Porphyromonas gingivalis-induced platelet aggregation in plasma depends on Hgp44 adhesin but not Rgp proteinase

Molecular Microbiology

Volumn 59, Issue 1, 2006, Pages 152-167

  Naito, Mariko ^a   Sakai, Eiko ^a   Shi, Yixin ^b,d   Ideguchi, Hiroshi ^c   Shoji, Mikio ^a   Ohara, Naoya ^a   Yamamoto, Kenji ^b   Nakayama, Koji ^a  

^a NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c FUKUOKA UNIVERSITY   (Japan)

^d WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL ENZYME; BACTERIAL PROTEIN; FC GAMMA RIIA RECEPTOR; FC RECEPTOR; GINGIPAIN R; GINGIPAIN R PROTEINASE; GLYCOPROTEIN IBALPHA RECEPTOR; HEMAGGLUTININ; HGP44 ADHESIN; IMMUNOGLOBULIN G; LYSINE GINGIPAIN; PROTEINASE; PROTEINASE INHIBITOR; RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CELL SURFACE; CONTROLLED STUDY; CYTOPATHOLOGY; GENE FUNCTION; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MUTATIONAL ANALYSIS; NONHUMAN; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEINASE INHIBITION; THROMBOCYTE; THROMBOCYTE AGGREGATION; THROMBOCYTE AGGREGATION INHIBITION; THROMBOCYTE RICH PLASMA;

ADHESINS, BACTERIAL; ANIMALS; ANTIGENS, CD; BACTERIAL PROTEINS; BLOOD PLATELETS; CELL MEMBRANE; CYSTEINE ENDOPEPTIDASES; DNA MUTATIONAL ANALYSIS; GENETIC COMPLEMENTATION TEST; HUMANS; IMMUNOGLOBULIN G; INTEGRIN ALPHA2; METALLOENDOPEPTIDASES; PERIODONTAL DISEASES; PLASMA; PLATELET AGGREGATION; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PORPHYROMONAS GINGIVALIS; PROTEASE INHIBITORS; RECEPTORS, IGG; TRYPSIN;

BACTERIA (MICROORGANISMS); PORPHYROMONAS GINGIVALIS;

EID: 33645069437     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04942.x     Document Type: Article

References (55)

