VimA mediates multiple functions that control virulence in Porphyromonas gingivalis

Molecular Oral Microbiology

Volumn 28, Issue 3, 2013, Pages 167-180

  Aruni, A W ^a   Robles, A ^a   Fletcher, H M ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acetylation; Gingipain; Oxidative stress; Protein sorting; VimA; Virulence regulation

Indexed keywords

CYSTEINE PROTEINASE; CYTOKINE; FIMBRIA PROTEIN; GLYCOPROTEIN; LIPID; LIPOPOLYSACCHARIDE; LIPOPROTEIN; MEMBRANE PROTEIN; PEPTIDOGLYCAN; PROTEIN; PROTEIN VIMA; SORTASE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 3; UNCLASSIFIED DRUG;

ACETYLATION; APOPTOSIS; ARTICLE; BIOGENESIS; BIOSYNTHESIS; CELL SURFACE; CLOSTRIDIUM BOTULINUM; DEACETYLATION; ENZYME ACTIVITY; ESCHERICHIA COLI; FUSOBACTERIUM NUCLEATUM; GENE; GENE EXPRESSION; GENE REGULATORY NETWORK; NONHUMAN; OXIDATIVE STRESS; PORPHYROMONAS GINGIVALIS; PROTEIN SYNTHESIS; PROTEIN TARGETING; RHODOBACTER SPHAEROIDES; SALMONELLA ENTERICA; SIALYLATION; SURVIVAL; THROMBOCYTE AGGREGATION; VIRULENCE;

ACETYLATION; ADHESINS, BACTERIAL; BACTERIAL ADHESION; CYSTEINE ENDOPEPTIDASES; GENES, BACTERIAL; OXIDATIVE STRESS; PORPHYROMONAS GINGIVALIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; VIRULENCE;

EID: 84876177722     PISSN: 20411006     EISSN: 20411014     Source Type: Journal    
DOI: 10.1111/omi.12017     Document Type: Article

References (84)

