Activation of protease-activated receptors by gingipains from Porphyromonas gingivalis leads to platelet aggregation: A new trait in microbial pathogenicity

Blood

Volumn 97, Issue 12, 2001, Pages 3790-3797

  Lourbakos, Afrodite ^a,b,c,d,e   Yuan, YuPing ^a,b,c,d,e   Jenkins, Alison L ^a,b,c,d,e   Travis, James ^a,b,c,d,e   Andrade Gordon, Patricia ^a,b,c,d,e   Santulli, Rosemary ^a,b,c,d,e   Potempa, Jan ^a,b,c,d,e   Pike, Robert N ^a,b,c,d,e  

^a MONASH UNIVERSITY   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c RW Johnson Pharmaceutical Research Institute ^*  (United States)

^d R W JOHNSON PHARMACEUTICAL RES I   (United States)

^e JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE PROTEINASE; GINGIPAIN R; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 4; THROMBIN INHIBITOR;

ANIMAL CELL; ARTICLE; BACTERIAL VIRULENCE; BLOOD CLOTTING; CARDIOVASCULAR DISEASE; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; MOUSE; NONHUMAN; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; THROMBOCYTE AGGREGATION;

EID: 0035877969     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood.V97.12.3790     Document Type: Article

References (72)

1. Tansey WP. How cells use proteolysis to control their growth. Mol Med. 1999;5:773-782.
2. Peschon JJ, Slack JL, Reddy P, et al. An essential role for ectodomain shedding in mammalian development. Science. 1998;282:1281-1284.
3. Blasi F. Proteolysis, cell adhesion, chemotaxis, and invasiveness are regulated by the u-PA-u-PAR-PAI-1 system. Thromb Haemost. 1999;82:298-304.
4. Murphy G, Gavrilovic J. Proteolysis and cell migration: creating a path? Curr Opin Cell Biol. 1999;11:614-621.
5. Kiessling LL, Gordon EJ. Transforming the cell surface through proteolysis. Chem Biol. 1998;5: R49-R62.
6. Mullberg J, Althoff K, Jostock T, Rose-John S. The importance of shedding of membrane proteins for cytokine biology. Eur Cytokine Netw. 2000;11:27-38.
7. Schlondorff J, Blobel CP. Metalloprotease-disintegrins: modular proteins capable of promoting cell-cell interactions and triggering signals by protein-ectodomain shedding. J Cell Sci. 1999;112:3603-3617.
8. Coughlin SR. How the protease thrombin talks to cells. Proc Natl Acad Sci U S A. 1999;96:11023-11027.
9. Ijiri Y, Matsumoto K, Kamata R, et al. Suppression of polymorphonuclear leucocyte chemotaxis by Pseudomonas aeruginosa elastase in vitro: a study of the mechanisms and the correlation with ring abscess in pseudomonal keratitis. Int J Exp Pathol. 1994;75:441-451.
10. Vollmer P, Walev I, Rose-John S, Bhakdi S. Novel pathogenic mechanism of microbial metalloproteases: liberation of membrane-anchored molecules in biologically active form exemplified by studies with the human interleukin-6 receptor. Infect Immun. 1996;64:3646-3651.
11. Wolf BB, Gibson CA, Kapur V, et al. Proteolytically active streptococcal pyrogenic exotoxin B cleaves monocytic cell urokinase receptor and releases an active fragment of the receptor from the cell surface. J Biol Chem. 1994;269:30682-30687.
12. Lala A, Amano A, Sojar HT, et al. Porphyromonas gingivalistrypsin-like protease: a possible natural ligand for the neutrophil formyl peptide receptor. Biochem Biophys Res Commun. 1994;199:1489-1496.
13. Jagels MA, Travis J, Potempa J, et al. Proteolytic inactivation of the leukocyte C5a receptor by proteases derived from Porphyromonas gingivalis. Infect Immun. 1996;64:1984-1991.
14. Lourbakos A, Chinni C, Thompson P, et al. Cleavage and activation of protease-activated receptor-2 on human neutrophils by gingipain-R from Porphyromonas gingivalis. FEBS Lett. 1998;435:45-48.
15. Scragg MA, Cannon SJ, Rangarajan M, et al. Targeted disruption of fibronectin-integrin interactions in human gingival fibroblasts by the RI protease of Porphyromonas gingivalis W50. Infect Immun. 1999;67:1837-1843.
16. Katz J, Sambandam V, Wu JH, et al. Characterization of Porphyromonas gingivalis-induced degradation of epithelial cell junctional complexes. Infect Immun. 2000;68:1441-1449.
17. Sugawara S, Nemoto E, Tada H, et al. Proteolysis of human monocyte CD14 by cysteine proteases (gingipains) from Porphyromonas gingivalis leading to lipopolysaccharide hyporesponsiveness. J Immunol. 2000;165:411-418.
18. Offenbacher S, Lieff S, Beck JD. Periodontitis-associated pregnancy complications. Prenat Neonat Med. 1999;3:82-85.
