1887

Abstract

The gene has been previously shown to play a significant role in the biogenesis of gingipains. Further, in FLL92, a -defective mutant, there was increased auto-aggregation, suggesting alteration in membrane surface proteins. In order to determine the role of the VimA protein in cell surface biogenesis, the surface morphology of FLL92 was further characterized. Transmission electron microscopy demonstrated abundant fimbrial appendages and a less well defined and irregular capsule in FLL92 compared with the wild-type. In addition, atomic force microscopy showed that the wild-type had a smoother surface compared with FLL92. Western blot analysis using anti-FimA antibodies showed a 41 kDa immunoreactive protein band in FLL92 which was missing in the wild-type W83 strain. There was increased sensitivity to globomycin and vancomycin in FLL92 compared with the wild-type. Outer membrane fractions from FLL92 had a modified lectin-binding profile. Furthermore, in contrast with the wild-type strain, nine proteins were missing from the outer membrane fraction of FLL92, while 20 proteins present in that fraction from FLL92 were missing in the wild-type strain. Taken together, these results suggest that the VimA protein affects capsular synthesis and fimbrial phenotypic expression, and plays a role in the glycosylation and anchorage of several surface proteins.

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2010-07-01
2020-07-11
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References

  1. Abaibou H., Chen Z., Olango G. J., Liu Y., Edwards J., Fletcher H. M.. 2001; vimA gene downstream of recA is involved in virulence modulation in Porphyromonas gingivalis W83. Infect Immun69:325–335
    [Google Scholar]
  2. Amano A., Nakagawa I., Kataoka K., Morisaki I., Hamada S.. 1999; Distribution of Porphyromonas gingivalis strains with fimA genotypes in periodontitis patients. J Clin Microbiol37:1426–1430
    [Google Scholar]
  3. Amano A., Kuboniwa M., Nakagawa I., Akiyama S., Morisaki I., Hamada S.. 2000; Prevalence of specific genotypes of Porphyromonas gingivalis fimA and periodontal health status. J Dent Res79:1664–1668
    [Google Scholar]
  4. Amano A., Nakagawa I., Okahashi N., Hamada N.. 2004; Variations of Porphyromonas gingivalis fimbriae in relation to microbial pathogenesis. J Periodontal Res39:136–142
    [Google Scholar]
  5. Athavankar S., Peterson B. R.. 2003; Control of gene expression with small molecules: biotin-mediated acylation of targeted lysine residues in recombinant yeast. Chem Biol10:1245–1253
    [Google Scholar]
  6. Bogen G., Slots J.. 1999; Black-pigmented anaerobic rods in closed periapical lesions. Int Endod J32:204–210
    [Google Scholar]
  7. Brakstad O. G., Maeland J. A.. 1997; Mechanisms of methicillin resistance in staphylococci. APMIS105:264–276
    [Google Scholar]
  8. Chen Y. Y., Cross K. J., Paolini R. A., Fielding J. E., Slakeski N., Reynolds E. C.. 2002; CPG70 is a novel basic metallocarboxypeptidase with C-terminal polycystic kidney disease domains from Porphyromonas gingivalis. J Biol Chem277:23433–23440
    [Google Scholar]
  9. Cutler C. W., Kalmar J. R., Genco C. A.. 1995; Pathogenic strategies of the oral anaerobe, Porphyromonas gingivalis. Trends Microbiol3:45–51
    [Google Scholar]
  10. Dave S., Van D. T.. 2008; The link between periodontal disease and cardiovascular disease is probably inflammation. Oral Dis14:95–101
    [Google Scholar]