1. Abaibou, H., Chen, Z., Olango, G.J., Liu, Y., Edwards, J. and Fletcher, H.M. (2001) vimA gene downstream of recA is involved in virulence modulation in Porphyromonas gingivalis W83. Infect Immun 69: 325-335.
2. Angata, T. and Varki, A. (2002) Chemical diversity in the sialic acids and related alpha-keto acids: an evolutionary perspective. Chem Rev 102: 439-469.
3. Aruni, W., Vanterpool, E., Osbourne, D. et al. (2011) Sialidase and sialoglycoproteases can modulate virulence in Porphyromonas gingivalis. Infect Immun 79: 2779-2791.
4. Aruni, A.W., Lee, J., Osbourne, D. et al. (2012) VimA-dependent modulation of acetyl-CoA levels and lipid A biosynthesis can alter virulence in Porphyromonas gingivalis. Infect Immun 80: 550-564.
5. Barnard, M.R. and Holt, S.C. (1985) Isolation and characterization of the peptidoglycans from selected gram-positive and gram-negative periodontal pathogens. Can J Microbiol 31: 154-160.
6. Bugg, T.D. and Brandish, P.E. (1994) From peptidoglycan to glycoproteins: common features of lipid-linked oligosaccharide biosynthesis. FEMS Microbiol Lett 119: 255-262.
7. Chen, Y.Y., Peng, B., Yang, Q. et al. (2011) The outer membrane protein LptO is essential for the O-deacylation of LPS and the co-ordinated secretion and attachment of A-LPS and CTD proteins in Porphyromonas gingivalis. Mol Microbiol 79: 1380-1401.
8. Craig, J.W., Cherry, M.A. and Brady, S.F. (2011) Long-chain N-acyl amino acid synthases are linked to the putative PEP-CTERM/exosortase protein-sorting system in Gram-negative bacteria. J Bacteriol 193: 5707-5715.
9. Curtis, M.A., Thickett, A., Slaney, J.M. et al. (1999) Variable carbohydrate modifications to the catalytic chains of the RgpA and RgpB proteases of Porphyromonas gingivalis W50. Infect Immun 67: 3816-3823.
10. Curtis, M.A., Duse-Opoku, J. and Rangarajan, M. (2001) Cysteine proteases of Porphyromonas gingivalis. Crit Rev Oral Biol Med 12: 192-216.
11. Darveau, R.P., Hajishengallis, G. and Curtis, M.A. (2012) Porphyromonas gingivalis as a potential community activist for disease. J Dent Res 91: 816-820.
12. Davey, M.E. and Duncan, M.J. (2006) Enhanced biofilm formation and loss of capsule synthesis: deletion of a putative glycosyltransferase in Porphyromonas gingivalis. J Bacteriol 188: 5510-5523.
13. Dewhirst, F.E., Chen, T., Izard, J. et al. (2010) The human oral microbiome. J Bacteriol 192: 5002-5017.
14. Diaz, P.I., Slakeski, N., Reynolds, E.C., Morona, R., Rogers, A.H. and Kolenbrander, P.E. (2006) Role of oxyR in the oral anaerobe Porphyromonas gingivalis. J Bacteriol 188: 2454-2462.
15. Dou, Y., Osbourne, D., McKenzie, R. and Fletcher, H.M. (2010) Involvement of extracytoplasmic function sigma factors in virulence regulation in Porphyromonas gingivalis W83. FEMS Microbiol Lett 312: 24-32.
16. Dramsi, S., Magnet, S., Davison, S. and Arthur, M. (2008) Covalent attachment of proteins to peptidoglycan. FEMS Microbiol Rev 32: 307-320.
17. Eichler, J. and Adams, M.W. (2005) Posttranslational protein modification in Archaea. Microbiol Mol Biol Rev 69: 393-425.
18. Eley, B.M. and Cox, S.W. (2003) Proteolytic and hydrolytic enzymes from putative periodontal pathogens: characterization, molecular genetics, effects on host defenses and tissues and detection in gingival crevice fluid. Periodontol 2000 31: 105-124.
19. Gallagher, A., Aduse-Opoku, J., Rangarajan, M., Slaney, J.M. and Curtis, M.A. (2003) Glycosylation of the Arg-gingipains of Porphyromonas gingivalis and comparison with glycoconjugate structure and synthesis in other bacteria. Curr Protein Pept Sci 4: 427-441.
20. + involvement in Bacillus subtilis. J Bacteriol, 188: 5460-5468.
21. Griffen, A.L., Beall, C.J., Campbell, J.H. et al. (2012) Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J 6: 1176-1185.
22. Gross, E.L., Leys, E.J., Gasparovich, S.R. et al. (2010) Bacterial 16S sequence analysis of severe caries in young permanent teeth. J Clin Microbiol 48: 4121-4128.
