Acquisition of complement inhibitor serine protease factor i and its cofactors C4b-binding protein and factor H by prevotella intermedia

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Malm, Sven ^a   Jusko, Monika ^a   Eick, Sigrun ^b   Potempa, Jan ^c,d   Riesbeck, Kristian ^a   Blom, Anna M ^a  

^a LUND UNIVERSITY HOSPITAL   (Sweden)

^b UNIVERSITY OF BERN   (Switzerland)

^c JAGIELLONIAN UNIVERSITY   (Poland)

^d UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3B; COMPLEMENT COMPONENT C4B BINDING PROTEIN; COMPLEMENT FACTOR H; SERINE PROTEINASE; COMPLEMENT FACTOR I;

ARTICLE; BACTERIUM ISOLATE; CONTROLLED STUDY; ENZYME ACTIVITY; GRAM NEGATIVE INFECTION; NONHUMAN; PERIODONTITIS; PREVOTELLA INTERMEDIA; PROTEIN BINDING; PROTEIN DEGRADATION; RHEUMATOID ARTHRITIS; HUMAN; METABOLISM;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PREVOTELLA INTERMEDIA;

COMPLEMENT C4B-BINDING PROTEIN; COMPLEMENT FACTOR H; COMPLEMENT FACTOR I; HUMANS; PREVOTELLA INTERMEDIA; PROTEIN BINDING;

EID: 84859718234     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034852     Document Type: Article

References (50)

