The potential role of α2-macroglobulin in the control of cysteine proteinases (gingipains) from Porphyromonas gingivalis

Journal of Periodontal Research

Volumn 32, Issue 1 PART 1, 1997, Pages 61-68

  Gron H ^a   Pike, R ^b   Potempa, J ^c   Travis, J ^b   Thogersen I B ^a   Enghild, J J ^a   Pizzo, S V ^a,d  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c JAGIELLONIAN UNIVERSITY   (Poland)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Gingipain; Periodontitis; Porphyromonas gingivalis; 2 macroglobulin

Indexed keywords

ADHESIN; ALPHA 2 MACROGLOBULIN; ARGINGIPAIN, PORPHYROMONAS GINGIVALIS; BACTERIAL PROTEIN; CYSTEINE PROTEINASE; HEMAGGLUTININ; LYS GINGIPAIN; LYS-GINGIPAIN; PROTEINASE INHIBITOR;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; DRUG ANTAGONISM; ENZYMOLOGY; HUMAN; METABOLISM; MOLECULAR GENETICS; PORPHYROMONAS GINGIVALIS; RAT;

ADHESINS, BACTERIAL; ALPHA-MACROGLOBULINS; AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; CYSTEINE ENDOPEPTIDASES; HEMAGGLUTININS; HUMANS; MOLECULAR SEQUENCE DATA; PORPHYROMONAS GINGIVALIS; PROTEASE INHIBITORS; RATS;

EID: 0003054849     PISSN: 00223484     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0765.1997.tb01383.x     Document Type: Article

References (70)