23. Haft, D.H. and Varghese, N. (2011) GlyGly-CTERM and rhombosortase: a C-terminal protein processing signal in a many-to-one pairing with a rhomboid family intramembrane serine protease. PLoS ONE 6: e28886.
24. Haft, D.H., Paulsen, I.T., Ward, N. and Selengut, J.D. (2006) Exopolysaccharide-associated protein sorting in environmental organisms: the PEP-CTERM/EpsH system. Application of a novel phylogenetic profiling heuristic. BMC Biol 4: 29.
25. Haft, D.H., Payne, S.H. and Selengut, J.D. (2012) Archaeosortases and exosortases are widely distributed systems linking membrane transit with posttranslational modification. J Bacteriol 194: 36-48.
26. Hajishengallis, G. (2011) Immune evasion strategies of Porphyromonas gingivalis. J Oral Biosci 53: 233-240.
27. Hajishengallis, G. and Lamont, R.J. (2012) Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Mol Oral Microbiol 27: 409-419.
28. Hajishengallis, G., Liang, S., Payne, M.A. et al. (2011) Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe, 10: 497-506.
29. Hasegawa, Y., Nishiyama, S., Nishikawa, K. et al. (2003) A novel type of two-component regulatory system affecting gingipains in Porphyromonas gingivalis. Microbiol Immunol 47: 849-858.
30. Haurat, M.F., Aduse-Opoku, J., Rangarajan, M. et al. (2011) Selective sorting of cargo proteins into bacterial membrane vesicles. J Biol Chem 286: 1269-1276.
31. Henry, L.G., Sandberg, L., Zhang, K. and Fletcher, H.M. (2008) DNA repair of 8-oxo-7, 8-dihydroguanine lesions in Porphyromonas gingivalis. J Bacteriol 190: 7985-7993.
32. Henry, L.G., McKenzie, R.M., Robles, A. and Fletcher, H.M. (2012) Oxidative stress resistance in Porphyromonas gingivalis. Future Microbiol 7: 497-512.
33. Holt, S.C. and Ebersole, J.L. (2000) Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the "red complex", a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000 38: 72-122.
34. Iijima, R., Takahashi, H., Namme, R., Ikegami, S. and Yamazaki, M. (2004) Novel biological function of sialic acid (N-acetylneuraminic acid) as a hydrogen peroxide scavenger. FEBS Lett 561: 163-166.
35. Johnson, N.A., McKenzie, R., McLean, L., Sowers, L.C. and Fletcher, H.M. (2004) 8-oxo-7, 8-dihydroguanine is removed by a nucleotide excision repair-like mechanism in Porphyromonas gingivalis W83. J Bacteriol 186: 7697-7703.
36. Kadowaki, T., Nakayama, K., Okamoto, K. et al. (2000) Porphyromonas gingivalis proteinases as virulence determinants in progression of periodontal diseases. J Biochem 128: 153-159.
37. Kilian, M. (1998) Clonal basis of bacterial virulence. In: Guggenheim B., Shapiro S., eds. Oral Biology at the Turn of the Century. S. Basel, Switzerland: Karger AG.
38. Kumar, P.S., Griffen, A.L., Barton, J.A., Paster, B.J., Moeschberger, M.L. and Leys, E.J. (2003) New bacterial species associated with chronic periodontitis. J Dent Res 82: 338-344.
39. Lamont, R.J and Jenkinson, H.F. (1998) Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol Mol Biol Rev 62: 1244-1263.
40. Lewis, J.P., Iyer, D. and Anaya-Bergman, C. (2009) Adaptation of Porphyromonas gingivalis to microaerophilic conditions involves increased consumption of formate and reduced utilization of lactate. Microbiology 155: 3758-3774.
41. Lima, B.P., Antelmann, H., Gronau, K. et al. (2011) Involvement of protein acetylation in glucose-induced transcription of a stress-responsive promoter. Mol Microbiol 81: 1190-1204.
42. Mahmud, T., Wenzel, S.C., Wan, E. et al. (2005) A biosynthetic pathway to isovaleryl-CoA in myxobacteria: the involvement of the mevalonate pathway. ChemBioChem 6: 322-330.
43. Marraffini, L.A., Dedent, A.C. and Schneewind, O. (2006) Sortases and the art of anchoring proteins to the envelopes of gram-positive bacteria. Microbiol Mol Biol Rev 70: 192-221.
44. Mazmanian, S.K., Ton-That, H. and Schneewind, O. (2001) Sortase-catalysed anchoring of surface proteins to the cell wall of Staphylococcus aureus. Mol Microbiol 40: 1049-1057.
45. McKenzie, R.M., Johnson, N.N., Aruni, W., Dou, Y., Masinde, G. and Fletcher, H.M. (2012) Differential response of Porphyromonas gingivalis to varying levels and duration of hydrogen peroxide-induced oxidative stress. Microbiology 158: 2465-2479.