  11. Davey M. E., Duncan M. J.. 2006; Enhanced biofilm formation and loss of capsule synthesis: deletion of a putative glycosyltransferase in Porphyromonas gingivalis. J Bacteriol188:5510–5523
    [Google Scholar]
  12. Demmer R. T., Desvarieux M.. 2006; Periodontal infections and cardiovascular disease: the heart of the matter. J Am Dent Assoc137:Suppl14S–20S
    [Google Scholar]
  13. Desvaux M., Dumas E., Chafsey I., Hebraud M.. 2006; Protein cell surface display in Gram-positive bacteria: from single protein to macromolecular protein structure. FEMS Microbiol Lett256:1–15
    [Google Scholar]
  14. Dramsi S., Trieu-Cuot P., Bierne H.. 2005; Sorting sortases: a nomenclature proposal for the various sortases of Gram-positive bacteria. Res Microbiol156:289–297
    [Google Scholar]
  15. Duban M. E., Lee K., Lynn D. G.. 1993; Strategies in pathogenesis: mechanistic specificity in the detection of generic signals. Mol Microbiol7:637–645
    [Google Scholar]
  16. Egea L., Aguilera L., Gimenez R., Sorolla M. A., Aguilar J., Badia J., Baldoma L.. 2007; Role of secreted glyceraldehyde-3-phosphate dehydrogenase in the infection mechanism of enterohemorrhagic and enteropathogenic Escherichia coli: interaction of the extracellular enzyme with human plasminogen and fibrinogen. Int J Biochem Cell Biol39:1190–1203
    [Google Scholar]
  17. Ford P. J., Yamazaki K., Seymour G. J.. 2007; Cardiovascular and oral disease interactions: what is the evidence?. Prim Dent Care14:59–66
    [Google Scholar]
  18. Frirdich E., Whitfield C.. 2005; Lipopolysaccharide inner core oligosaccharide structure and outer membrane stability in human pathogens belonging to the Enterobacteriaceae. J Endotoxin Res11:133–144
    [Google Scholar]
  19. Gardy J. L., Laird M. R., Chen F., Rey S., Walsh C. J., Ester M., Brinkman F. S.. 2005; PSORTb v.2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics21:617–623
    [Google Scholar]
  20. Gough J., Karplus K., Hughey R., Chothia C.. 2001; Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol313:903–919
    [Google Scholar]
  21. Gozalbo D., Gil-Navarro I., Azorin I., Renau-Piqueras J., Martinez J. P., Gil M. L.. 1998; The cell wall-associated glyceraldehyde-3-phosphate dehydrogenase of Candida albicans is also a fibronectin and laminin binding protein. Infect Immun66:2052–2059
    [Google Scholar]
  22. Grivet M., Morrier J. J., Benay G., Barsotti O.. 2000; Effect of hydrophobicity on in vitro streptococcal adhesion to dental alloys. J Mater Sci Mater Med11:637–642
    [Google Scholar]
  23. Haft D. H., Paulsen I. T., Ward N., Selengut J. D.. 2006; Exopolysaccharide-associated protein sorting in environmental organisms: the PEP-CTERM/EpsH system. Application of a novel phylogenetic profiling heuristic. BMC Biol4:29
    [Google Scholar]
  24. Handley P. S., Tipler L. S.. 1986; An electron microscope survey of the surface structures and hydrophobicity of oral and non-oral species of the bacterial genus Bacteroides. Arch Oral Biol31:325–335
    [Google Scholar]
  25. Harris J. R.. 1991; Electron Microscopy in Biology: a Practical Approach Oxford, UK: IRL Press;
  26. Henry L. G., Sandberg L., Zhang K., Fletcher H. M.. 2008; DNA repair of 8-oxo-7,8-dihydroguanine lesions in Porphyromonas gingivalis. J Bacteriol190:7985–7993
    [Google Scholar]
  27. Herlax V., Mate S., Rimoldi O., Bakas L.. 2009; Relevance of fatty acid covalently bound to Escherichia coli α-hemolysin and membrane microdomains in the oligomerization process. J Biol Chem284:25199–25210