1. Slots J, Listgarten MA. Bacteroides gingivalis, Bacteroides intermedius and Actinobacillus actinomycetemcomitans in human periodontal diseases. J Clin Periodont 1988; 15: 85-93.
2. Slots J, Bragd L, Wikström M, Dahlén G. The occurrence of Actinobacillus actinomycetemcomitans, Bacteroides gingivalis and Bacteroides intermedius in destructive periodontal disease in adults J Clin Periodont 1986; 13: 570-577.
3. Holt SC, Ebersole J, Felton J, Brunsvold M, Kornmann KS. Implantation of Bacteroides gingivalis in nonhuman primates initiates progression of periodontitis. Science 1988; 239: 55-57.
4. Lamster IB, Smith QT, Celenti RS, Singer RE, Grbic JT. Development of a risk profile for periodontal disease: microbial and host responce factors. J Periodontol 1994; 65: 511-520.
5. Mayrand D, Holt SC. Biology of asaccharolytic black-pigmented Bacteroides species. Microbiol Rev 1988; 52: 134-152.
6. Birkedal-Hansen H, Taylor RE, Zambon JJ, Barwa PK, Neiders ME. Characterization of collagenolytic activity from strains of Bacteroides gingivalis. J Periodont Res 1988; 23: 258-264.
7. Wikström M, Linde A. Ability of oral bacteria to degrade fibronectin. Infect Immun 1986; 51: 707-711.
8. Lantz MS, Allen RD, L. W. Duck LW, Blume JL, L. Switalski LM, Höök M. Identification of Porphyromonas gingivalis components that mediate its interactions with fibronectin. J Bacteriol 1991; 173: 4263-4270.
9. Kilian M. Degradation of immunoglobulins A1, A2, and G by suspected principal periodontal pathogens. Infect Immun 1981; 34: 757-765.
10. Sundqvist G, Carlsson J, Herrmann B, Tarnvik A. Degradation of human immunoglobulins G and M and complement factors C3 and C5 by black-pigmented Bacteroides. J Med Microbiol 1985; 19: 85-94.
11. . Schenkein HA. The effect of periodontal proteolytic Bacteroides species on proteins of the human complement system. J Periodont Res 1988; 23: 187-192.
12. Otsuka M, Endo J, Hinode D, et al. Isolation and characterization of protease from culture supernatant of Bacteroides gingivalis. J Periodont Res 1987; 22: 491-498.
13. Odell EW, Wu PJ. Susceptibility of Porphyromonas gingivalis and P. asaccharolytica to the non-oxidative killing mechanisms of human neutrophils. Arch Oral Biol 1992; 37: 597-601.
14. Carlsson J, Höfling JF, Sundqvist GK. Degradation of albumin, haemopexin, haptoglobin and transferrin, by black-pigmented Bacteroides species. J Med Microbiol 1984; 18: 39-46.
15. Wikström MB, Dahlén G, Linde A. Fibrinogenolytic and fibrinolytic activity in oral microorganisms. J Clin Microbiol 1983; 17: 759-767.
16. Lantz MS, Rowland RW, Switalski LM, Höök M. Interactions of Bacteroides gingivalis with fibrinogen. Infect Immun 1986; 54: 654-658.
17. Nilsson T, Carlsson J, Sundqvist G. Inactivation of key factors of the plasma proteinase cascade systems by Bacteroides gingivalis. Infect Immun 1985; 50: 467-471.
18. Carlsson J, Herrmann BF, Höfling JF, Sundqvist GK. Degradation of the human proteinase inhibitors alpha-1-antitrypsin and alpha-2-macroglobulin by Bacteroides gingivalis. Infect Immun 1984; 43: 644-648.
19. Potempa J, Pike R, Travis J. Host and Porphyromonas gingivalis proteinases in periodontitis: a biochemical model of infection and tissue destruction. Perspec Drug Discovery Design 1995; 2: 445-458.
20. Potempa J, Pike R, Travis J. The multiple forms of trypsin-like activity present in various strains of Porphyromonas gingivalis are due to the presence of either Arg-gingipain or Lys-gingipain. Infect Immun 1995; 63: 1176-1182.
21. 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.
22. Shah HN, Gharbia SE, Kowlessur D, Wilkie E, Brocklehurst K. A cysteine proteinase isolated from Porphyromonas gingivalis. Microbiol Ecol Health Dis 1991; 4: 319-328.
23. Scott CF, Whitaker EJ, Hammond BF, Colman RW. Purification and characterization of a potent 70-kDa thiol lysyl-proteinase (Lys-gingivain) from Porphyromonas gingivalis that cleaves kininogens and fibrinogen. J Biol Chem 1993; 268: 7935-7942.