1. Abe N. Kadowaki T. Okamoto K. Nakayama K. Ohishi M. Yamamoto K. 1998 Biochemical and functional properties of lysine-specific cysteine proteinase (Lys-gingipain) as a virulence factor of Porphyromonas gingivalis in periodontal disease J Biochem (Tokyo) 123 305 312
2. Baba A. Kadowaki T. Asao T. Yamamoto K. 2002 Roles for Arg- and Lys-gingipains in the disruption of cytokine responses and loss of viability of human endothelial cells by Porphyromonas gingivalis infection Biol Chem 383 1223 1230
3. Banbula A. Mak P. Bugno M. Silberring J. Dubin A. Nelson D. et al. 1999a Prolyl tripeptidyl peptidase from Porphyromonas gingivalis. A novel enzyme with possible pathological implications for the development of periodontitis J Biol Chem 274 9246 9252
4. Banbula A. Bugno M. Kuster A. Heinrich PC. Travis J. Potempa J. 1999b Rapid and efficient inactivation of IL-6 gingipains, lysine- and arginine-specific proteinases from Porphyromonas gingivalis Biochem Biophys Res Commun 261 598 602
5. Beck J. Garcia R. Heiss G. Vokonas PS. Offenbacher S. 1996 Periodontal disease and cardiovascular disease J Periodontol 67 1123 1137
6. Byrne MF. Kerrigan SW. Corcoran PA. Atherton JC. Murray FE. Fitzgerald DJ. Cox DM. 2003 Helicobacter pylori binds von Willebrand factor and interacts with GPIb to induce platelet aggregation Gastroenterology 124 1846 1854
7. Calkins CC. Platt K. Potempa J. Travis J. 1998 Inactivation of tumor necrosis factor-alpha by proteinases (gingipains) from the periodontal pathogen, Porphyromonas gingivalis. Implications of immune evasion J Biol Chem 273 6611 6614
8. Chiu B. 1999 Multiple infections in carotid atherosclerotic plaques Am Heart J 138 S534 S536
9. Curtis MA. Macey M. Slaney JM. Howells GL. 1993 Platelet activation by protease I of Porphyromonas gingivalis W83 FEMS Microbiol Lett 110 167 173
10. Gibbons RJ. MacDonald JB. 1960 Hemin and vitamin K compounds as required factors for the cultivation of certain strains of Bacteroides melaninogenicus J Bacteriol 80 164 170
11. Han N. Whitlock J. Progulske-Fox A. 1996 The hemagglutinin gene A (hagA) of Porphyromonas gingivalis 381 contains four large, contiguous, direct repeats Infect Immun 64 4000 4007
12. Herzberg MC. MacFarlane GD. Liu P. Erickson PR. 1994 The platelet as an inflammatory cell in periodontal diseases: interancton with Porphyromonas gingivalis. In Molecular Pathogenesis of Periodontal Disease Genco R. (eds) Washington, DC American Society of Microbiology, pp. 247 255
13. Howell TH. Ridker PM. Ajani UA. Hennekens CH. Christen WG. 2001 Periodontal disease and risk of subsequent cardiovascular disease in US male physicians J Am Coll Cardiol 37 445 450
14. Hujoel PP. Drangsholt M. Spiekerman C. DeRouen TA. 2000 Periodontal disease and coronary heart disease risk JAMA 284 1406 1410
15. Iida Y. Honda K. Suzuki T. Matsukawa S. Kawai T. Shimahara T. Chiba H. 2004 Brain abscess in which Porphyromonas gingivalis was detected in cerebrospinal fluid Br J Oral Maxillofac Surg 42 180
16. Imamura T. Pike RN. Potempa J. Travis J. 1994 Pathogenesis of periodontitis: a major arginine-specific cysteine proteinase from Porphyromonas gingivalis induces vascular permeability enhancement through activation of the kallikrein/kinin pathway J Clin Invest 94 361 367
17. Imamura T. Potempa J. Tanase S. Travis J. 1997 Activation of blood coagulation factor X by arginine-specific cysteine proteinases (gingipain-Rs) from Porphyromonas gingivalis J Biol Chem 272 16062 16067
18. Jagels MA. Travis J. Potempa J. Pike R. Hugli TE. 1996 Proteolytic inactivation of the leukocyte C5a receptor by proteinases derived from Porphyromonas gingivalis Infect Immun 64 1984 1991
19. Joshipura KJ. Rimm EB. Douglass CW. Trichopoulos D. Ascherio A. Willett WC. 1996 Poor oral health and coronary heart disease J Dent Res 75 1631 1636