    [Google Scholar]
  28. Imamura T.. 2003; The role of gingipains in the pathogenesis of periodontal disease. J Periodontol74:111–118
    [Google Scholar]
  29. Kall L., Krogh A., Sonnhammer E. L.. 2007; Advantages of combined transmembrane topology and signal peptide prediction – the Phobius web server. Nucleic Acids Res35:W429–W432
    [Google Scholar]
  30. Kato T., Tsuda T., Omori H., Kato T., Yoshimori T., Amano A.. 2007; Maturation of fimbria precursor protein by exogenous gingipains in Porphyromonas gingivalis gingipain-null mutant. FEMS Microbiol Lett273:96–102
    [Google Scholar]
  31. Kinoshita H., Wakahara N., Watanabe M., Kawasaki T., Matsuo H., Kawai Y., Kitazawa H., Ohnuma S., Miura K.. other authors 2008; Cell surface glyceraldehyde-3-phosphate dehydrogenase (GAPDH) of Lactobacillus plantarum LA 318 recognizes human A and B blood group antigens. Res Microbiol159:685–691
    [Google Scholar]
  32. Kumada H., Haishima Y., Umemoto T., Tanamoto K.. 1995; Structural study on the free lipid A isolated from lipopolysaccharide of Porphyromonas gingivalis. J Bacteriol177:2098–2106
    [Google Scholar]
  33. Kuramitsu H. K.. 1998; Proteases of Porphyromonas gingivalis: what don't they do?. Oral Microbiol Immunol13:263–270
    [Google Scholar]
  34. Lama A., Kucknoor A., Mundodi V., Alderete J. F.. 2009; Glyceraldehyde-3-phosphate dehydrogenase is a surface-associated, fibronectin-binding protein of Trichomonas vaginalis. Infect Immun77:2703–2711
    [Google Scholar]
  35. Lamont R. J., Jenkinson H. F.. 1998; Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol Mol Biol Rev62:1244–1263
    [Google Scholar]
  36. Lin X., Wu J., Xie H.. 2006; Porphyromonas gingivalis minor fimbriae are required for cell–cell interactions. Infect Immun74:6011–6015
    [Google Scholar]
  37. Linton D., Allan E., Karlyshev A. V., Cronshaw A. D., Wren B. W.. 2002; Identification of N-acetylgalactosamine-containing glycoproteins PEB3 and CgpA in Campylobacter jejuni. Mol Microbiol43:497–508
    [Google Scholar]
  38. Maeda K., Nagata H., Kuboniwa M., Kataoka K., Nishida N., Tanaka M., Shizukuishi S.. 2004; Characterization of binding of Streptococcus oralis glyceraldehyde-3-phosphate dehydrogenase to Porphyromonas gingivalis major fimbriae. Infect Immun72:5475–5477
    [Google Scholar]
  39. Mainardi J. L., Villet R., Bugg T. D., Mayer C., Arthur M.. 2008; Evolution of peptidoglycan biosynthesis under the selective pressure of antibiotics in Gram-positive bacteria. FEMS Microbiol Rev32:386–408
    [Google Scholar]
  40. Marraffini L. A., Dedent A. C., Schneewind O.. 2006; Sortases and the art of anchoring proteins to the envelopes of Gram-positive bacteria. Microbiol Mol Biol Rev70:192–221
    [Google Scholar]
  41. Matatov R., Goldhar J., Skutelsky E., Sechter I., Perry R., Podschun R., Sahly H., Thankavel K., Abraham S. N.. other authors 1999; Inability of encapsulated Klebsiella pneumoniae to assemble functional type 1 fimbriae on their surface. FEMS Microbiol Lett179:123–130
    [Google Scholar]
  42. McAlister A. D., Sroka A., Fitzpatrick R. E., Quinsey N. S., Travis J., Potempa J., Pike R. N.. 2009; Gingipain enzymes from Porphyromonas gingivalis preferentially bind immobilized extracellular proteins: a mechanism favouring colonization?. J Periodontal Res44:348–353
    [Google Scholar]
