Deletion of a 77-base-pair inverted repeat element alters the synthesis of surface polysaccharides in Porphyromonas gingivalis

Journal of Bacteriology

Volumn 197, Issue 7, 2015, Pages 1208-1220

  Bainbridge, Brian W ^a   Hirano, Takanori ^a,c   Grieshaber, Nicole ^b   Davey, Mary E ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF IDAHO   (United States)

^c KENNESAW STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL A ANTIGEN; BACTERIAL ANTIGEN; BACTERIAL POLYSACCHARIDE; BACTERIAL PROTEIN; COMPLEMENTARY RNA; GLYCOSYLTRANSFERASE; HISTONE; K ANTIGEN; MONOCLONAL ANTIBODY; O ANTIGEN; UNCLASSIFIED DRUG; LIPOPOLYSACCHARIDE; TRANSCRIPTOME;

ANTIBODY SPECIFICITY; ANTIGEN EXPRESSION; ARTICLE; BACTERIAL CAPSULE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM MUTANT; BASE PAIRING; CARBOHYDRATE SYNTHESIS; CONTROLLED STUDY; DELETION MUTANT; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE DELETION; GENE LOCUS; GENE OVEREXPRESSION; GROWTH RATE; IMMUNOBLOTTING; INVERTED REPEAT; NONHUMAN; OPEN READING FRAME; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANS ISOMER; TRANSMISSION ELECTRON MICROSCOPY; BIOSYNTHESIS; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY; REPRODUCIBILITY;

BACTERIA (MICROORGANISMS); PORPHYROMONAS GINGIVALIS;

BACTERIAL CAPSULES; GENE EXPRESSION REGULATION, BACTERIAL; LIPOPOLYSACCHARIDES; MUTATION; POLYSACCHARIDES, BACTERIAL; PORPHYROMONAS GINGIVALIS; REPRODUCIBILITY OF RESULTS; TRANSCRIPTOME;

EID: 84924706161     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02589-14     Document Type: Article

References (45)