19. Beck J, Garcia R, Heiss G, et al. Periodontal disease and cardiovascular disease. J Periodontol. 1996;67:1123-1137.
20. Page RC. The pathobiology of periodontal diseases may affect systemic diseases: inversion of a paradigm. Ann Periodontol. 1998;3:108-120.
21. Schenkein H. The pathogenesis of periodontal diseases. J Periodontol. 1999;70:457-470.
22. Newman MG. Periodontal diseases: pathogenesis and microbial factors: consensus report of the world workshop in periodontitis. Ann Periodontol. 1996;1:926-932.
23. Haffajee AD, Socransky SS. Microbial etiological agents of destructive periodontal diseases. Periodontology. 1994;5:78-111.
24. Holt SC, Felton J, Brunsvold M, et al. Implantation of Bacterioides gingivalis in non-human primates initiates progression of periodontitis. Science. 1987;239:55-57.
25. Mattila KJ. Viral and bacterial infections in patients with acute myocardial infarction. J Intern Med. 1989;225:293-296.
26. Mattila K, Niemen M, Valtonen V, et al. Association between dental health and acute myocardial infarction. Br Med J. 1989;298:779-782.
27. Mattila K, Valle MS, Niemen M, et al. Dental infections and coronary atherosclerosis. Atherosclerosis. 1993;103:205-211.
28. DeStefano F, Anda RF, Kahn HS, et al. Dental disease and risk of coronary heart disease and mortality. Br Med J. 1993;306:688-691.
29. Mattila K, Niemen M, Valtonen VV, et al. Dental infection and the risk of new coronary events: prospective study of patients with documented coronary artery disease. Clin Infect Dis. 1995;20:558-592.
30. Watanakunakorn C, Pantelakakis J. Alpha-hemolytic streptococcal bacteremia: a review of 203 episodes during 1980-1991. Scand J Infect Dis. 1993;25:403-408.
31. Silver JG, Martin AW, McBride BC. Experiment transient bacteremias in human subjects with varying degrees of plaque accumulation and gingival inflammation. J Clin Periodontol. 1980;4:92-99.
32. Carroll GC, Sebor RJ. Flossing and its relationship to transient bacteremia. J Periodontol. 1980;51:691-692.
33. Sconyers JR, Crawford JJ, Moriarty JD. Relationship of bacteremia to toothbrushing in patients with periodontitis. J Am Dent Assoc. 1973;87:616-692.
34. Haraszthy VI, Zambon M, Trevisan R, et al. Identification of pathogens in atheromatous plaques [abstract]. J Dent Res. 1998;77:666.
35. Chiu B. Multiple infections in carotid atherosclerotic plaques. Am Heart J. 2000;138:S534-S536.
36. Potempa J, Banbula A, Travis J. Role of bacterial proteases in matrix destruction and modulation of host responses. Periodontology 2000. 2000;24:153-192.
37. Pike R, McGraw W, Potempa J, Travis J. Lysine and arginine-specific proteases from Porphyromonas gingivalis: isolation, characterization, and evidence for the existence of complexes with hemagglutinins. J Biol Chem. 1994;269:406-411.
38. Potempa J, Mikolajczyk-Pawlinska J, Brassell D, et al. Comparative properties of two cysteine proteases (gingipains R), the products of two related but individual genes of Porphyromonas gingivalis. J Biol Chem. 1998;273:21648-21657.
39. Pike RN, Potempa J, McGraw W, et al. Characterization and binding activities of protease-adhesin complexes from Porphyromonas gingivalis. J Bacteriol. 1996;178:2876-2882.
40. Curtis MA, Macey JM, Slaney JM, et al. Platelet activation by protease I W83. FEMS Microbiol Lett. 1993;110:167-173.
41. Vu T-K, Hung DT, Wheaten VI, et al. Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell. 1991;64:1057-1068.
42. Ishihara H, Conolly AJ, Zeng D, et al. Protease-activated receptor 3 is a second thrombin receptor in humans. Nature. 1997;386:502-506.
43. Kahn ML, Zheng Y-W, Huang W, et al. A dual thrombin receptor system for platelet activation. Nature. 1998;394:690-694.
44. Xu W-F, Andersen H, Whitmore TE, et al. Cloning and characterization of human protease-activated receptor 4. Proc Natl Acad Sci U S A. 1998;95:6642-6646.
45. Hung DT, Vu TK, Wheaton VI, et al. Cloned platelet thrombin receptor is necessary for thrombin-induced platelet activation. J Clin Invest, 1992;89:1350-1353.
46. Vassallo RR Jr, Kieber-Emmons T, Cichowski K, et al. Structure-function relationships in the activation of platelet thrombin receptors by receptor-derived peptides. J Biol Chem. 1992;267:6081-6085.