  43. McGraw W. T., Potempa J., Farley D., Travis J.. 1999; Purification, characterization, and sequence analysis of a potential virulence factor from Porphyromonas gingivalis, peptidylarginine deiminase. Infect Immun67:3248–3256
    [Google Scholar]
  44. Mikolajczyk-Pawlinska J., Kordula T., Pavloff N., Pemberton P. A., Chen W. C., Travis J., Potempa J.. 1998; Genetic variation of Porphyromonas gingivalis genes encoding gingipains, cysteine proteinases with arginine or lysine specificity. Biol Chem379:205–211
    [Google Scholar]
  45. Murakami Y., Masuda T., Imai M., Iwami J., Nakamura H., Noguchi T., Yoshimura F.. 2004; Analysis of major virulence factors in Porphyromonas gingivalis under various culture temperatures using specific antibodies. Microbiol Immunol48:561–569
    [Google Scholar]
  46. Nagata H., Iwasaki M., Maeda K., Kuboniwa M., Hashino E., Toe M., Minamino N., Kuwahara H., Shizukuishi S.. 2009; Identification of the binding domain of Streptococcus oralis glyceraldehyde-3-phosphate dehydrogenase for Porphyromonas gingivalis major fimbriae. Infect Immun77:5130–5138
    [Google Scholar]
  47. Nakano K., Nemoto H., Nomura R., Inaba H., Yoshioka H., Taniguchi K., Amano A., Ooshima T.. 2009; Detection of oral bacteria in cardiovascular specimens. Oral Microbiol Immunol24:64–68
    [Google Scholar]
  48. Nakayama K., Yoshimura F., Kadowaki T., Yamamoto K.. 1996; Involvement of arginine-specific cysteine proteinase (Arg–gingipain) in fimbriation of Porphyromonas gingivalis. J Bacteriol178:2818–2824
    [Google Scholar]
  49. Nguyen K. A., Zylicz J., Szczesny P., Sroka A., Hunter N., Potempa J.. 2009; Verification of a topology model of PorT as an integral outer-membrane protein in Porphyromonas gingivalis. Microbiology155:328–337
    [Google Scholar]
  50. Nielsen H., Engelbrecht J., Brunak S., von Heijne G.. 1997; Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng10:1–6
    [Google Scholar]
  51. Nimchuk Z., Marois E., Kjemtrup S., Leister R. T., Katagiri F., Dangl J. L.. 2000; Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several type III effector proteins from Pseudomonas syringae. Cell101:353–363
    [Google Scholar]
  52. Nishiyama S., Murakami Y., Nagata H., Shizukuishi S., Kawagishi I., Yoshimura F.. 2007; Involvement of minor components associated with the FimA fimbriae of Porphyromonas gingivalis in adhesive functions. Microbiology153:1916–1925
    [Google Scholar]
  53. Olango G. J., Roy F., Sheets S. M., Young M. K., Fletcher H. M.. 2003; Gingipain RgpB is excreted as a proenzyme in the vimA-defective mutant Porphyromonas gingivalis FLL92. Infect Immun71:3740–3747
    [Google Scholar]
  54. Olsen H. B., Kaarsholm N. C.. 2000; Structural effects of protein lipidation as revealed by LysB29-myristoyl, des(B30) insulin. Biochemistry39:11893–11900
    [Google Scholar]
  55. Pancholi V., Fischetti V. A.. 1992; A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. J Exp Med176:415–426
    [Google Scholar]
  56. Paramonov N., Rangarajan M., Hashim A., Gallagher A., Aduse-Opoku J., Slaney J. M., Hounsell E., Curtis M. A.. 2005; Structural analysis of a novel anionic polysaccharide from Porphyromonas gingivalis strain W50 related to Arg-gingipain glycans. Mol Microbiol58:847–863
    [Google Scholar]
  57. Pavloff N., Potempa J., Pike R. N., Prochazka V., Kiefer M. C., Travis J., Barr P. J.. 1995; Molecular cloning and structural characterization of the Arg–gingipain proteinase of Porphyromonas gingivalis. Biosynthesis as a proteinase–adhesin polyprotein. J Biol Chem270:1007–1010
