A surface-exposed neuraminidase affects complement resistance and virulence of the oral spirochaete Treponema denticola

Molecular Microbiology

Volumn 89, Issue 5, 2013, Pages 842-856

  Kurniyati, Kurni ^a   Zhang, Weiyan ^a   Zhang, Kai ^a   Li, Chunhao ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOCONJUGATE; IMMUNOGLOBULIN G; PLASMA PROTEIN; SIALIC ACID; SIALIDASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CELL SURFACE; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME ACTIVITY; HUMAN; IN VIVO STUDY; MOUSE; NONHUMAN; NORMAL HUMAN; NUTRIENT UPTAKE; PERIODONTITIS; PRIORITY JOURNAL; SIALYLATION; SPIROCHETE; TISSUE INJURY; TREPONEMA DENTICOLA;

ANIMALIA; BACTERIA (MICROORGANISMS); MUS; MUS MUSCULUS; SPIROCHAETA; TREPONEMA DENTICOLA;

ANIMALS; BLOOD BACTERICIDAL ACTIVITY; BLOOD PROTEINS; COMPLEMENT SYSTEM PROTEINS; CULTURE MEDIA; DISEASE MODELS, ANIMAL; GENE DELETION; HUMANS; MEMBRANE PROTEINS; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; N-ACETYLNEURAMINIC ACID; NEURAMINIDASE; SURVIVAL ANALYSIS; TREPONEMA DENTICOLA; TREPONEMAL INFECTIONS; VIRULENCE;

EID: 84883204508     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12311     Document Type: Article

References (89)

1. Achyuthan, K.E., and Achyuthan, A.M. (2001) Comparative enzymology, biochemistry and pathophysiology of human exo-alpha-sialidases (neuraminidases). Comp Biochem Physiol B Biochem Mol Biol 129: 29-64.
2. Aruni, W., Vanterpool, E., Osbourne, D., Roy, F., Muthiah, A., Dou, Y., and Fletcher, H.M. (2011) Sialidase and sialoglycoproteases can modulate virulence in Porphyromonas gingivalis. Infect Immun 79: 2779-2791.
3. Avril, T., Wagner, E.R., Willison, H.J., and Crocker, P.R. (2006) Sialic acid-binding immunoglobulin-like lectin 7 mediates selective recognition of sialylated glycans expressed on Campylobacter jejuni lipooligosaccharides. Infect Immun 74: 4133-4141.
4. Barnes, M.G., and Weiss, A.A. (2001) BrkA protein of Bordetella pertussis inhibits the classical pathway of complement after C1 deposition. Infect Immun 69: 3067-3072.
5. Barrett, S., Mohr, P.G., Schmidt, P.M., and McKimm-Breschkin, J.L. (2011) Real time enzyme inhibition assays provide insights into differences in binding of neuraminidase inhibitors to wild type and mutant influenza viruses. PLoS ONE 6: e23627.
6. Ben, N.A., and Klimpel, G.R. (2008) Subversion of complement activation at the bacterial surface promotes serum resistance and opsonophagocytosis of Francisella tularensis. J Leukoc Biol 84: 77-85.
7. Berger, M., Birx, D.L., Wetzler, E.M., O'Shea, J.J., Brown, E.J., and Cross, A.S. (1985) Calcium requirements for increased complement receptor expression during neutrophil activation. J Immunol 135: 1342-1348.
8. Bian, J., Shen, H., Tu, Y., Yu, A., and Li, C. (2011) The riboswitch regulates a thiamine pyrophosphate ABC transporter of the oral spirochete Treponema denticola. J Bacteriol 193: 3912-3922.
9. Bian, J., Fenno, J.C., and Li, C. (2012) Development of a modified gentamicin resistance cassette for genetic manipulation of the oral spirochete Treponema denticola. Appl Environ Microbiol 78: 2059-2062.
10. Bian, X.L., Wang, H.T., Ning, Y., Lee, S.Y., and Fenno, J.C. (2005) Mutagenesis of a novel gene in the prcA-prtP protease locus affects expression of Treponema denticola membrane complexes. Infect Immun 73: 1252-1255.