20. Kadowaki T. Yoneda M. Okamoto K. Maeda K. Yamamoto K. 1994 Purification and characterization of a novel arginine-specific cysteine proteinase (argingipain) involved in the pathogenesis of periodontal disease from the culture supernatant of Porphyromonas gingivalis J Biol Chem 269 21371 21378
21. Kadowaki T. Nakayama K. Yoshimura F. Okamoto K. Abe N. Yamamoto K. 1998 Arg-gingipain acts as a major processing enzyme for various cell surface proteins in Porphyromonas gingivalis J Biol Chem 273 29072 29076
22. Kamaguchi A. Ohyama T. Sakai E. Nakamura R. Watanabe T. Baba H. Nakayama K. 2003 Adhesins encoded by the gingipain genes of Porphyromonas gingivalis are responsible for co-aggregation with Prevotella intermedia Microbiology 149 1257 1264
23. Kariyazono H. Nakamura K. Shinkawa T. Yamaguchi T. Sakata R. Yamada K. 2001 Inhibition of platelet aggregation and the release of P-selectin from platelets by cilostazol Thromb Res 101 445 453
24. Kelly CG. Booth V. Kendal H. Slaney JM. Curtis MA. Lehner T. 1997 The relationship between colonization and haemagglutination inhibiting and B cell epitopes of Porphyromonas gingivalis Clin Exp Immunol 110 285 291
25. Kerrigan SW. Douglas I. Wray A. Heath J. Byrne MF. Fitzgerald D. Cox D. 2002 A role for glycoprotein Ib in Streptococcus sanguis-induced platelet aggregation Blood 100 509 516
26. Kozarov EV. Dorn BR. Shelburne CE. Dunn WA., Jr, Progulske-Fox A. 2005 Human atherosclerotic plaque contains viable invasive Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis Arterioscler Thromb Vasc Biol 25 e17 18. Epub 2005 January 20.
27. Lalla E. Lamster IB. Hofmann MA. Bucciarelli L. Jerud AP. Tucker S. et al. 2003 Oral infection with a periodontal pathogen accelerates early atherosclerosis in apolipoprotein E-null mice Arterioscler Thromb Vasc Biol 23 1405 1411
28. Lev M. Keudell KC. Milford AF. 1971 Succinate as a growth factor for Bacteroides melaninogenicus J Bacteriol 108 175 178
29. Li L. Messas E. Batista EL. Levine RA. Amar S. 2002 Porphyromonas gingivalis infection accelerates the progression of atherosclerosis in a heterozygous apolipoprotein E-deficient murine model Circulation 105 861 867
30. Lourbakos A. Yuan YP. Jenkins AL. Travis J. Andrade-Gordon P. Santulli R. et al. 2001 Activation of protease-activated receptors by gingipains from Porphyromonas gingivalis leads to platelet aggregation: a new trait in microbial pathogenicity Blood 97 3790 3797
31. Mattila KJ. Valtonen VV. Nieminen M. Huttunen JK. 1995 Dental infection and the risk of new coronary events: prospective study of patients with documented coronary artery disease Clin Infect Dis 20 588 592
32. Morrison HI. Ellison LF. Taylor GW. 1999 Periodontal disease and risk of fatal coronary heart and cerebrovascular diseases J Cardiovasc Risk 6 7 11
33. Murakami Y. Imai M. Nakamura H. Yoshimura F. 2002 Separation of the outer membrane and identification of major outer membrane proteins from Porphyromonas gingivalis Eur J Oral Sci 110 157 162
34. Nakayama K. Yoshimura F. Kadowaki T. Yamamoto K. 1996 Involvement of arginine-specific cysteine proteinase (Arg-gingipain) in fimbriation of Porphyromonas gingivalis J Bacteriol 178 2818 2824
35. Nakayama K. Ratnayake DB. Tsukuba T. Kadowaki T. Yamamoto K. Fujimura S. 1998 Haemoglobin receptor protein is intragenically encoded by the cysteine proteinase-encoding genes and the haemagglutinin-encoding gene of Porphyromonas gingivalis Mol Microbiol 27 51 61
36. Oleksy A. Banbula A. Bugno M. Travis J. Potempa J. 2002 Proteolysis of interleukin-6 receptor (IL-6R) by Porphyromonas gingivalis cysteine proteinases (gingipains) inhibits interleukin-6-mediated cell activation Microb Pathog 32 173 181
37. Rosenfeld SI. Looney RJ. Leddy JP. Phipps DC. Abraham GN. Anderson CL. 1985 Human platelet Fc receptor for immunoglobulin G. Identification as a 40 000-molecular-weight membrane protein shared by monocytes J Clin Invest 76 2317 2322
38. Sato K. Sakai E. Veith PD. Shoji M. Kikuchi Y. Yukitake H. et al. 2005 Identification of a new membrane-associated protein which influences transport/maturation of gingipains and adhesins of Porphyromonas gingivalis J Biol Chem 280 8668 8677
