gingivalis are associated with virulence. Oral Microbiol Immunol 1993 : 8 : 259 265.
72. Wang M, Shakhatreh MA, James D 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.
73. Weinberg A, Belton CM, Park Y, Lamont RJ. Role of fimbriae in Porphyromonas gingivalis invasion of gingival epithelial cells. Infect Immun 1997 : 65 : 313 316.
74. Yavuzyilmaz E, Yamalik N, Bulut S, Ozen S, Ersoy F, Saatci U. The gingival crevicular fluid interleukin-1 beta and tumour necrosis factor-alpha levels in patients with rapidly progressive periodontitis. Aust Dent J 1995 : 40 : 46 49.
75. Yumoto H, Chou HH, Takahashi Y, Davey M, Gibson FC 3rd., Genco CA. Sensitization of human aortic endothelial cells to lipopolysaccharide via regulation of Toll-like receptor 4 by bacterial fimbria-dependent invasion. Infect Immun 2005 : 73 : 8050 8059.
76. Zimmerli S, Edwards S, Ernst JD. Selective receptor blockade during phagocytosis does not alter the survival and growth of Mycobacterium tuberculosis in human macrophages. Am J Respir Cell Mol Biol 1996 : 15 : 760 770.