1. Darby I, Curtis M, (2001) Microbiology of periodontal disease in children and young adults. Periodontol 2000 26: 33-53.
2. Pihlstrom BL, Michalowicz BS, Johnson NW, (2005) Periodontal diseases. Lancet 366: 1809-1820.
3. Genco RJ, van Dyke TE, (2010) Prevention: Reducing the risk of CVD in patients with periodontitis. Nat Rev Cardiol 7: 479-480.
4. Marcelino SL, Gaetti-Jardim E Jr, Nakano V, Canonico LA, Nunes FD, et al. (2010) Presence of periodontopathic bacteria in coronary arteries from patients with chronic periodontitis. Anaerobe 16: 629-632.
5. Martinez-Martinez RE, Abud-Mendoza C, Patino-Marin N, Rizo-Rodriguez JC, Little JW, et al. (2009) Detection of periodontal bacterial DNA in serum and synovial fluid in refractory rheumatoid arthritis patients. J Clin Periodontol 36: 1004-1010.
6. de Pablo P, Dietrich T, McAlindon TE, (2008) Association of periodontal disease and tooth loss with rheumatoid arthritis in the US population. J Rheumatol 35: 70-76.
7. Ricklin D, Hajishengallis G, Yang K, Lambris JD, (2010) Complement: a key system for immune surveillance and homeostasis. Nat Immunol 11: 785-797 doi:10.1038/ni.1923.
8. Blom AM, Villoutreix BO, Dahlback B, (2004) Complement inhibitor C4b-binding protein-friend or foe in the innate immune system? Mol Immunol 40: 1333-1346.
9. de Cordoba SR, de Jorge EG, (2008) Translational mini-review series on complement factor H: genetics and disease associations of human complement factor H. Clin Exp Immunol 151: 1-13.
10. Catterall CF, Lyons A, Sim RB, Day AJ, Harris TJ, (1987) Characterization of primary amino acid sequence of human complement control protein factor I from an analysis of cDNA clones. Biochem J 242: 849-856.
11. Dahlback B, (1983) Purification of human C4b-binding protein and formation of its complex with vitamin K-dependent protein S. Biochem J 209: 847-856.
12. Boon CJ, van de Kar NC, Klevering BJ, Keunen JE, Cremers FP, et al. (2009) The spectrum of phenotypes caused by variants in the CFH gene. Mol Immunol 46: 1573-1594.
13. Schenkein HA, Genco RJ, (1977) Gingival fluid and serum in periodontal diseases. I. Quantitative study of immunoglobulins, complement components, and other plasma proteins. J Periodontol 48: 772-777.
14. Boackle RJ, (1991) The Interaction of Salivary Secretions with the Human Complement System - A Model for the Study of Host Defense Systems on Inflamed Mucosal Surfaces. Critical Reviews in Oral Biology & Medicine 2: 355-367.
15. Blom AM, Hallstrom T, Riesbeck K, (2009) Complement evasion strategies of pathogens-acquisition of inhibitors and beyond. Mol Immunol 46: 2808-2817.
16. Ferreira VP, Pangburn MK, Cortes C, (2010) Complement control protein factor H: the good, the bad, and the inadequate. Mol Immunol 47: 2187-2197.
17. Asakawa R, Komatsuzawa H, Kawai T, Yamada S, Goncalves RB, et al. (2003) Outer membrane protein 100, a versatile virulence factor of Actinobacillus actinomycetemcomitans. Mol Microbiol 50: 1125-1139.
18. Potempa M, Potempa J, Okroj M, Popadiak K, Eick S, et al. (2008) Binding of complement inhibitor C4b-binding protein contributes to serum resistance of Porphyromonas gingivalis. J Immunol 181: 5537-5544.
19. McDowell JV, Huang B, Fenno JC, Marconi RT, (2009) Analysis of a unique interaction between the complement regulatory protein factor H and the periodontal pathogen Treponema denticola. Infect Immun 77: 1417-1425.
20. Hair PS, Echague CG, Sholl AM, Watkins JA, Geoghegan JA, et al. (2010) Clumping factor A interaction with complement factor I increases C3b cleavage on the bacterial surface of Staphylococcus aureus and decreases complement-mediated phagocytosis. Infect Immun 78: 1717-1727.
21. Hair PS, Ward MD, Semmes OJ, Foster TJ, Cunnion KM, (2008) Staphylococcus aureus clumping factor A binds to complement regulator factor I and increases factor I cleavage of C3b. J Infect Dis 198: 125-133.
22. Cunnion KM, Buescher ES, Hair PS, (2005) Serum complement factor I decreases Staphylococcus aureus phagocytosis. J Lab Clin Med 146: 279-286.
23. Frandsen EV, Poulsen K, Kilian M, (1995) Confirmation of the species Prevotella intermedia and Prevotella nigrescens. Int J Syst Bacteriol 45: 429-435.
24. Nordstrom T, Blom AM, Forsgren A, Riesbeck K, (2004) The emerging pathogen Moraxella catarrhalis interacts with complement inhibitor C4b binding protein through ubiquitous surface proteins A1 and A2. J Immunol 173: 4598-4606.
25. Aduse-Opoku J, Davies NN, Gallagher A, Hashim A, Evans HEA, et al. (2000) Generation of Lys-gingipain protease activity in Porphyromonas gingivalis W50 is independent of Arg-gingipain protease activities. Microbiology 146: 1933-1940.
26. Sztukowska M, Sroka A, Bugno M, Banbula A, Takahashi Y, et al. (2004) The C-terminal domains of the gingipain K polyprotein are necessary for assembly of the active enzyme and expression of associated activities. Mol Microbiol 54: 1393-1408.
