Sialic acid, periodontal pathogens and Tannerella forsythia: Stick around and enjoy the feast!

Molecular Oral Microbiology

Volumn 27, Issue 1, 2012, Pages 11-22

  Stafford, G ^a   Roy, S ^a   Honma, K ^b   Sharma, A ^b  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

Biofilm; Glycoproteins; Periodontitis; Sialic acid

Indexed keywords

SIALIC ACID; SIALIDASE;

AGGREGATIBACTER ACTINOMYCETEMCOMITANS; ANTIGEN RECOGNITION; CAMPYLOBACTER JEJUNI; FUSOBACTERIUM NUCLEATUM; GENE SEQUENCE; GUILLAIN BARRE SYNDROME; HAEMOPHILUS DUCREYI; HAEMOPHILUS INFLUENZAE; HUMAN; MEMBRANE TRANSPORT; MICROBIAL DIVERSITY; MOUTH FLORA; NEISSERIA MENINGITIDIS; NONHUMAN; PERIODONTITIS; PERIODONTIUM; PORPHYROMONAS GINGIVALIS; PROTEIN GLYCOSYLATION; REVIEW; SALMONELLA TYPHIMURIUM; STREPTOCOCCUS PNEUMONIAE; TANNERELLA FORSYTHENSIS; TREPONEMA DENTICOLA;

ANIMALS; BACTERIAL ADHESION; BACTEROIDES; BIOFILMS; HUMANS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR MIMICRY; N-ACETYLNEURAMINIC ACID; NEURAMINIDASE; PERIODONTITIS; VIRULENCE FACTORS;

EID: 84863406922     PISSN: 20411006     EISSN: 20411014     Source Type: Journal    
DOI: 10.1111/j.2041-1014.2011.00630.x     Document Type: Review

References (71)