1. Whitfield C. 2006. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75:39-68. http://dx.doi.org/10.1146/annurev.biochem.75.103004.142545.
2. Cress BF, Englaender JA, He W, Kasper D, Linhardt RJ, Koffas MA. 2014. Masquerading microbial pathogens: capsular polysaccharides mimic host-tissue molecules. FEMS Microbiol Rev 38:660-697. http://dx.doi.org/10.1111/1574-6976.12056.
3. Brunner J, Scheres N, El Idrissi NB, Deng DM, Laine ML, van Winkelhoff AJ, Crielaard W. 2010. The capsule of Porphyromonas gingivalis reduces the immune response of human gingival fibroblasts. BMC Microbiol 10:5. http://dx.doi.org/10.1186/1471-2180-10-5.
4. Singh A, Wyant T, Anaya-Bergman C, Aduse-Opoku J, Brunner J, Laine ML, Curtis MA, Lewis JP. 2011. The capsule of Porphyromonas gingivalis leads to a reduction in the host inflammatory response, evasion of phagocytosis, and increase in virulence. Infect Immun 79:4533-4542. http://dx.doi.org/10.1128/IAI.05016-11.
5. Laine ML, van Winkelhoff AJ. 1998. Virulence of six capsular serotypes of Porphyromonas gingivalis in a mouse model. Oral Microbiol Immunol 13:322-325. http://dx.doi.org/10.1111/j.1399-302X.1998.tb00714.x.
6. Irshad M, van der Reijden WA, Crielaard W, Laine ML. 2012. In vitro invasion and survival of Porphyromonas gingivalis in gingival fibroblasts; role of the capsule. Arch Immunol Ther Exp (Warsz) 60:469-476. http://dx.doi.org/10.1007/s00005-012-0196-8.
7. Rangarajan M, Aduse-Opoku J, Hashim A, Paramonov N, Curtis MA. 2013. Characterization of the alpha-and beta-mannosidases of Porphyromonas gingivalis. J Bacteriol 195:5297-5307. http://dx.doi.org/10.1128/JB.00898-13.
8. Paramonov N, Rangarajan M, Hashim A, Gallagher A, Aduse-Opoku J, Slaney JM, Hounsell E, Curtis MA. 2005. Structural analysis of a novel anionic polysaccharide from Porphyromonas gingivalis strain W50 related to Arg-gingipain glycans. Mol Microbiol 58:847-863. http://dx.doi.org/10.1111/j.1365-2958.2005.04871.x.
9. Rangarajan M, Aduse-Opoku J, Paramonov N, Hashim A, Bostanci N, Fraser OP, Tarelli E, Curtis MA. 2008. Identification of a second lipopolysaccharide in Porphyromonas gingivalis W50. J Bacteriol 190:2920-2932. http://dx.doi.org/10.1128/JB.01868-07.
10. Farquharson SI, Germaine GR, Gray GR. 2000. Isolation and characterization of the cell-surface polysaccharides of Porphyromonas gingivalis ATCC 53978. Oral Microbiol Immunol 15:151-157. http://dx.doi.org/10.1034/j.1399-302x.2000.150302.x.
11. Paramonov N, Bailey D, Rangarajan M, Hashim A, Kelly G, Curtis MA, Hounsell EF. 2001. Structural analysis of the polysaccharide from the lipopolysaccharide of Porphyromonas gingivalis strain W50. Eur J Biochem 268:4698-4707. http://dx.doi.org/10.1046/j.1432-1327.2001.02397.x.
12. Curtis MA, Thickett A, Slaney JM, Rangarajan M, Aduse-Opoku J, Shepherd P, Paramonov N, Hounsell EF. 1999. Variable carbohydrate modifications to the catalytic chains of the RgpA and RgpB proteases of Porphyromonas gingivalis W50. Infect Immun 67:3816-3823.
13. Shoji M, Sato K, Yukitake H, Naito M, Nakayama K. 2014. Involvement of the Wbp pathway in the biosynthesis of Porphyromonas gingivalis lipopolysaccharide with anionic polysaccharide. Sci Rep 4:5056. http://dx.doi.org/10.1038/srep05056.
14. Slaney JM, Curtis MA. 2008. Mechanisms of evasion of complement by Porphyromonas gingivalis. Front Biosci 13:188-196. http://dx.doi.org/10.2741/2669.
15. Slaney JM, Gallagher A, Aduse-Opoku J, Pell K, Curtis MA. 2006. Mechanisms of resistance of Porphyromonas gingivalis to killing by serum complement. Infect Immun 74:5352-5361. http://dx.doi.org/10.1128/IAI.00304-06.
16. Sims TJ, Schifferle RE, Ali RW, Skaug N, Page RC. 2001. Immunoglobulin G response of periodontitis patients to Porphyromonas gingivalis capsular carbohydrate and lipopolysaccharide antigens. Oral Microbiol Immunol 16:193-201. http://dx.doi.org/10.1034/j.1399-302X.2001.160401.x.
17. van Winkelhoff AJ, Appelmelk BJ, Kippuw N, de Graaff J. 1993. K-antigens in Porphyromonas gingivalis are associated with virulence. Oral Microbiol Immunol 8:259-265. http://dx.doi.org/10.1111/j.1399-302X.1993.tb00571.x.
18. Nelson KE, Fleischmann RD, DeBoy RT, Paulsen IT, Fouts DE, Eisen JA, Daugherty SC, Dodson RJ, Durkin AS, Gwinn M, Haft DH, Kolonay JF, Nelson WC, Mason T, Tallon L, Gray J, Granger D, Tettelin H, Dong H, Galvin JL, Duncan MJ, Dewhirst FE, Fraser CM. 2003. Complete genome sequence of the oral pathogenic bacterium Porphyromonas gingivalis strain W83. J Bacteriol 185:5591-5601. http://dx.doi.org/10.1128/JB.185.18.5591-5601.2003.
19. Aduse-Opoku J, Slaney JM, Hashim A, Gallagher A, Gallagher RP, Rangarajan M, Boutaga K, Laine ML, Van Winkelhoff AJ, Curtis MA. 2006. Identification and characterization of the capsular polysaccharide (K-antigen) locus of Porphyromonas gingivalis. Infect Immun 74:449-460. http://dx.doi.org/10.1128/IAI.74.1.449-460.2006.
20. Davey ME, Duncan MJ. 2006. Enhanced biofilm formation and loss of capsule synthesis: deletion of a putative glycosyltransferase in Porphyromonas gingivalis. J Bacteriol 188:5510-5523. http://dx.doi.org/10.1128/JB.01685-05.
21. Nakao R, Senpuku H, Watanabe H. 2006. Porphyromonas gingivalis galE is involved in lipopolysaccharide O-antigen synthesis and biofilm formation. Infect Immun 74:6145-6153. http://dx.doi.org/10.1128/IAI.00261-06.