27. Feng H, Xiang H, Zhang J, Liu G, Guo N, et al. (2009) Genome-wide transcriptional profiling of the response of Staphylococcus aureus to cryptotanshinone. J Biomed Biotechnol 2009: 617509.
28. Monecke S, Slickers P, Ehricht R, (2008) Assignment of Staphylococcus aureus isolates to clonal complexes based on microarray analysis and pattern recognition. FEMS Immunol Med Microbiol 53: 237-251.
29. Wann ER, Gurusiddappa S, Hook M, (2000) The fibronectin-binding MSCRAMM FnbpA of Staphylococcus aureus is a bifunctional protein that also binds to fibrinogen. J Biol Chem 275: 13863-13871.
30. Horstmann RD, Sievertsen HJ, Knobloch J, Fischetti VA, (1988) Antiphagocytic activity of streptococcal M protein: selective binding of complement control protein factor H. Proc Natl Acad Sci U S A 85: 1657-1661.
31. Friberg N, Carlson P, Kentala E, Mattila PS, Kuusela P, et al. (2008) Factor H Binding as a Complement Evasion Mechanism for an Anaerobic Pathogen, Fusobacterium necrophorum. J Immunol 181: 8624-8632.
32. Blom AM, Kask L, Dahlback B, (2003) CCP1-4 of the C4b-binding protein alpha-chain are required for factor I mediated cleavage of complement factor C3b. Mol Immunol 39: 547-556.
33. Crossley LG, Porter RR, (1980) Purification of the human complement control protein C3b inactivator. Biochem J 191: 173-182.
34. Nilsson SC, Karpman D, Vaziri-Sani F, Kristoffersson AC, Salomon R, et al. (2007) A mutation in factor I that is associated with atypical hemolytic uremic syndrome does not affect the function of factor I in complement regulation. Mol Immunol 44: 1835-1844.
35. Greenwood FC, Hunter WM, Glover JS, (1963) The preparation of 131I-labelled human growth hormone of high specific radioactivity. Biochem J 89: 114-123.
36. Dieudonne-Vatran A, Krentz S, Blom AM, Meri S, Henriques-Normark B, et al. (2009) Clinical isolates of Streptococcus pneumoniae bind the complement inhibitor C4b-binding protein in a PspC allele-dependent fashion. J Immunol 182: 7865-7877.
37. Potempa M, Potempa J, Kantyka T, Nguyen K-A, Wawrzonek K, et al. (2009) Interpain A, a Cysteine Proteinase from Prevotella intermedia, Inhibits Complement by Degrading Complement Factor C3. PLoS Pathog 5 doi:10.1371/journal.ppat.1000316.
38. Cunnion KM, Hair PS, Buescher ES, (2004) Cleavage of complement C3b to iC3b on the surface of Staphylococcus aureus is mediated by serum complement factor I. Infect Immun 72: 2858-2863.
39. Cunnion KM, Lee JC, Frank MM, (2001) Capsule Production and Growth Phase Influence Binding of Complement to Staphylococcus aureus. Infect Immun 69: 6796-6803.
40. Grenier D, Michaud J, (1994) Demonstration of human immunoglobulin G Fc-binding activity in oral bacteria. Clin Diagn Lab Immunol 1: 247-249.
41. Labbé S, Grenier D, (1995) Characterization of the human immunoglobulin G Fc-binding activity in Prevotella intermedia. Infect Immun 63: 2785-2789.
42. Okuda K, Adachi M, Iijima K, (1998) The efficacy of antimicrobial mouth rinses in oral health care. Bull Tokyo Dent Coll 39: 7-14.
43. Popadiak K, Potempa J, Riesbeck K, Blom AM, (2007) Biphasic Effect of Gingipains from Porphyromonas gingivalis on the Human Complement System. J Immunol 178: 7242-7250.
44. Wingrove JA, DiScipio RG, Chen Z, Potempa J, Travis J, et al. (1992) Activation of complement components C3 and C5 by a cysteine proteinase (gingipain-1) from Porphyromonas (Bacteroides) gingivalis. J Biol Chem 267: 18902-18907.
45. Guo Y, Nguyen K-A, Potempa J, (2010) Dichotomy of gingipains action as virulence factors: from cleaving substrates with the precision of a surgeon's knife to a meat chopper-like brutal degradation of proteins. Periodontol 2000 54: 15-44.
46. Krauss JL, Potempa J, Lambris JD, Hajishengallis G, (2010) Complementary Tolls in the periodontium: How periodontal bacteria modify complement and Toll-like receptor responses to prevail in the host. Periodontol 2000 52: 141-162.
47. Agarwal V, Asmat TM, Luo S, Jensch I, Zipfel PF, et al. (2010) Complement regulator Factor H mediates a two-step uptake of Streptococcus pneumoniae by human cells. J Biol Chem 285: 23486-23495.
48. Hamad OA, Nilsson PH, Lasaosa M, Ricklin D, Lambris JD, et al. (2010) Contribution of Chondroitin Sulfate A to the Binding of Complement Proteins to Activated Platelets. PLoS ONE 5: e12889 doi:10.1371/journal.pone.0012889.
49. Hessing M, Vlooswijk RA, Hackeng TM, Kanters D, Bouma BN, (1990) The localization of heparin-binding fragments on human C4b-binding protein. J Immunol 144: 204-208.
50. Meri S, Pangburn MK, (1994) Regulation of alternative pathway complement activation by glycosaminoglycans: specificity of the polyanion binding site on factor H. Biochem Biophys Res Commun 198: 52-59.