    [Google Scholar]
  58. Pavloff N., Pemberton P. A., Potempa J., Chen W. C., Pike R. N., Prochazka V., Kiefer M. C., Travis J., Barr P. J.. 1997; Molecular cloning and characterization of Porphyromonas gingivalis lysine-specific gingipain. A new member of an emerging family of pathogenic bacterial cysteine proteinases. J Biol Chem272:1595–1600
    [Google Scholar]
  59. Pearson W. R., Lipman D. J.. 1988; Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A85:2444–2448
    [Google Scholar]
  60. Pike R. N., Potempa J., McGraw W., Coetzer T. H., Travis J.. 1996; Characterization of the binding activities of proteinase–adhesin complexes from Porphyromonas gingivalis. J Bacteriol178:2876–2882
    [Google Scholar]
  61. Potempa J., Pike R., Travis J.. 1995; 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 Immun63:1176–1182
    [Google Scholar]
  62. Pratto F., Suzuki Y., Takeyasu K., Alonso J. C.. 2009; Single-molecule analysis of protein–DNA complexes formed during partition of newly replicated plasmid molecules in Streptococcus pyogenes. J Biol Chem284:30298–30306
    [Google Scholar]
  63. Rangarajan M., Aduse-Opoku J., Paramonov N., Hashim A., Bostanci N., Fraser O. P., Tarelli E., Curtis M. A.. 2008; Identification of a second lipopolysaccharide in Porphyromonas gingivalis W50. J Bacteriol190:2920–2932
    [Google Scholar]
  64. Rodriguez S. B., Stitt B. L., Ash D. E.. 2009; Expression of peptidylarginine deiminase from Porphyromonas gingivalis in Escherichia coli: enzyme purification and characterization. Arch Biochem Biophys488:14–22
    [Google Scholar]
  65. Sahly H., Podschun R., Oelschlaeger T. A., Greiwe M., Parolis H., Hasty D., Kekow J., Ullmann U., Ofek I.. other authors 2000; Capsule impedes adhesion to and invasion of epithelial cells by Klebsiella pneumoniae. Infect Immun68:6744–6749
    [Google Scholar]
  66. Salinero K. K., Keller K., Feil W. S., Feil H., Trong S., Di B. G., Lapidus A.. 2009; Metabolic analysis of the soil microbe Dechloromonas aromatica str. RCB: indications of a surprisingly complex life-style and cryptic anaerobic pathways for aromatic degradation. BMC Genomics10:351
    [Google Scholar]
  67. Sato K., Sakai E., Veith P. D., Shoji M., Kikuchi Y., Yukitake H., Ohara N., Naito M., Okamoto K.. other authors 2005; Identification of a new membrane-associated protein that influences transport/maturation of gingipains and adhesins of Porphyromonas gingivalis. J Biol Chem280:8668–8677
    [Google Scholar]
  68. Shirai H., Blundell T. L., Mizuguchi K.. 2001; A novel superfamily of enzymes that catalyze the modification of guanidino groups. Trends Biochem Sci26:465–468
    [Google Scholar]
  69. Shoji M., Ratnayake D. B., Shi Y., Kadowaki T., Yamamoto K., Yoshimura F., Akamine A., Curtis M. A., Nakayama K.. 2002; Construction and characterization of a nonpigmented mutant of Porphyromonas gingivalis: cell surface polysaccharide as an anchorage for gingipains. Microbiology148:1183–1191
    [Google Scholar]
  70. 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 Microbiol52:1513–1525
    [Google Scholar]
  71. Slakeski N., Margetts M., Moore C., Czajkowski L., Barr I. G., Reynolds E. C.. 2002; Characterization and expression of a novel Porphyromonas gingivalis outer membrane protein, Omp28. Oral Microbiol Immunol17:150–156
    [Google Scholar]