39. Scragg MA. Cannon SJ. Rangarajan M. Williams DM. Curtis MA. 1999 Targeted disruption of fibronectin-integrin interactions in human gingival fibroblasts by the RI protease of Porphyromonas gingivalis W50 Infect Immun 67 1837 1843
40. Sharma A. Novak EK. Sojar HT. Swank RT. Kuramitsu HK. Genco RJ. 2000 Porphyromonas gingivalis platelet aggregation activity: outer membrane vesicles are potent activators of murine platelets Oral Microbiol Immunol 15 393 396
41. Shen Y. Romo GM. Dong JF. Schade A. McIntire LV. Kenny D. et al. 2000 Requirement of leucine-rich repeats of glycoprotein (GP) Ibα for shear-dependent and static binding of von Willebrand factor to the platelet membrane GP Ib-IX-V complex Blood 95 903 910
42. Shi Y. Ratnayake DB. Okamoto K. Abe N. Yamamoto K. Nakayama K. 1999 Genetic analyses of proteolysis, hemoglobin binding, and hemagglutination of Porphyromonas gingivalis. Construction of mutants with a combination of rgpA, rgpB, kgp, and hagA J Biol Chem 274 17955 17960
43. Shi Y. Kong W. Nakayama K. 2000 Human lactoferrin binds and removes the hemoglobin receptor protein of the periodontopathogen Porphyromonas gingivalis J Biol Chem 275 30002 30008
44. Shibata Y. Hayakawa M. Takiguchi H. Shiroza T. Abiko Y. 1999 Determination and characterization of the hemagglutinin-associated short motifs found in Porphyromonas gingivalis multiple gene products J Biol Chem 274 5012 5020
45. Shoji M. Naito M. Yukitake H. Sato K. Sakai E. Ohara N. Nakayama K. 2004 The major structural components of two cell surface filaments of Porphyromonas gingivalis are matured through lipoprotein precursors Mol Microbiol 52 1513 1525
46. Sjöbring U. Ringdahl U. Ruggeri ZM. 2002 Induction of platelet thrombi by bacteria and antibodies Blood 100 4470 4477
47. Studier FW. Rosenberg AH. Dunn JJ. Dubendorff JW. 1990 Use of T7 RNA polymerase to direct expression of cloned genes Methods Enzymol 185 60 89
48. Sugawara S. Nemoto E. Tada H. Miyake K. Imamura T. Takada H. 2000 Proteolysis of human monocyte CD14 by cysteine proteinases (gingipains) from Porphyromonas gingivalis leading to lipopolysaccharide hyporesponsiveness J Immunol 165 411 418
49. Sullam PM. Hyun WC. Szollosi J. Dong J. Foss WM. Lopez JA. 1998 Physical proximity and functional interplay of the glycoprotein Ib-IX-V complex and the Fc receptor FcγRIIA on the platelet plasma membrane J Biol Chem 273 5331 5336
50. Taniguchi A. Nishimura F. Murayama Y. Nagasaka S. Fukushima M. Sakai M. et al. 2003 Porphyromonas gingivalis infection is associated with carotid atherosclerosis in non-obese Japanese type 2 diabetic patients Metabolism 52 142 145
51. Trinh S. Haggoud A. Reysset G. Sebald M. 1995 Plasmids pIP419 and pIP421 from Bacteroides: 5-nitroimidazole resistance genes and their upstream insertion sequence elements Microbiology 141 927 935
52. Ward CM. Andrews RK. Smith AI. Berndt MC. 1996 Mocarhagin, a novel cobra venom metalloproteinase, cleaves the platelet von Willebrand factor receptor glycoprotein Ibα. Identification of the sulfated tyrosine/anionic sequence Tyr-276-Glu-282 of glycoprotein Ibα as a binding site for von Willebrand factor and α-thrombin Biochemistry 35 4929 4938
53. Wingrove JA. DiScipio RG. Chen Z. Potempa J. Travis J. Hugli TE. 1992 Activation of complement components C3 and C5 by a cysteine proteinase (gingipain-1) from Porphyromonas (Bacteroides) gingivalis J Biol Chem 267 18902 18907
54. Wu Y. Suzuki-Inoue K. Satoh K. Asazuma N. Yatomi Y. Berndt MC. Ozaki Y. 2001 Role of Fc receptor γ-chain in platelet glycoprotein Ib-mediated signaling Blood 97 3836 3845
55. Yoneda M. Hirofuji T. Anan H. Matsumoto A. Hamachi T. Nakayama K. Maeda K. 2001 Mixed infection of Porphyromonas gingivalis and Bacteroides forsythus in a murine abscess model: involvement of gingipains in a synergistic effect J Periodontal Res 36 237 243