11. Bickel, M., and Cimasoni, G. (1985) The pH of human crevicular fluid measured by a new microanalytical technique. J Periodontal Res 20: 35-40.
12. Brooks, C.S., Vuppala, S.R., Jett, A.M., and Akins, D.R. (2006) Identification of Borrelia burgdorferi outer surface proteins. Infect Immun 74: 296-304.
13. Cacalano, G., Kays, M., Saiman, L., and Prince, A. (1992) Production of the Pseudomonas aeruginosa neuraminidase is increased under hyperosmolar conditions and is regulated by genes involved in alginate expression. J Clin Invest 89: 1866-1874.
14. Cassidy, J.T., Jourdian, G.W., and Roseman, S. (1965) The sialic acids. VI. Purification and properties of sialidase from Clostridium perfringens. J Biol Chem 240: 3501-3506.
15. Chien, C.H., Shann, Y.J., and Sheu, S.Y. (1996) Site-directed mutations of the catalytic and conserved amino acids of the neuraminidase gene, nanH, of Clostridium perfringens ATCC 10543. Enzyme Microb Technol 19: 267-276.
16. Comb, D.G., and Roseman, S. (1960) The sialic acids. I. The structure and enzymatic synthesis of N-acetylneuraminic acid. J Biol Chem 235: 2529-2537.
17. Comstock, L.E., and Kasper, D.L. (2006) Bacterial glycans: key mediators of diverse host immune responses. Cell 126: 847-850.
18. Copley, R.R., Russell, R.B., and Ponting, C.P. (2001) Sialidase-like Asp-boxes: sequence-similar structures within different protein folds. Protein Sci 10: 285-292.
19. Crennell, S.J., Garman, E.F., Laver, W.G., Vimr, E.R., and Taylor, G.L. (1993) Crystal structure of a bacterial sialidase (from Salmonella typhimurium LT2) shows the same fold as an influenza virus neuraminidase. Proc Natl Acad Sci USA 90: 9852-9856.
20. Crocker, P.R., Paulson, J.C., and Varki, A. (2007) Siglecs and their roles in the immune system. Nat Rev Immunol 7: 255-266.
21. Crowley, J.F., Goldstein, I.J., Arnarp, J., and Lonngren, J. (1984) Carbohydrate binding studies on the lectin from Datura stramonium seeds. Arch Biochem Biophys 231: 524-533.
22. Darveau, R.P. (2010) Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol 8: 481-490.
23. Dramsi, S., Kocks, C., Forestier, C., and Cossart, P. (1993) Internalin-mediated invasion of epithelial cells by Listeria monocytogenes is regulated by the bacterial growth state, temperature and the pleiotropic activator prfA. Mol Microbiol 9: 931-941.
24. Eggert, F.M., Drewell, L., Bigelow, J.A., Speck, J.E., and Goldner, M. (1991) The pH of gingival crevices and periodontal pockets in children, teenagers and adults. Arch Oral Biol 36: 233-238.
25. Ellen, R.P., and Galimanas, V.B. (2005) Spirochetes at the forefront of periodontal infections. Periodontol 2000 38: 13-32.
26. Fenno, J.C., Hannam, P.M., Leung, W.K., Tamura, M., Uitto, V.J., and McBride, B.C. (1998) Cytopathic effects of the major surface protein and the chymotrypsin-like protease of Treponema denticola. Infect Immun 66: 1869-1877.
27. Fenno, J.C., Tamura, M., Hannam, P.M., Wong, G.W., Chan, R.A., and McBride, B.C. (2000) Identification of a Treponema denticola OppA homologue that binds host proteins present in the subgingival environment. Infect Immun 68: 1884-1892.
28. Figueira, M.A., Ram, S., Goldstein, R., Hood, D.W., Moxon, E.R., and Pelton, S.I. (2007) Role of complement in defense of the middle ear revealed by restoring the virulence of nontypeable Haemophilus influenzae siaB mutants. Infect Immun 75: 325-333.
29. Galen, J.E., Ketley, J.M., Fasano, A., Richardson, S.H., Wasserman, S.S., and Kaper, J.B. (1992) Role of Vibrio cholerae neuraminidase in the function of cholera toxin. Infect Immun 60: 406-415.