46. Meuric, V., Gracieux, P., Tamanai-Shacoori, Z., Perez-Chaparro, J. and Bonnaure-Mallet, M. (2008) Expression patterns of genes induced by oxidative stress in Porphyromonas gingivalis. Oral Microbiol Immunol 23: 308-314.
47. Moynihan, P.J. and Clarke, A.J. (2011) O-Acetylated peptidoglycan: controlling the activity of bacterial autolysins and lytic enzymes of innate immune systems. Int J Biochem Cell Biol 43: 1655-1659.
48. Mydel, P., Takahashi, Y., Yumoto, H. et al. (2006) Roles of the host oxidative immune response and bacterial antioxidant rubrerythrin during Porphyromonas gingivalis infection. PLoS Pathog 2: e76.
49. Nguyen, K.A., Travis, J. and Potempa, J. (2007) Does the importance of the C-terminal residues in the maturation of RgpB from Porphyromonas gingivalis reveal a novel mechanism for protein export in a subgroup of Gram-negative bacteria? J Bacteriol 189: 833-843.
50. Nishikawa, K. and Duncan, M.J. (2010) Histidine kinase-mediated production and autoassembly of Porphyromonas gingivalis fimbriae. J Bacteriol 192: 1975-1987.
51. Okamoto, K., Nakayama, K., Kadowaki, T., Abe, N., Ratnayake, D.B. and Yamamoto, K. (1998) Involvement of a lysine-specific cysteine proteinase in hemoglobin adsorption and heme accumulation by Porphyromonas gingivalis. J Biol Chem 273: 21225-21231.
52. Olango, G.J., Roy, F., Sheets, S.M., Young, M.K. and Fletcher, H.M. (2003) Gingipain RgpB is excreted as a proenzyme in the vimA-defective mutant Porphyromonas gingivalis FLL92. Infect Immun 71: 3740-3747.
53. Osbourne, D.O., Aruni, W., Roy, F. et al. (2010) The role of vimA in cell surface biogenesis in Porphyromonas gingivalis. Microbiology 156: 2180-2193.
54. Osbourne, D., Wilson Aruni, A., Dou, Y. et al. (2012) VimA dependent modulation of secretome in Porphyromonas gingivalis. Mol Oral Microbiol 27: 420-435.
55. Pallen, M.J., Lam, A.C., Antonio, M. and Dunbar, K. (2001) An embarrassment of sortases - a richness of substrates? Trends Microbiol 9: 97-102.
56. Rangarajan, M., Hashim, A., Aduse-Opoku, J., Paramonov, N., Hounsell, E.F. and Curtis, M.A. (2005) Expression of Arg-Gingipain RgpB is required for correct glycosylation and stability of monomeric Arg-gingipain RgpA from Porphyromonas gingivalis W50. Infect Immun 73: 4864-4878.
57. Rangarajan, M., Aduse-Opoku, J., Paramonov, N. et al. (2008) Identification of a second lipopolysaccharide in Porphyromonas gingivalis W50. J Bacteriol 190: 2920-2932.
58. Roy, F., Vanterpool, E. and Fletcher, H.M. (2006) HtrA in Porphyromonas gingivalis can regulate growth and gingipain activity under stressful environmental conditions. Microbiology 152: 3391-3398.
59. Saiki, K. and Konishi, K. (2010) The role of Sov protein in the secretion of gingipain protease virulence factors of Porphyromonas gingivalis. FEMS Microbiol Lett 302: 166-174.
60. Sakai, E., Naito, M., Sato, K. et al. (2007) Construction of recombinant hemagglutinin derived from the gingipain-encoding gene of Porphyromonas gingivalis, identification of its target protein on erythrocytes, and inhibition of hemagglutination by an interdomain regional peptide. J Bacteriol 189: 3977-3986.
61. Sato, K., Kido, N., Murakami, Y., Hoover, C.I., Nakayama, K. and Yoshimura, F. (2009) Lipopolysaccharide biosynthesis-related genes are required for colony pigmentation of Porphyromonas gingivalis. Microbiology 155: 1282-1293.
62. Sato, K., Naito, M., Yukitake, H. et al. (2010) A protein secretion system linked to bacteroidete gliding motility and pathogenesis. Proc Natl Acad Sci U S A 107: 276-281.
63. Schneewind, O., Fowler, A. and Faull, K.F. (1995) Structure of the cell wall anchor of surface proteins in Staphylococcus aureus. Science 268: 103-106.
64. Seers, C.A., Slakeski, N., Veith, P.D. et al. (2006) The RgpB C-terminal domain has a role in attachment of RgpB to the outer membrane and belongs to a novel C-terminal-domain family found in Porphyromonas gingivalis. J Bacteriol 188: 6376-6386.