1. Agnani, G., Tricot-Doleux, S., Du, L. and Bonnaure-Mallet, M. (2000) Adherence of Porphyromonas gingivalis to gingival epithelial cells: modulation of bacterial protein expression. Oral Microbiol Immunol 15: 48-52.
2. Amith, S.R., Jayanth, P., Franchuk, S. et al. (2009) Dependence of pathogen molecule-induced toll-like receptor activation and cell function on Neu1 sialidase. Glycoconj J 26: 1197-1212.
3. Amith, S.R., Jayanth, P., Franchuk, S. et al. (2010) Neu1 desialylation of sialyl alpha-2, 3-linked beta-galactosyl residues of TOLL-like receptor 4 is essential for receptor activation and cellular signaling. Cell Signal 22: 314-324.
4. Aruni, W., Vanterpool, E., Osbourne, D. et al. (2011) Sialidase and sialoglycoproteases can modulate virulence in Porphyromonas gingivalis. Infect Immun 79: 2779-27791.
5. Blanvillain, S., Meyer, D., Boulanger, A. et al. (2007) Plant carbohydrate scavenging through tonb-dependent receptors: a feature shared by phytopathogenic and aquatic bacteria. PLoS ONE 2: e224.
6. Bolstad, A.I., Jensen, H.B. and Bakken, V. (1996) Taxonomy, biology, and periodontal aspects of Fusobacterium nucleatum. Clin Microbiol Rev 9: 55-71.
7. Brigham, C.J. and Malamy, M.H. (2005) Characterization of the RokA and HexA broad-substrate-specificity hexokinases from Bacteroides fragilis and their role in hexose and N-acetylglucosamine utilization. J Bacteriol 187: 890-901.
8. Brigham, C., Caughlan, R., Gallegos, R., Dallas, M.B., Godoy, V.G. and Malamy, M.H. (2009) Sialic acid (N-acetyl neuraminic acid) utilization by Bacteroides fragilis requires a novel N-acetyl mannosamine epimerase. J Bacteriol 191: 3629-3638.
9. Carlin, A.F., Lewis, A.L., Varki, A. and Nizet, V. (2007) Group B streptococcal capsular sialic acids interact with siglecs (immunoglobulin-like lectins) on human leukocytes. J Bacteriol 189: 1231-1237.
10. Chou, W.K., Dick, S., Wakarchuk, W.W. and and Tanner, M.E. (2005) Identification and characterization of NeuB3 from Campylobacter jejuni as a pseudaminic acid synthase. J Biol Chem 280: 35922-35928.
11. Condemine, G., Berrier, C., Plumbridge, J. and Ghazi, A. (2005) Function and expression of an N-acetylneuraminic acid-inducible outer membrane channel in Escherichia coli. J Bacteriol 187: 1959-1965.
12. Corfield, T. (1992) Bacterial sialidases - roles in pathogenicity and nutrition. Glycobiology 2: 509-521.
13. Curtis, M.A., Hanley, S.A. and Aduse-Opoku, J. (1999) The rag locus of Porphyromonas gingivalis: a novel pathogenicity island. J Periodontal Res 34: 400-405.
14. Dahl, U., Jaeger, T., Nguyen, B.T., Sattler, J.M. and Mayer, C. (2004) Identification of a phosphotransferase system of Escherichia coli required for growth on N-acetylmuramic acid. J Bacteriol 186: 2385-2392.
15. Dalia, A.B., Standish, A.J. and Weiser, J.N. (2010) Three surface exoglycosidases from Streptococcus pneumoniae, NanA, BgaA, and StrH, promote resistance to opsonophagocytic killing by human neutrophils. Infect Immun 78: 2108-2116.
16. Fischer, M., Zhang, Q.Y., Hubbard, R.E. and Thomas, G.H. (2010) Caught in a TRAP: substrate-binding proteins in secondary transport. Trends Microbiol 18: 471-478.
17. Fletcher, C.M., Coyne, M.J. and Comstock, L.E. (2011) Theoretical and experimental characterization of the scope of protein O-glycosylation in Bacteroides fragilis. J Biol Chem 286: 3219-3226.
18. Gibbons, R.J., Hay, D.I., Childs, W.C. III and Davis, G. (1990) Role of cryptic receptors (cryptitopes) in bacterial adhesion to oral surfaces. Arch Oral Biol 35(Suppl): 107S-114S.
19. Godoy, V.G., Dallas, M.M., Russo, T.A. and Malamy, M.H. (1993) A role for Bacteroides fragilis neuraminidase in bacterial growth in two model systems. Infect Immun 61: 4415-4426.
20. Hallen, U., Angstrom, J. and Bjorkner, A.E. (2008) Glycolipid binding epitopes involved in adherence of the periodontitis-associated bacterium Porphyromonas gingivalis. Glycoconj J 25: 561-572.
21. Honma, K., Inagaki, S., Okuda, K., Kuramitsu, H.K. and Sharma, A. (2007) Role of a Tannerella forsythia exopolysaccharide synthesis operon in biofilm development. Microb Pathog 42: 156-166.
22. Honma, K., Mishima, E. and Sharma, A. (2011) Role of Tannerella forsythia NanH sialidase in epithelial cell attachment. Infect Immun 79: 393-401.