30. Gut, H., King, S.J., and Walsh, M.A. (2008) Structural and functional studies of Streptococcus pneumoniae neuraminidase B: an intramolecular trans-sialidase. FEBS Lett 582: 3348-3352.
31. Hajishengallis, G. (2010) Complement and periodontitis. Biochem Pharmacol 80: 1992-2001.
32. Hajishengallis, G., Darveau, R.P., and Curtis, M.A. (2012a) The keystone-pathogen hypothesis. Nat Rev Microbiol 10: 717-725.
33. Hajishengallis, G., Krauss, J.L., Liang, S., McIntosh, M.L., and Lambris, J.D. (2012b) Pathogenic microbes and community service through manipulation of innate immunity. Adv Exp Med Biol 946: 69-85.
34. Holt, S.C., and Ebersole, J.L. (2005) Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the 'red complex', a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000 38: 72-122.
35. Honma, K., Mishima, E., and Sharma, A. (2011) Role of Tannerella forsythia NanH sialidase in epithelial cell attachment. Infect Immun 79: 393-401.
36. Kaneko, Y., Nimmerjahn, F., and Ravetch, J.V. (2006) Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 313: 670-673.
37. Kesavalu, L., Walker, S.G., Holt, S.C., Crawley, R.R., and Ebersole, J.L. (1997) Virulence characteristics of oral treponemes in a murine model. Infect Immun 65: 5096-5102.
38. Lambris, J.D., Ricklin, D., and Geisbrecht, B.V. (2008) Complement evasion by human pathogens. Nat Rev Microbiol 6: 132-142.
39. Lamont, R.J., and Jenkinson, H.F. (2000) Subgingival colonization by Porphyromonas gingivalis. Oral Microbiol Immunol 15: 341-349.
40. Leprat, R., and Michel-Briand, Y. (1980) Extracellular neuraminidase production by a strain of Pseudomonas aeruginosa isolated from cystic fibrosis. Ann Microbiol (Paris) 131B: 209-222.
41. Li, C., Kurniyati, Hu, B., Bian, J., Sun, J., Zhang, W., etal. (2012) Abrogation of neuraminidase reduces biofilm formation, capsule biosynthesis, and virulence of Porphyromonas gingivalis. Infect Immun 80: 3-13.
42. Li, H., Ruby, J., Charon, N., and Kuramitsu, H. (1996) Gene inactivation in the oral spirochete Treponema denticola: construction of an flgE mutant. J Bacteriol 178: 3664-3667.
43. McDowell, J.V., Lankford, J., Stamm, L., Sadlon, T., Gordon, D.L., and Marconi, R.T. (2005) Demonstration of factor H-like protein 1 binding to Treponema denticola, a pathogen associated with periodontal disease in humans. Infect Immun 73: 7126-7132.
44. McDowell, J.V., Huang, B., Fenno, J.C., and Marconi, R.T. (2009) Analysis of a unique interaction between the complement regulatory protein factor H and the periodontal pathogen Treponema denticola. Infect Immun 77: 1417-1425.
45. McDowell, J.V., Frederick, J., Miller, D.P., Goetting-Minesky, M.P., Goodman, H., Fenno, J.C., and Marconi, R.T. (2011) Identification of the primary mechanism of complement evasion by the periodontal pathogen, Treponema denticola. Mol Oral Microbiol 26: 140-149.
46. Madico, G., Ngampasutadol, J., Gulati, S., Vogel, U., Rice, P.A., and Ram, S. (2007) Factor H binding and function in sialylated pathogenic neisseriae is influenced by gonococcal, but not meningococcal, porin. J Immunol 178: 4489-4497.
47. Moncla, B.J., and Braham, P. (1989) Detection of sialidase (neuraminidase) activity in Actinomyces species by using 2′-(4-methylumbelliferyl)alpha-D-N-acetylneuraminic acid in a filter paper spot test. J Clin Microbiol 27: 182-184.
48. 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.
49. Nimmerjahn, F., and Ravetch, J.V. (2008) Anti-inflammatory actions of intravenous immunoglobulin. Annu Rev Immunol 26: 513-533.