24. Ciborowski P, Nishikata M, Allen RD, Lantz MS. Purification and characterization of two forms of a high-molecular-weight cysteine proteinase (porphypain) from Porphyromonas gingivalis. J Bacteriol 1994; 176: 4549-4557.
25. Kadowaki T, Yoneda M, Okamoto K, Maeda K, Yamamoto K. Purification and characterization of a novel arginine-specific cysteine proteinase (argingipain) involved in the pathogenesis of perodontal disease from the culture supernatant of Porphyromonas gingivalis. J Biol Chem 1994; 269: 21371-21378.
26. Pike R, McGraw W, Potempa J, Travis J. Lysine- and arginine-specific proteinases from Porphyromonas gingivalis. Isolation, characterization, and evidence for the existence of complexes with hemagglutinins. J Biol Chem 1994; 269: 406-411.
27. Wingrove JA, DiScipio RG, Chen Z, Potempa J, Travis J, Hugli TE. Activation of complement components C3 and C5 by a cysteine proteinase (Gingipain-1) from Porphyromonas (Bacteroides) gingivalis. J Biol Chem 1992; 267: 18902-18907.
28. Schenkein HA, Fletcher HM, Bodnar M, Macrina FL. Increased opsonization of a prtH-defective mutant of Porphyromonas gingivalis W83 is caused by reduced degradation of complement-derived opsonins. J Immunol 1995; 154: 5331-5337.
29. Lala A, Amano A, Sojar HT, Radel SJ, DeNardin E. Porphyromonas gingivalis trypsin-like protease: a possible natural ligand for the neutrophil formyl peptide receptor. Biochem Biophys Res Commun 1994; 199: 1489-1496.
30. Nakayama K, Kadowaki T, Okamoto K, Yamamoto K. Construction and characterization of arginine-specific cysteine proteinase (Arg-gingipain)-deflcient mutants of Porphyromonas gingivalis. Evidence for significant contribution of Arg-gingipain to virulence. J Biol Chem 1995; 270: 23619-23626.
31. Imamura T, Potempa J, Pike R, Moore JN, Barton MH, Travis J. Effect of free and vesicle-bound cysteine proteinases of Porphyromonas gingivalis on plasma clot formation: implications for bleeding tendency at periodontitis sites. Infect Immun 1995; 63: 4877-4882.
32. Imamura T, Pike RN, Potempa J, Travis J. 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 1994; 94: 361-367.
33. Imamura T, Potempa J, Pike RN, Travis J. Dependence of vascular permeability enhancement on cysteine proteinases in vesicles of Porphyromonas gingivalis. Infect Immun 1995; 63: 1999-2003.
34. Smalley JW, Birss, AJ, Kay HM, McKee AS, Marsh PD. The distribution of trypsin-like enzyme activity in cultures of a virulent and an avirulent strains of Bacteroides gingivalis W50. Oral Microbiol Immunol 1989; 4: 178-181.
35. Fletcher HM, Schenkein HA, Morgan RM, Bailey KA, Berry CR, Macrina FL. Virulence of a Porphyromonas gingivalis W83 mutant defective in the prtH gene. Infect Immun 1995; 63: 1521-1528.
36. Rubenstein DS, Thøgersen IB, Pizzo SV, Enghild JJ. Identification of monomeric α-macroglobulin proteinase inhibitors in birds, reptiles, amphibians and mammals, and purification and characterization of a monomeric α-macroglobulin proteinase inhibitor from the American bullfrog Rana catesbiana. Biochem J 1993; 290: 85-95.
37. 2-macroglobulin receptor. Biochemistry 1986; 25: 721-727.
38. 2-macroglobulin: structure-function and the ancient thiol ester bond. Ann NY Acad Sci 1994; 712: 131-145.
39. Rubenstein DS, Enghild JJ, Pizzo SV. Limited proteolysis of the α-macroglobulin rat α1-inhibitor-3: implications for a domain structure. J Biol Chem 1991; 266: 11252-11261.
40. 2-Macroglobulin. Methods Enzymol 1981; 80: 737-754.
41. Thøgersen IB, Salvesen G, Brucato FH, Pizzo SV, Enghild JJ. Purification and characterization of an α-macroglobulin proteinase inhibitor from the mollusc Octopus vulgaris. Biochem J 1992; 285: 521-527.
42. 2-Macroglobulin and related thiol ester plasma proteins. In: Putman FW, ed. The plasma proteins: structure, function, and genetic control. Orlando, FL: Academic Press, 1987; 191-291
43. Sottrup-Jensen L, Sand O, Kristensen L, Fey GH. The α-macroglobulin bait region: sequence diversity and localization of cleavage sites for proteinases in five mammalian α-macroglobulins. J Biol Chem 1989; 264: 15781-15789.
