Journal of Periodontal and Implant Science

Korean Academy of Periodontology (대한치주과학회)
권호 표지

Isolation and Partial Characterization of Hemin-binding Cell Envelope Proteins from Porphyromonas gingivalis, Prevotella intermedia, and Prevotella nigrescens

Porphyromonas gingivalis, Prevotella intermedia, 그리고 Prevotella nigrescens에서의 hemin 결합 단백질에 대한 연구

  • Kim, Sung-Jo (Department of Periodontology, School of Dentistry, Pusan National University)
  • 김성조 (부산대학교 치과대학 치주과학교실)
  • Published : 2006.03.30
Download PDF
⟨ Previous Next ⟩

Abstract

The results of this study confirm that the availability of hemin influences the expression of selected membrane proteins of Porphyromonas gingivalis, Prevotella intermedia, and Prevotella nigrescens. A 30 kDa (heated 24 kDa) hemin-binding protein whose expression is hemin regulated was identified and purified in P. gingivalis. A strong hemin-binding function was found by LDS-PAGE and TMBZ staining when P. gingivalis cells were grown under hemin-limited conditions. A 50 kDa cell envelope associated protein, whose expression is hemin regulated, is considered to be a putative hemin binding protein from P. intermedia and P. nigrescens, respectively. N-terminal amino acid sequence analysis of CNBr-digested 24 kDa hemin binding protein from P. gingivalis revealed that this protein belongs to a new, so far undescribed hemin-binding class of proteins. N-terminal amino acid sequence of a 50 kDa putative hemin binding protein from P. intermedia was identical with Enolase from Streptococcus intermedia. Work is in progress to further characterize the molecular structure of these proteins.