50. Ohta, K., Makinen, K.K., and Loesche, W.J. (1986) Purification and characterization of an enzyme produced by Treponema denticola capable of hydrolyzing synthetic trypsin substrates. Infect Immun 53: 213-220.
51. Pihlstrom, B.L., Michalowicz, B.S., and Johnson, N.W. (2005) Periodontal diseases. Lancet 366: 1809-1820.
52. Ponnio, M., Alho, H., Nikkari, S.T., Olsson, U., Rydberg, U., and Sillanaukee, P. (1999) Serum sialic acid in a random sample of the general population. Clin Chem 45: 1842-1849.
53. Popadiak, K., Potempa, J., Riesbeck, K., and Blom, A.M. (2007) Biphasic effect of gingipains from Porphyromonas gingivalis on the human complement system. J Immunol 178: 7242-7250.
54. Powell, L.D., and Varki, A.P. (2001) Sialidases. Curr Protoc Mol Biol Chapter 17: Unit17.
55. Ram, S., McQuillen, D.P., Gulati, S., Elkins, C., Pangburn, M.K., and Rice, P.A. (1998a) Binding of complement factor H to loop 5 of porin protein 1A: a molecular mechanism of serum resistance of nonsialylated Neisseria gonorrhoeae. J Exp Med 188: 671-680.
56. Ram, S., Sharma, A.K., Simpson, S.D., Gulati, S., McQuillen, D.P., Pangburn, M.K., and Rice, P.A. (1998b) A novel sialic acid binding site on factor H mediates serum resistance of sialylated Neisseria gonorrhoeae. J Exp Med 187: 743-752.
57. Ricklin, D., Hajishengallis, G., Yang, K., and Lambris, J.D. (2010) Complement: a key system for immune surveillance and homeostasis. Nat Immunol 11: 785-797.
58. Ritchie, G.E., Moffatt, B.E., Sim, R.B., Morgan, B.P., Dwek, R.A., and Rudd, P.M. (2002) Glycosylation and the complement system. Chem Rev 102: 305-319.
59. 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.
60. Rosen, G., Naor, R., Rahamim, E., Yishai, R., and Sela, M.N. (1995) Proteases of Treponema denticola outer sheath and extracellular vesicles. Infect Immun 63: 3973-3979.
61. Roy, S., Honma, K., Douglas, C.W., Sharma, A., and Stafford, G.P. (2011) Role of sialidase in glycoprotein utilization by Tannerella forsythia. Microbiology 157: 3195-3202.
62. Ruby, J.D., Li, H., Kuramitsu, H., Norris, S.J., Goldstein, S.F., Buttle, K.F., and Charon, N.W. (1997) Relationship of Treponema denticola periplasmic flagella to irregular cell morphology. J Bacteriol 179: 1628-1635.
63. Schenkein, H.A., and Genco, R.J. (1977a) Gingival fluid and serum in periodontal diseases. I. Quantitative study of immunoglobulins, complement components, and other plasma proteins. J Periodontol 48: 772-777.
64. Schenkein, H.A., and Genco, R.J. (1977b) Gingival fluid and serum in periodontal diseases. II. Evidence for cleavage of complement components C3, C3 proactivator (factor B) and C4 in gingival fluid. J Periodontol 48: 778-784.
65. Schenkein, H.A., Fletcher, H.M., Bodnar, M., and Macrina, F.L. (1995) Increased opsonization of a prtH-defective mutant of Porphyromonas gingivalis W83 is caused by reduced degradation of complement-derived opsonins. J Immunol 154: 5331-5337.
66. Schultz, C.P., Wolf, V., Lange, R., Mertens, E., Wecke, J., Naumann, D., and Zahringer, U. (1998) Evidence for a new type of outer membrane lipid in oral spirochete Treponema denticola. Functioning permeation barrier without lipopolysaccharides. J Biol Chem 273: 15661-15666.
67. Seshadri, R., Myers, G.S., Tettelin, H., Eisen, J.A., Heidelberg, J.F., Dodson, R.J., etal. (2004) Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. Proc Natl Acad Sci USA 101: 5646-5651.
68. Severi, E., Hood, D.W., and Thomas, G.H. (2007) Sialic acid utilization by bacterial pathogens. Microbiology 153: 2817-2822.