23. Hood, D.W., Cox, A.D., Gilbert, M. et al. (2001) Identification of a lipopolysaccharide alpha-2, 3-sialyltransferase from Haemophilus influenzae. Mol Microbiol 39: 341-350.
24. Ilg, K., Yavuz, E., Maffioli, C., Priem, B. and Aebi, M. (2010) Glycomimicry: display of the GM3 sugar epitope on Escherichia coli and Salmonella enterica sv Typhimurium. Glycobiology 10: 1289-1297.
25. Juncker, A.S., Willenbrock, H., Von Heijne, G., Brunak, S., Nielsen, H. and Krogh, A. (2003) Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 12: 1652-1662.
26. Kapatral, V., Anderson, I., Ivanova, N. et al. (2002) Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 25586. J Bacteriol 184: 2005-2018.
27. King, S.J., Hippe, K.R. and Weiser, J.N. (2006) Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae. Mol Microbiol 59: 961-974.
28. Koebnik, R. (2005) TonB-dependent trans-envelope signalling: the exception or the rule? Trends Microbiol 13: 343-347.
29. Krivan, H.C., Roberts, D.D. and Ginsburg, V. (1988) Many pulmonary pathogenic bacteria bind specifically to the carbohydrate sequence GalNAc beta 1-4Gal found in some glycolipids. Proc Natl Acad Sci U S A 85: 6157-6161.
30. Litzinger, S., Duckworth, A., Nitzsche, K., Risinger, C., Wittmann, V. and Mayer, C. (2010) Muropeptide rescue in Bacillus subtilis involves sequential hydrolysis by beta-N-acetylglucosaminidase and N-acetylmuramyl-l-alanine amidase. J Bacteriol 192: 3132-3143.
31. Mikx, F.H. and Keulers, R.A. (1992) Hemagglutination activity of Treponema denticola grown in serum-free medium in continuous culture. Infect Immun 60: 1761-1766.
32. Moncla, B.J., Braham, P. and Hillier, S.L. (1990) Sialidase (neuraminidase) activity among gram-negative anaerobic and capnophilic bacteria. J Clin Microbiol 28: 422-425.
33. Murakami, Y., Higuchi, N., Nakamura, H., Yoshimura, F. and Oppenheim, F.G. (2002) Bacteroides forsythus hemagglutinin is inhibited by N-acetylneuraminyllactose. Oral Microbiol Immunol 17: 125-128.
34. Murray, P.A., Kern, D.G. and Winkler, J.R. (1988) Identification of a galactose-binding lectin on Fusobacterium nucleatum FN-2. Infect Immun 56: 1314-1319.
35. Nagano, K., Murakami, Y., Nishikawa, K., Sakakibara, J., Shimozato, K. and Yoshimura, F. (2007) Characterization of RagA and RagB in Porphyromonas gingivalis: study using gene-deletions mutants. J Med Microbiol 56: 1536-1548.
36. Okuda, K., Ono, M. and Kato, T. (1989) Neuraminidase-enhanced attachment of Bacteroides intermedius to human erythrocytes and buccal epithelial cells. Infect Immun 57: 1635-1637.
37. Oral Pathogen Sequence Database. (2008) Oral pathogen sequence databases [Internet]. Available from:.
38. Parker, D., Soong, G., Planet, P., Brower, J., Ratner, A.J. and Prince, A. (2009) The NanA neuraminidase of Streptococcus pneumoniae is involved in biofilm formation. Infect Immun 77: 3722-3730.
39. Plumbridge, J. (2009) An alternative route for recycling of N-acetylglucosamine from peptidoglycan involves the N-acetylglucosamine phosphotransferase system in Escherichia coli. J Bacteriol 191: 5641-5647.
40. Pollanen, M.T., Salonen, J.I. and Uitto, V.J. (2003) Structure and function of the tooth-epithelial interface in health and disease. Periodontol 2000 31: 12-31.
41. Post, D.M., Mungur, R., Gibson, B.W. and Munson, R.S. Jr (2005) Identification of a novel sialic acid transporter in Haemophilus ducreyi. Infect Immun 73: 6727-6735.
42. 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.
43. Reeves, A.R., Wang, G.R. and Salyers, A.A. (1997) Characterization of four outer membrane proteins that play a role in utilization of starch by Bacteroides thetaiotaomicron. J Bacteriol 179: 643-649.
44. Roggentin, P., Schauer, R., Hoyer, L.L. and Vimr, E.R. (1993) The sialidase superfamily and its spread by horizontal gene transfer. Mol Microbiol 9: 915-921.
45. Roy, S. (2010) Biofilm Formation and Sialic acid Utilisation by Tannerella forsythia, PhD thesis. The University of Sheffield, Sheffield, UK.
46. Roy, S., Douglas, C.W. and Stafford, G.P. (2010) A novel sialic acid utilization and uptake system in the periodontal pathogen Tannerella forsythia. J Bacteriol 192: 2285-2293.
47. Roy, S., Honma, K., Douglas, I., Sharma, A. and Stafford, G.P. (2011) Role of sialidase in glycoprotein utilisation by Tannerella forsythia. Microbiology 157: 3195-3202.