Keywords

References

  1. Bullen JJ. The significance of iron in infection. Rev Infect Dis 1981;3:1127-1138 https://doi.org/10.1093/clinids/3.6.1127
  2. Weinberg ED. Iron withholding: a de¬fense against infection and neoplasia. Physiol Rev 1984;64:65-102 https://doi.org/10.1152/physrev.1984.64.1.65
  3. Finkelstein RA, Sciortino CV. McIntosh MA. Role of iron in microbe-host interactions. Rev Infect Dis 1983;5:s759-s777 https://doi.org/10.1093/clinids/5.Supplement_4.S759
  4. Koskelo P, Muller Eberhard U. Interaction of porphyrins with proteins. Semin Hematol 1977;14:221-226
  5. Laurell CB, Gronvall C. Haptoglobins. Adv Clin Chem 1962;5:135-172
  6. Martinez JL, Delgado Iribarren A, Baquero F. Mechanisms of iron acquisition and bacterial virulence. FEMS Microbiol Rev 1990;75:45-56 https://doi.org/10.1111/j.1574-6968.1990.tb04085.x
  7. Muller Eberhard D, Morgan WT. Porphyrin-binding protein in serum. Ann NY Acad Sci 1975;244:624-649 https://doi.org/10.1111/j.1749-6632.1975.tb41558.x
  8. Seery VL, Muller Eberhard U. Binding of porphyrins to rabbit hemopexin and albumin. J Biol Chem 1973;248:3796-3800
  9. Eaton JW, Brandt, JR Mahoney. Haptoglobin: A natural bacteriostat. Science 1982;215:691-693 https://doi.org/10.1126/science.7036344
  10. Crosa JH. Genetics and molecular biology of siderophore-mediated iron transport in bacteria. Microbiol Lett 1989;53:517-530
  11. Schryvers AB, BC Lee. Comparative analysis of the transferrin and lactoferrin binding proteins in the family Neisseriaceae. Can J Microbiol 1989;35:409-415 https://doi.org/10.1139/m89-063
  12. Gonzalez GC, DI Caamano, AB Schryvers. Identification and characterization of a porcine-specific transferrin receptor in Actinobacillus pleuropneumoniae. Mol Microbiol 1990;4:1173-1179 https://doi.org/10.1111/j.1365-2958.1990.tb00692.x
  13. Yu R-H, SD Gray-Owen, J Ogunnariwo, AB Schryvers. Interraction of ruminant transferrin receptors in bovine isolates of Pasteurella haemolytica and Haemophilus somnus. Infect Immun 1992;60;2992-2994
  14. Schryvers AB, S Gray-Owen. Iron acquisition in Haemophilus influenzae receptors for human transferrin. J Infect Dis 1992;165:s103-s104 https://doi.org/10.1093/infdis/165-Supplement_1-S103
  15. Ogunnariwo JA, AB Schryvers. Correlation between the ability of Haemophilus paragallinarum to acquire ovotransferrin-bond iron and the expresssion of ovotransferrin-specific receptors. Avian Dis 1992;36:655-663 https://doi.org/10.2307/1591761
  16. Griffith E. The iron uptake systems of pathogenic bacteria. In: Bullen J. J. and Griffiths, E. eds. Iron and infection. New York: John Willey & Sons, 1987;69-137
  17. Neilands JB. Microbial envelope proteins related to iron. Ann Rev Microbiol 1982;36:285-309 https://doi.org/10.1146/annurev.mi.36.100182.001441
  18. Schryvers AB. Identification of the transferrin and lactoferrin binding proteins in Haemophilus influenzae. J Med Microbiol 1989;29:121-130 https://doi.org/10.1099/00222615-29-2-121
  19. Tsai J, DW Dyer, PF Sparling. Loss of transferrin receptor activity in Neisseria meningitidis correlates with inability to use transferrin as an iron source. Infect Immun 1988;56:3132-3138
  20. Bramanti TE, Holt SC. Hemin uptake in Porphyromonas gingivalis: Omp26 is a hemin-binding surface protein. J Bacteriol 1993;175:7413-7420 https://doi.org/10.1128/jb.175.22.7413-7420.1993
  21. Coulton JW, Pang JCS. Transport of hemin by Hemophilus influenzae type b. Curr Microbiol 1983;9:93-98 https://doi.org/10.1007/BF01568915
  22. Chu L, Song M, Holt SC. Effect of iron regulation on expression and hemin-binding function of outer-sheath proteins from Treponema denticola. Microb Pathog 1994;16:321-335 https://doi.org/10.1006/mpat.1994.1033
  23. Fujimura S, Shibata Y, Hirai K. Nakamura T. Some binding properties of the envelope of Porphyromonss gingivalis to hemoglobin. FEMS Immunol Med Microbiol 1995;10:109-114 https://doi.org/10.1111/j.1574-695X.1995.tb00018.x
  24. Hanson MS, Hansen EJ. Molecular cloning, partial purification, and characterization of a hemin-binding lipoprotein from Haemoohilus influenza type b. Mol Microbiol 1991;5:267-278 https://doi.org/10.1111/j.1365-2958.1991.tb02107.x
  25. Lee BC. Isolation of heamin-binding proteins of Neisseria gonorrheae. J Med Microbiol 1992;36:121-127 https://doi.org/10.1099/00222615-36-2-121
  26. Lee BC. Isolation of an outer membrane hemin-binding protein of Hemophilus influenzae type b. Infect Immun 1992;60:810-816
  27. Morse SA, Chen C-Y, LeFaopu A, Mietzner TA. A potential role for the major iron-regulated protein expressed by pathogenic Neisseria spp. Rev Inf Dis 1988;10:s306-s310 https://doi.org/10.1093/cid/10.Supplement_2.S306
  28. Otto BR, Sparrius M, Verweij-van Vught AMJJ, MacLaren DM. Iron-regulated outer membrane protein of Bacteroides fragilis involved in heme uptake. Infect Immun 1990;58:3954-3958
  29. Grenier D. Hemin-binding property of Porphyromonas gingivalis outer membranes. FEMS Microbiol Lett 1991; 77:45-50 https://doi.org/10.1111/j.1574-6968.1991.tb04319.x
  30. Smalley JW, Birss AJ, McKee AS, Marsh PD. Hemin-binding proteins of Porphyromonas gingivalis W50 grown in a chemostat under haemin-limitation. J Gen Microbiol 1993;139:2145-2150 https://doi.org/10.1099/00221287-139-9-2145