69. Sillanaukee, P., Ponnio, M., and Jaaskelainen, I.P. (1999) Occurrence of sialic acids in healthy humans and different disorders. Eur J Clin Invest 29: 413-425.
70. Socransky, S.S., and Haffajee, A.D. (2005) Periodontal microbial ecology. Periodontol 2000 38: 135-187.
71. Soong, G., Muir, A., Gomez, M.I., Waks, J., Reddy, B., Planet, P., etal. (2006) Bacterial neuraminidase facilitates mucosal infection by participating in biofilm production. J Clin Invest 116: 2297-2305.
72. Sze, C.W., and Li, C. (2011) Inactivation of bb0184, which encodes carbon storage regulator A, represses the infectivity of Borrelia burgdorferi. Infect Immun 79: 1270-1279.
73. Sze, C.W., Morado, D.R., Liu, J., Charon, N.W., Xu, H., and Li, C. (2011) Carbon storage regulator A (CsrA(Bb)) is a repressor of Borrelia burgdorferi flagellin protein FlaB. Mol Microbiol 82: 851-864.
74. Taylor, G. (1996) Sialidases: structures, biological significance and therapeutic potential. Curr Opin Struct Biol 6: 830-837.
75. 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.
76. Trappetti, C., Kadioglu, A., Carter, M., Hayre, J., Iannelli, F., Pozzi, G., etal. (2009) Sialic acid: a preventable signal for pneumococcal biofilm formation, colonization, and invasion of the host. J Infect Dis 199: 1497-1505.
77. Uchiyama, S., Carlin, A.F., Khosravi, A., Weiman, S., Banerjee, A., Quach, D., etal. (2009) The surface-anchored NanA protein promotes pneumococcal brain endothelial cell invasion. J Exp Med 206: 1845-1852.
78. Varki, A. (2007) Glycan-based interactions involving vertebrate sialic-acid-recognizing proteins. Nature 446: 1023-1029.
79. Varki, A. (2008) Sialic acids in human health and disease. Trends Mol Med 14: 351-360.
80. Veith, P.D., Dashper, S.G., O'Brien-Simpson, N.M., Paolini, R.A., Orth, R., Walsh, K.A., and Reynolds, E.C. (2009) Major proteins and antigens of Treponema denticola. Biochim Biophys Acta 1794: 1421-1432.
81. Vimr, E., and Lichtensteiger, C. (2002) To sialylate, or not to sialylate: that is the question. Trends Microbiol 10: 254-257.
82. Vimr, E.R. (1994) Microbial sialidases: does bigger always mean better? Trends Microbiol 2: 271-277.
83. 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.
84. Wang, M., Krauss, J.L., Domon, H., Hosur, K.B., Liang, S., Magotti, P., etal. (2010) Microbial hijacking of complement-toll-like receptor crosstalk. Sci Signal 3: ra11.
85. Wessels, M.R., Butko, P., Ma, M., Warren, H.B., Lage, A.L., and Carroll, M.C. (1995) Studies of group B streptococcal infection in mice deficient in complement component C3 or C4 demonstrate an essential role for complement in both innate and acquired immunity. Proc Natl Acad Sci USA 92: 11490-11494.
86. Wyss, C., Moter, A., Choi, B.K., Dewhirst, F.E., Xue, Y., Schupbach, P., etal. (2004) Treponema putidum sp. nov., a medium-sized proteolytic spirochaete isolated from lesions of human periodontitis and acute necrotizing ulcerative gingivitis. Int J Syst Evol Microbiol 54: 1117-1122.
87. Xu, H., Raddi, G., Liu, J., Charon, N.W., and Li, C. (2011) Chemoreceptors and flagellar motors are subterminally located in close proximity at the two cell poles in spirochetes. J Bacteriol 193: 2652-2656.
88. Yamazaki, T., Miyamoto, M., Yamada, S., Okuda, K., and Ishihara, K. (2006) Surface protease of Treponema denticola hydrolyzes C3 and influences function of polymorphonuclear leukocytes. Microbes Infect 8: 1758-1763.
89. Zipfel, P.F., and Skerka, C. (2009) Complement regulators and inhibitory proteins. Nat Rev Immunol 9: 729-740.