  72. Stapleton P. D., Taylor P. W.. 2002; Methicillin resistance in Staphylococcus aureus: mechanisms and modulation. Sci Prog85:57–72
    [Google Scholar]
  73. Stathopoulou P. G., Galicia J. C., Benakanakere M. R., Garcia C. A., Potempa J., Kinane D. F.. 2009; Porphyromonas gingivalis induce apoptosis in human gingival epithelial cells through a gingipain-dependent mechanism. BMC Microbiol9:107
    [Google Scholar]
  74. Suzuki Y., Yoshimura F., Takahashi K., Tani H., Suzuki T.. 1988; Detection of fimbriae and fimbrial antigens on the oral anaerobe Bacteroides gingivalis by negative staining and serological methods. J Gen Microbiol134:2713–2720
    [Google Scholar]
  75. Ton-That H., Marraffini L. A., Schneewind O.. 2004; Protein sorting to the cell wall envelope of Gram-positive bacteria. Biochim Biophys Acta 1694;269–278
    [Google Scholar]
  76. Tsukiji S., Nagamune T.. 2009; Sortase-mediated ligation: a gift from Gram-positive bacteria to protein engineering. ChemBioChem10:787–798
    [Google Scholar]
  77. Vanterpool E., Roy F., Fletcher H. M.. 2004; The vimE gene downstream of vimA is independently expressed and is involved in modulating proteolytic activity in Porphyromonas gingivalis W83. Infect Immun72:5555–5564
    [Google Scholar]
  78. Vanterpool E., Roy F., Fletcher H. M.. 2005a; Inactivation of vimF, a putative glycosyltransferase gene downstream of vimE, alters glycosylation and activation of the gingipains in Porphyromonas gingivalis W83. Infect Immun73:3971–3982
    [Google Scholar]
  79. Vanterpool E., Roy F., Sandberg L., Fletcher H. M.. 2005b; Altered gingipain maturation in vimA- and vimE-defective isogenic mutants of Porphyromonas gingivalis. Infect Immun73:1357–1366
    [Google Scholar]
  80. Vanterpool E., Roy F., Zhan W., Sheets S. M., Sangberg L., Fletcher H. M.. 2006; VimA is part of the maturation pathway for the major gingipains of Porphyromonas gingivalis W83. Microbiology152:3383–3389
    [Google Scholar]
  81. Veith P. D., Chen Y. Y., Reynolds E. C.. 2004; Porphyromonas gingivalis RgpA and Kgp proteinases and adhesins are C terminally processed by the carboxypeptidase CPG70. Infect Immun72:3655–3657
    [Google Scholar]
  82. Voytas D., Ke N.. 2001; Detection and quantitation of radiolabeled proteins and DNA in gels and blots. Curr Protoc Mol Biol Appendix3: Appendix 3A
    [Google Scholar]
  83. Wang M., Liang S., Hosur K. B., Domon H., Yoshimura F., Amano A., Hajishengallis G.. 2009; Differential virulence and innate immune interactions of type I and II fimbrial genotypes of Porphyromonas gingivalis. Oral Microbiol Immunol24:478–484
    [Google Scholar]
  84. Wright T. L., Ellen R. P., Lacroix J. M., Sinnadurai S., Mittelman M. W.. 1997; Effects of metronidazole on Porphyromonas gingivalis biofilms. J Periodontal Res32:473–477
    [Google Scholar]
  85. Yoshimura F., Murakami Y., Nishikawa K., Hasegawa Y., Kawaminami S.. 2009; Surface components of Porphyromonas gingivalis. J Periodontal Res44:1–12
    [Google Scholar]
  86. Zaas D. W., Duncan M., Rae W. J., Abraham S. N.. 2005; The role of lipid rafts in the pathogenesis of bacterial infections. Biochim Biophys Acta1746:305–313
    [Google Scholar]
  87. Zhang Y.. 2008; I-TASSER server for protein 3D structure prediction. BMC Bioinformatics9:40
    [Google Scholar]
  88. Zhang Y.. 2009; I-TASSER: Fully automated protein structure prediction in CASP8. Proteins77 :Suppl. 9100–113
    [Google Scholar]
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