47. Scarborough RM, Naughton MA, Teng W, et al, Tethered ligand agonist peptides: structural requirements for thrombin receptor activation reveal mechanism of proteolytic unmasking of agonist function. J Biol Chem. 1992;267:13146-13149.
48. Kahn ML, Nakanishi-Matsui M, Shapiro MJ, et al. Protease-activated receptors 1 and 4 mediate activation of human platelets by thrombin. J Clin Invest. 1999;103:879-887.
49. Jenkins AL, Bootman MD, Taylor CW, et al. Characterization of the receptor responsible for the thrombin-induced intracellular calcium responses in osteblast-like cells. J Biol Chem. 1993;168:21433-21437.
50. Darrow AL, Fang-Leung WP, Ye RD, et al. Biological consequences of thrombin receptor deficiency in mice. Thromb Haemost. 1996;76:860-866.
51. Andrade-Gordon P, Maryanoff BE, Derian BE, et al. Design, synthesis, and biological characterization of a peptide-mimetic antagonist for a tethered-ligand receptor. Proc Natl Acad Sci U S A. 1999;96:12257-12262.
52. 2+ mobilization from the intracellular stores of single histamine-stimulated HeLa cells. J Physiol. 1992;450:163-178.
53. Potempa J, Pike R, Travis J. Titration and mapping of the active site of cysteine proteases from Porphyromonas gingivalis (gingipains) using peptidyl chloromethanes. Biol Chem. 1997;378:223-230.
54. Covic L, Gresser AL, Kuliopulos A. Biphasic kinetics of activation and signaling for PAR1 and PAR4 thrombin receptors in platelets. Biochemistry. 2000;39:5458-5467.
55. Curtis MA, Ramakrishnan M, Slaney JM. Characterization of the trypsin-like enzymes of Porphyromonas gingivalis W83 using a radiolabelled active site-directed inhibitor. J Gen Microbiol. 1993;139:949-955.
56. Shi Y, Ratnayake DB, Okamoto K, et al. 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. 1999;274:17955-17960.
57. Herzberg MC. Platelet-streptococcal interactions in endocarditis. Crit Rev Oral Biol Med. 1996;7:222-236.
58. Vanags DM, Lloyd JV, Rodgers SE, et al. ADP, adrenaline and serotonin stimulate inositol 1,4,5-trisphosphate production in human platelets. Eur J Pharmacol. 1998;358:93-100.
59. Vu T-K, Wheaton VI, Hung DT, et al. Domains specifying thrombin-receptor interaction. Nature. 1991;353:674-677.
60. Liu L, Vu T-KH, Esmon CT, et al. The region of the thrombin receptor resembling hirudin binds to thrombin and alters enzyme specificity. J Biol Chem. 1991;266:16977-16980.
61. Imamura T, Potempa J, Tanase S, et al. Activation of blood coagulation factor X by arginine-specific cysteine proteases (gingipain-Rs) from Porphyromonas gingivalis. J Biol Chem. 1997;272:16062-16067.
62. Eichinger A, Beisel H-G, Jacob U, et al. Crystal structure of gingipain R: an Arg-specific bacterial cysteine protease with a caspase-like fold. EMBO J, 1999;18:5453-5462.
63. Covic L, Gresser AL, Kuliopulos A. Biphasic kinetics of activation and signaling for PAR1 and PAR4 thrombin receptors in platelets. Biochemistry. 2000;39:5458-5467.
64. Fox JEB. Regulation of platelet function by the cytoskeleton. In: Authi KS, ed. Mechanisms of Platelet Activation and Control. New York, NY: Plenum Press; 1993:175-185.
65. Loesche WJ. Periodontal disease as a risk factor for heart disease. Compend Contin Educ Dent. 1994;15:976-991.
66. Herzberg MC, Meyer M. Dental plaque, platelets, and cardiovascular disease. J Periodontol. 1998;3:151-160.
67. Joshipura KJ, Douglass CW, Willett WC. Possible explanations for the tooth loss and cardiovascular disease relationship. Ann Periodontol. 1998;3:175-183.
68. Lopes-Virella MF, Virella G. Immunological and microbiological factors in the pathogenesis of atherosclerosis. Clin Immunol Immunopathol. 1985;37:377-386.
69. Eley BM, Cox SW. Advances in periodontal diagnosis. 5. Potential inflammatory and immune markers. Br Dent J. 1998;184:220-223.
70. Lowe GDO, Kweider M, Murray GD, Kinane D, McGowan DA. Fibrinogen - a "new" cardiovascular risk factor. In: Ernst E, Koeinig W, Lowe GDO, Meade T, eds. Fibrinogen and Dental Disease - A Coronary Risk Factor. Oxford, United Kingdom: Blackwell-MZV Publications; 1992:187-191.
71. Kweider M, Lowe G, Murray G, et al. Dental disease, fibrinogen and white cell count: links with myocardial infarction? Scot Med J. 1993;38:73-74.
72. Mattila KJ, Rasi V, Niemen M. von Willebrand factor antigen and dental infections. Thromb Res. 1989;56:325-329.