22. Maeda K, Tribble GD, Tucker CM, Anaya C, Shizukuishi S, Lewis JP, Demuth DR, Lamont RJ. 2008. A Porphyromonas gingivalis tyrosine phosphatase is a multifunctional regulator of virulence attributes. Mol Microbiol 69:1153-1164. http://dx.doi.org/10.1111/j.1365-2958.2008.06338.x.
23. Simionato MR, Tucker CM, Kuboniwa M, Lamont G, Demuth DR, Tribble GD, Lamont RJ. 2006. Porphyromonas gingivalis genes involved in community development with Streptococcus gordonii. Infect Immun 74:6419-6428. http://dx.doi.org/10.1128/IAI.00639-06.
24. Wright CJ, Xue P, Hirano T, Liu C, Whitmore SE, Hackett M, Lamont RJ. 2014. Characterization of a bacterial tyrosine kinase in Porphyromonas gingivalis involved in polymicrobial synergy. Microbiologyopen 3:383-394. http://dx.doi.org/10.1002/mbo3.177.
25. Alberti-Segui C, Arndt A, Cugini C, Priyadarshini R, Davey ME. 2010. HU protein affects transcription of surface polysaccharide synthesis genes in Porphyromonas gingivalis. J Bacteriol 192:6217-6229. http://dx.doi.org/10.1128/JB.00106-10.
26. Priyadarshini R, Cugini C, Arndt A, Chen T, Tjokro NO, Goodman SD, Davey ME. 2013. The nucleoid-associated protein HUβ affects global gene expression in Porphyromonas gingivalis. Microbiology 159:219-229. http://dx.doi.org/10.1099/mic.0.061002-0.
27. Tjokro NO, Rocco CJ, Priyadarshini R, Davey ME, Goodman SD. 2014. A biochemical analysis of the interaction of Porphyromonas gingivalis HU PG0121 protein with DNA. PLoS One 9:e93266. http://dx.doi.org/10.1371/journal.pone.0093266.
28. Veillard F, Potempa B, Poreba M, Drag M, Potempa J. 2012. Gingipain aminopeptidase activities in Porphyromonas gingivalis. Biol Chem 393: 1471-1476. http://dx.doi.org/10.1515/hsz-2012-0222.
29. Towbin H, Staehelin T, Gordon J. 1992. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. 1979. Biotechnology 24:145-149.
30. Hitchcock PJ, Brown TM. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol 154:269-277.
31. Tsai CM, Frasch CE. 1982. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 119:115-119. http://dx.doi.org/10.1016/0003-2697(82)90673-X.
32. Hirano T, Beck DA, Demuth DR, Hackett M, Lamont RJ. 2012. Deep sequencing of Porphyromonas gingivalis and comparative transcriptome analysis of a LuxS mutant. Front Cell Infect Microbiol 2:79. http://dx.doi.org/10.3389/fcimb.2012.00079.
33. Britton RA, Wen T, Schaefer L, Pellegrini O, Uicker WC, Mathy N, Tobin C, Daou R, Szyk J, Condon C. 2007. Maturation of the 5' end of Bacillus subtilis 16S rRNA by the essential ribonuclease YkqC/RNase J1. Mol Microbiol 63:127-138. http://dx.doi.org/10.1111/j.1365-2958.2006.05499.x.
34. Aruni AW, Robles A, Fletcher HM. 2013. VimA mediates multiple functions that control virulence in Porphyromonas gingivalis. Mol Oral Microbiol 28:167-180. http://dx.doi.org/10.1111/omi.12017.
35. Shoji M, Ratnayake DB, Shi Y, Kadowaki T, Yamamoto K, Yoshimura F, Akamine A, Curtis MA, Nakayama K. 2002. Construction and characterization of a nonpigmented mutant of Porphyromonas gingivalis: cell surface polysaccharide as an anchorage for gingipains. Microbiology 148: 1183-1191.
36. Osbourne DO, Aruni W, Roy F, Perry C, Sandberg L, Muthiah A, Fletcher HM. 2010. Role of vimA in cell surface biogenesis in Porphyromonas gingivalis. Microbiology 156:2180-2193. http://dx.doi.org/10.1099/mic.0.038331-0.
37. Chatzidaki-Livanis M, Coyne MJ, Comstock LE. 2009. A family of transcriptional antitermination factors necessary for synthesis of the capsular polysaccharides of Bacteroides fragilis. J Bacteriol 191:7288-7295. http://dx.doi.org/10.1128/JB.00500-09.
38. Henkin TM, Yanofsky C. 2002. Regulation by transcription attenuation in bacteria: how RNA provides instructions for transcription termination/antitermination decisions. Bioessays 24:700-707. http://dx.doi.org/10.1002/bies.10125.
39. Gottesman S, Storz G. 2011. Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb Perspect Biol 3:a003798. http://dx.doi.org/10.1101/cshperspect.a003798.
40. Repoila F, Majdalani N, Gottesman S. 2003. Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli: the RpoS paradigm. Mol Microbiol 48:855-861. http://dx.doi.org/10.1046/j.1365-2958.2003.03454.x.
41. Georg J, Hess WR. 2011. cis-Antisense RNA, another level of gene regulation in bacteria. Microbiol Mol Biol Rev 75:286-300. http://dx.doi.org/10.1128/MMBR.00032-10.
42. Thomason MK, Storz G. 2010. Bacterial antisense RNAs: how many are there, and what are they doing? Annu Rev Genet 44:167-188. http://dx.doi.org/10.1146/annurev-genet-102209-163523.
43. Gimpel M, Heidrich N, Mader U, Krugel H, Brantl S. 2010. A dualfunction sRNA from B. subtilis: SR1 acts as a peptide encoding mRNA on the gapA operon. Mol Microbiol 76:990-1009. http://dx.doi.org/10.1111/j.1365-2958.2010.07158.x.
44. Fletcher HM, Schenkein HA, Morgan RM, Bailey KA, Berry CR, Macrina FL. 1995. Virulence of a Porphyromonas gingivalis W83 mutant defective in the prtH gene. Infect Immun 63:1521-1528.
45. Gardner RG, Russell JB, Wilson DB, Wang GR, Shoemaker NB. 1996. Use of a modified Bacteroides-Prevotella shuttle vector to transfer a reconstructed beta-1,4-D-endoglucanase gene into Bacteroides uniformis and Prevotella ruminicola B(1)4. Appl Environ Microbiol 62:196-202.