  31. Stugard CE, Daskaleros PA, Payne SM. A 101-kilodalton heme-binding protein associated with Congo red binding and virulence of Shigella flexneri and enteroinvasive Escherichia coli strains. Infect Immun 1989;57:3534-3539
  32. Hanson MS, Slaughter C, Hansen E. The hbpA gene of Haemophilus influenza type b encodes a heme-binding lipoprotein conserved among heme-dependent Haemophilus species. Infect Immun 1992;60:2257-2266
  33. Scott D, Siboo IR, Chan ECS, Klitorinos A, Siboo R. Binding of hemin and congo red by oral hemolytic spirochetes. Oral Microbiol Immunol 1993;8:245-250 https://doi.org/10.1111/j.1399-302X.1993.tb00568.x
  34. Pendrak ML, RD Perry. Characterization of a haemin-storage reservoirs of hemin and inorganic iron in Yersinia pestis. Infect Immun 1991;61:32-39
  35. Perry RD, TS Lucier, DJ Sikkema, RR Brubaker. Storage reservoirs of hemin and inorganic iron in Yersinia pestis. Infect Immun 1993;61:32-39
  36. Maciver I, O'Reilly T, Brown MRW. Porphyrin ring source can alter the outer membrane protein profile of non-typeable Hemophilus influenzae. J Med Microbiol 1990;31:163-168 https://doi.org/10.1099/00222615-31-3-163
  37. Williams P, Brown MRW. Influence of iron restriction on growth and the expression of outer membrane proteins in Hemophilus influenzae and H. parainfluenzae. FEMS Microbiol Lett 1985;33:153-157
  38. Bramanti TE, Holt SC. Iron-regulated outer membrane proteins in the periodontopathic bacterium Bacteroids gingivalis. Biochem Biophys Res Commun 1990;166:1146-1154 https://doi.org/10.1016/0006-291X(90)90986-W
  39. Tanner ACR, Haffer C, Bratthall GT, Visconti RA, Socransky SS. A study of the bacteria associated with advancing periodontitis in man. J Clin Periodontol 1979;6: 278-307 https://doi.org/10.1111/j.1600-051X.1979.tb01931.x
  40. Slots J, Bragd L, Wikstrom M, Dahlen G. The occurrence of Actinobacillus actinomycetemcomitans, Bacteroides gingivalis and Bacteroides intermedius in destructive periodontal disease in adults. J Clin Periodontol 1986;13: 570-577 https://doi.org/10.1111/j.1600-051X.1986.tb00849.x
  41. Socransky SS, Haffajee AD. The bacterial etiology of destructive periodontal disease: current concepts. J Periodontol 1992;63:322-331 https://doi.org/10.1902/jop.1992.63.4s.322
  42. Chung CP, Nisengard RJ, Slots J, Genco RJ. Bacterial IgG and IgM antibody titers m acute necrotizing ulcerative gingivitis. J Periodontol 1983;54:557-562 https://doi.org/10.1902/jop.1983.54.9.557
  43. Kornman KS, Loesche WJ. The subgingival microbial flora during pregnancy. J Periodont Res 1980;15: 111-122 https://doi.org/10.1111/j.1600-0765.1980.tb00265.x
  44. Shah HN, Gharbia SE. Proposal of a new species Prevotella nigrescens sp. nov. among strains previously classified as P. intermedia. FEMS Immunol Med Microbiol 1993;6:97 https://doi.org/10.1111/j.1574-695X.1993.tb00309.x
  45. Okamoto M, Maeda N, Kondo K, Leung KP. Hemolytic and hemagglutinating activities of Prevotella intermedia and Prevotella nigrescens. FEMS Microbiol Lett 1999;178:299-304 https://doi.org/10.1111/j.1574-6968.1999.tb08691.x
  46. Matto J, Asikainen S, Vaisanen ML, Von Troil Linden B, Kononen E, Saarela M, Salminen K, Finegold SM, Jousimies Somer H. Beta-lactamase production in Prevotella intermedia, Prevotella nigrescens, and Prevotella pallens genotypes and in vitro susceptibilities to selected antimicrobial agents. Antimicrob Agents Chemother 1999;43:2383-2388
  47. Andres MT, Chung WO, Roberts MC, Fierro JF. Antimicrobial susceptibilities of Porphyromonas gingivalis, Prevotella intermedia, and Prevotella nigrescens spp. Isolated in Spain. Antimicrob Agents Chemother 1998;42:3022- 3023
  48. Baumgartner JC, Bae KS, Xia T, Whitt J, David LL. Sodium dodecyl sulfate polyacrylamide gel electrophoresis and polymerase chain reaction for differentiation of Prevotella intermedia and nigrescens. J Endod 1999;25:324-328 https://doi.org/10.1016/S0099-2399(06)81164-7
  49. Conrads G, Pelz K, Hughes B, Seyfarth I, Devine DA. Optimized oligonucleotides for the differentiation of Prevotella intermedia and Prevotella nigrescens. Oral Microbiol Immunol 1997;12:117-120 https://doi.org/10.1111/j.1399-302X.1997.tb00627.x
  50. Premaraj T, Kato N, Fukui K, Kato H, Watanabe K. Use of PCR and sodium dodecyl sulfate-polyacrylamide gel electrophoresis techniques for differentiation of Prevotella intermedia sensu stricto and Prevotella nigrescens. J Clin Microbiol 1999;37:1057-1061
  51. Guillot E, Mouton C. PCR-DNA probe assays for identification and detection of Prevotella intermedia sensu stricto and Prevotella nigrescens. J Clin Microbiol 1997;35:1876-1882
  52. Kennel W, Holt SC. Comparative studies of the outer membranes of Bacteroides gingivalis strains ATCC 33277, W50, W83, 381. Oral Microbiol Immunol 1990;5:121-130 https://doi.org/10.1111/j.1399-302X.1990.tb00409.x
  53. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 1970;227:680-685 https://doi.org/10.1038/227680a0
  54. Hager DA, Burgess RR. Elution of proteins from sodium dodecyl sulfatepolyacrylamide gels. removal of sodium dodecyl sulfate. and renaturation of enzymatic activity: results with Sigma subunit of Escherichia coli RNA polymerase. wheat germ DNA topoisomerase, and other enzymes. Anal Biochem 1980;109:76-86 https://doi.org/10.1016/0003-2697(80)90013-5
  55. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 1979;76: 4350-4354 https://doi.org/10.1073/pnas.76.9.4350