65. Sheets, S.M., Robles-Price, A.G., McKenzie, R.M., Casiano, C.A. and Fletcher, H.M. (2008) Gingipain-dependent interactions with the host are important for survival of Porphyromonas gingivalis. Front Biosci, 13: 3215-3238.
66. Shoji, M., Ratnayake, D.B., Shi, Y. et al. (2002) Construction and characterization of a nonpigmented mutant of Porphyromonas gingivalis: cell surface polysaccharide as an anchorage for gingipains. Microbiology 148: 1183-1191.
67. Shoji, M., Sato, K., Yukitake, H. et al. (2011) Por secretion system-dependent secretion and glycosylation of Porphyromonas gingivalis hemin-binding protein 35. PLoS ONE, 6: e21372.
68. Slakeski, N., Seers, C.A., Ng, K. et al. (2011) C-terminal domain residues important for secretion and attachment of RgpB in Porphyromonas gingivalis. J Bacteriol 193: 132-142.
69. Smalley, J.W., Birss, A.J. and Silver, J. (2000) The periodontal pathogen Porphyromonas gingivalis harnesses the chemistry of the mu-oxo bishaem of iron protoporphyrin IX to protect against hydrogen peroxide. FEMS Microbiol Lett 183: 159-164.
70. Smalley, J.W., Thomas, M.F., Birss, A.J., Withnall, R. and Silver, J. (2004) A combination of both arginine- and lysine-specific gingipain activity of Porphyromonas gingivalis is necessary for the generation of the micro-oxo bishaem-containing pigment from haemoglobin. Biochem J 379: 833-840.
71. Smith, K.T. and Workman, J.L. (2009) Introducing the acetylome. Nat Biotechnol 27: 917-919.
72. Starai, V.J. and Escalante-Semerena, J.C. (2004) Identification of the protein acetyltransferase (Pat) enzyme that acetylates acetyl-CoA synthetase in Salmonella enterica. J Mol Biol 340: 1005-1012.
73. Starai, V.J., Gardner, J.G. and Escalante-Semerena, J.C. (2005) Residue Leu-641 of Acetyl-CoA synthetase is critical for the acetylation of residue Lys-609 by the Protein acetyltransferase enzyme of Salmonella enterica. J Biol Chem 280: 26200-26205.
74. Strahilevitz, J., Jacoby, G.A., Hooper, D.C. and Robicsek, A. (2009) Plasmid-mediated quinolone resistance: a multifaceted threat. Clin Microbiol Rev 22: 664-689.
75. Tatar, L.D., Marolda, C.L., Polischuk, A.N., van Leeuwen, D. and Valvano, M.A. (2007) An Escherichia coli undecaprenyl-pyrophosphate phosphatase implicated in undecaprenyl phosphate recycling. Microbiology 153: 2518-2529.
76. Thanassi, D.G. and Hultgren, S.J. (2000) Multiple pathways allow protein secretion across the bacterial outer membrane. Curr Opin Cell Biol 12: 420-430.
77. Ton-That, H., Marraffini, L.A. and Schneewind, O. (2004) Protein sorting to the cell wall envelope of Gram-positive bacteria. Biochim Biophys Acta 1694: 269-278.
78. Vanterpool, E., Roy, F. and 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 Immun 72: 5555-5564.
79. Vanterpool, E., Roy, F. and 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 Immun 73: 3971-3982.
80. Vanterpool, E., Roy, F., Sandberg, L. and Fletcher, H.M. (2005b) Altered gingipain maturation in vimA- and vimE-defective isogenic mutants of Porphyromonas gingivalis. Infect Immun 73: 1357-1366.
81. Vanterpool, E., Roy, F., Zhan, W., Sheets, S.M., Sandberg, L. and Fletcher, H.M. (2006) VimA is part of the maturation pathway for the major gingipains of Porphyromonas gingivalis W83. Microbiology 152: 3383-3389.
82. Vanterpool, E., Aruni, A.W., Roy, F. and Fletcher, H.M. (2010) regT can modulate gingipain activity and response to oxidative stress in Porphyromonas gingivalis. Microbiology 156: 3065-3072.
83. Yamaguchi, M., Sato, K., Yukitake, H., Noiri, Y., Ebisu, S. and Nakayama, K. (2010) A Porphyromonas gingivalis mutant defective in a putative glycosyltransferase exhibits defective biosynthesis of the polysaccharide portions of lipopolysaccharide, decreased gingipain activities, strong autoaggregation, and increased biofilm formation. Infect Immun 78: 3801-3812.
84. Yoshimura, F., Murakami, Y., Nishikawa, K., Hasegawa, Y. and Kawaminami, S. (2009) Surface components of Porphyromonas gingivalis. J Periodontal Res 44: 1-12.