48. Severi, E., Hood, D.W. and Thomas, G.H. (2007) Sialic acid utilization by bacterial pathogens. Microbiology 153: 2817-2822.
49. Severi, E., Hosie, A.H.F., Hawkhead, J.A. and Thomas, G.H. (2010) Characterization of a novel sialic acid transporter of the sodium solute symporter (SSS) family and in vivo comparison with known bacterial sialic acid transporters. FEMS Microbiol Lett 304: 47-54.
50. Shakhnovich, E.A., King, S.J. and Weiser, J.N. (2002) Neuraminidase expressed by Streptococcus pneumoniae desialylates the lipopolysaccharide of Neisseria meningitidis and Haemophilus influenzae: a paradigm for interbacterial competition among pathogens of the human respiratory tract. Infect Immun 70: 7161-7164.
51. Sharma, A. (2011) Genome functions of Tannerella forsythia in bacterial communities. In: Kolenbrander P.E. ed. Oral Microbial Communities: Genome Inquiry and Interspecies Communication. Washington, DC: American Society for Microbiology, 135-147.
52. Sharma, A., Inagaki, S., Sigurdson, W. and Kuramitsu, H.K. (2005) Synergy between Tannerella forsythia and Fusobacterium nucleatum in biofilm formation. Oral Microbiol Immunol 20: 39-42.
53. Shell, D.M., Chiles, L., Judd, R.C., Seal, S. and Rest, R.F. (2002) The Neisseria lipooligosaccharide-specific alpha-2, 3-sialyltransferase is a surface-exposed outer membrane protein. Infect Immun 70: 3744-3751.
54. Socransky, S.S., Haffajee, A.D., Cugini, M.A., Smith, C. and Kent, R.L. Jr (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25: 134-144.
55. Sonnenburg, J.L., Xu, J., Leip, D.D. et al. (2005) Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307: 1955-1959.
56. Soong, G., Muir, A., Gomez, M.I. et al. (2006) Bacterial neuraminidase facilitates mucosal infection by participating in biofilm production. J Clin Invest 116: 2297-2305.
57. Stamatos, N.M., Carubelli, I., van de Vlekkert, D. et al. (2010) LPS-induced cytokine production in human dendritic cells is regulated by sialidase activity. J Leukoc Biol 88: 1227-1239.
58. Steenbergen, S.M., Lichtensteiger, C.A., Caughlan, R., Garfinkle, J., Fuller, T.E. and Vimr, E.R. (2005) Sialic acid metabolism and systemic pasteurellosis. Infect Immun 73: 1284-1294.
59. Steenbergen, S.M., Jirik, J.L. and Vimr, E.R. (2009) YjhS (NanS) is required for Escherichia coli to grow on 9-O-acetylated N-acetylneuraminic acid. J Bacteriol 191: 7134-7139.
60. Stinson, M.W., Safulko, K. and Levine, M.J. (1991) Adherence of Porphyromonas-(Bacteroides)-gingivalis to Streptococcus-sanguis in vitro. Infect Immu 59: 102-108.
61. Thompson, H., Homer, K.A., Rao, S., Booth, V. and Hosie, A.H. (2009) An orthologue of Bacteroides fragilis NanH is the principal sialidase in Tannerella forsythia. J Bacteriol 191: 3623-3628.
62. Uchiyama, S., Carlin, A.F., Khosravi, A. et al. (2009) The surface-anchored NanA protein promotes pneumococcal brain endothelial cell invasion. J Exp Med 206: 1845-1852.
63. Varki, A. and Diaz, S. (1983) A neuraminidase from Streptococcus sanguis that can release O-acetylated sialic acids. J Biol Chem 258: 12465-12471.
64. Varki, A. and Schauer, R. (2009) Sialic acids. In: Varki A., Cummings R.D., Esko J.D. eds. Essentials of Glycobiology. New York: Cold Spring Harbor Laboratory Press, 199-218.
65. Vimr, E. and Lichtensteiger, C. (2002) To sialylate, or not to sialylate: that is the question. Trends Microbiol 10: 254-257.
66. Vimr, E.R., Kalivoda, K.A., Deszo, E.L. and Steenbergen, S.M. (2004) Diversity of microbial sialic acid metabolism. Microbiol Mol Biol Rev 68: 132-153.
67. Wyss, C. (1989) Dependence of proliferation of Bacteroides-forsythus on exogenous N-acetylmuramic acid. Infect Immun 57: 1757-1759.
68. Xu, J. and Gordon, J.I. (2003) Inaugural article: honor thy symbionts. Proc Natl Acad Sci U S A 100: 10452-10459.
69. Xu, J., Bjursell, M.K., Himrod, J. et al. (2003) A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 299: 2074-2076.
70. Xu, J., Chiang, H.C., Bjursell, M.K. and Gordon, J.I. (2004) Message from a human gut symbiont: sensitivity is a prerequisite for sharing. Trends Microbiol 12: 21-28.
71. Xu, J., Mahowald, M.A., Ley, R.E. et al. (2007) Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol 5: e156.