44. 2-macroglobun with proteinases: characteristics and specificity of the reaction, and a hypothesis concerning its molecular mechanism. Biochem J 1973; 133: 709-724.
45. Salvesen G, Enghild JJ. α-Macroglobulins: detection and characterization. Methods Enzymol 1993; 223: 121-141.
46. 2-Macroglobulin, complement and biological defense: antigens, growth factors, microbial proteases, and receptor ligation. Lab Invest 1994; 71: 792-812.
47. Chen Z, Potempa J, Polanowski A, Wikström M, Travis J. Purification and characterization of a 50-kDa cysteine proteinase (gingipain) from Porphyromonas gingivalis. J Biol Chem 1992; 267: 18896-18901.
48. Wikström M, Potempa J, Polanowski A, Travis J, Renvert S. Detection of Porphyromonas gingivalis in gingival exudate by a dipeptide-enhanced trypsin-like activity. J Periodontol 1994; 65: 47-55.
49. Sibraa PD, Reinhardt RA, Dyer JK, DuBois LM. Acute-phase protein detection and quantification in gingival crevicular fluid by direct and indirect immunodot. J Clin Periodontol 1991; 18: 101-106.
50. Skaleric U, Zajsek P, Cvetko E, Lah T, Babnik J. Alpha-2-macroglobulin in gingival fluid: correlation with alveolar bone loss in periodontal disease. J Clin Periodontol 1986; 13: 833-836.
51. Enghild JJ, Salvesen G, Thøgersen IB, Pizzo SV. Proteinase binding and inhibition by the monomeric α-macroglobulin rat α1-inhibitor-3. J Biol Chem 1989; 264: 11428-11435.
52. 2-macroglobulin: implications for the study of peptide and growth factor binding. Biochemistry 1991; 30: 1551-1560.
53. Habeeb AFSA. Reaction of protein sulphydryl groups with Ellman's reagent. Methods Enzymol 1972; 25: 457-464.
54. Hall PK, Roberts RC. Physical and chemical properties of human plasma α2-macroglobulin. Biochem J 1978; 173: 27-38.
55. Esnard F, Gauthier F. Purification and physiochemical characterization of a new rat plasma proteinase inhibitor, alpha 1-inhibitor III. Biochim Biophys Acta 1980; 614: 553-563.
56. Bury AF. Analysis of protein and peptide mixtures: evaluation of three sodium dodecyl sulphate-polyacrylamide gel electrophoresis buffer systems. J Chromatogr 1981; 213: 491-500.
57. Salvesen G, Nagase H. Inhibition of proteolytic enzymes. In: Beyton RJ, Bond JS, eds. Proteolytic enzymes a practical approach. Oxford: IRL Press, 1989; 83-104.
58. Enghild JJ, Thøgersen IB, Salvesen G, et al. α-Macroglobulin from Limulus polyphemus exhibits proteinase hibitory activity and participates in a hemolytic system. Biochemistry 1990; 29: 10070-10080.
59. 2-macroglobulin subunits. J Biol Chem 1979; 254: 4452-4456.
60. 2-macroglobulin. J Biol Chem 1979; 254: 8669-8678.
61. 2-macroglobulin without hydrolysis of the internal thiolesters or expression of the receptor recognition site. J Biol Chem 1988; 263: 468-473.
62. 2-macroglobulin Isolation after limited proteolysis with a bacterial proteinase. J Biol Chem 1986; 261: 11369-11373.
63. 2-macroglobulin molecule. Biochem J 1979; 181: 401-418.
64. 2-macroglobulin. Biochem J 1995; 312: 191-195.
65. Sengupta S, Lamster IB, Khocht A, Duffy TA, Gordon JM. The effect of treatment on IgG, IgA, IgM and α-2-macroglobulin in gingiva crevicular fluid from patients with chronic adult periodontitis. Arch Oral Biol 1988; 33: 425-431.
66. Rosin M, Benjamin P, Rogers P, et al. Elevated conversion of alpha-2-macroglobulin to the complex form in gingival crevicular fluid from adult periodontitis patients. J Periodont Res 1995; 30: 436-444.
67. 2-macroglobulin in biological fluids using a sandwich immunoassay. J Immunol Methods 1990; 126: 13-20
68. 2-macroglobulin-proteinase interactions. Studies with trypsin and plasmin. Biochemistry 1984; 23: 6619-6626.
69. 2-macroglobulin and chicken ovostatin: binding kinetics and identification of matrix metalloproteinase cleavage sites. J Biol Chem 1989; 264: 8779-8785.
70. Sottrup-Jensen L, Birkedal-Hansen H. Human fibroblast collagenase-α-macroglobulin interactions. Localization of cleavage sites in the bait regions of five mammalian α-macroglobulins. J Biol Chem 1989; 264: 393-401.