Abrogation of neuraminidase reduces biofilm formation, capsule biosynthesis, and virulence of Porphyromonas gingivalis

Infection and Immunity

Volumn 80, Issue 1, 2012, Pages 3-13

  Li, Chen ^a,b   Kurniyati, ^a   Hu, Bo ^c   Bian, Jiang ^a   Sun, Jianlan ^d   Zhang, Weiyan ^a   Liu, Jun ^c   Pan, Yaping ^b   Li, Chunhao ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b CHINA MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^d UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT; GLYCOSIDE; PG0352 PROTEIN; SIALIC ACID; SIALIDASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR; N ACETYLNEURAMINIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL INFECTION; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; BIOFILM; BIOSYNTHESIS; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; ENZYME ACTIVITY; FEMALE; GENE DELETION; GENETIC TRANSCRIPTION; IN VIVO STUDY; MEMBRANE FORMATION; MOUSE; NONHUMAN; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SURVIVAL; TOMOGRAPHY; AMINO ACID SEQUENCE; ANIMAL; BACTEROIDACEAE INFECTION; CYTOCHEMISTRY; DISEASE MODEL; ELECTRON TOMOGRAPHY; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN EXPERIMENT; LIVER; LUNG; METABOLISM; MICROBIOLOGY; MORTALITY; PATHOLOGY; PHYSIOLOGY; PROMOTER REGION; SEQUENCE ALIGNMENT; ULTRASTRUCTURE; VIRULENCE;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL CAPSULES; BACTEROIDACEAE INFECTIONS; BIOFILMS; CRYOELECTRON MICROSCOPY; DISEASE MODELS, ANIMAL; ELECTRON MICROSCOPE TOMOGRAPHY; GENE DELETION; HISTOCYTOCHEMISTRY; HUMAN EXPERIMENTATION; LIVER; LUNG; MICE; N-ACETYLNEURAMINIC ACID; NEURAMINIDASE; PORPHYROMONAS GINGIVALIS; PROMOTER REGIONS, GENETIC; SEQUENCE ALIGNMENT; SURVIVAL ANALYSIS; TRANSCRIPTION, GENETIC; VIRULENCE;

EID: 84863231535     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05773-11     Document Type: Article

References (84)

1. Achyuthan KE, Achyuthan AM. 2001. Comparative enzymology, biochemistry, and pathophysiology of human exo-α-sialidases (neuraminidases). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 129:29-64.
2. Aduse-Opoku J, et al. 2006. Identification and characterization of the capsular polysaccharide (K-antigen) locus of Porphyromonas gingivalis. Infect. Immun. 74:449-460.
3. Aruni W, et al. 2011. Sialidase and sialoglycoproteases can modulate virulence in Porphyromonas gingivalis. Infect. Immun. 79:2779-2791.
4. Boone D, Castenholtz RW (ed). 2001. Bergey's manual of systematic bacteriology, 2nd ed, vol 1. Springer-Verlag, New York, NY.
5. Bouchet V, et al. 2003. Host-derived sialic acid is incorporated into Haemophilus influenzae lipopolysaccharide and is a major virulence factor in experimental otitis media. Proc. Natl. Acad. Sci. U. S. A. 100:8898-8903.
6. Brien-Simpson NM, Veith PD, Dashper SG, Reynolds EC. 2003. Porphyromonas gingivalis gingipains: the molecular teeth of a microbial vampire. Curr. Protein Pept. Sci. 4:409-426.
7. Brunner J, Crielaard W, Van Winkelhoff AJ. 2008. Analysis of the capsular polysaccharide biosynthesis locus of Porphyromonas gingivalis and development of a K1-specific polymerase chain reaction-based serotyping assay. J. Periodontal Res. 43:698-705.
8. Cacalano G, Kays M, Saiman L, 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.
9. Chen W, Honma K, Sharma A, Kuramitsu HK. 2006. A universal stress protein of Porphyromonas gingivalis is involved in stress responses and biofilm formation. FEMS Microbiol. Lett. 264:15-21.
10. Chien CH, Shann YJ, Sheu SY. 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.
11. Comstock LE, Kasper DL. 2006. Bacterial glycans: key mediators of diverse host immune responses. Cell 126:847-850.
12. Copley RR, Russell RB, Ponting CP. 2001. Sialidase-like Asp-boxes: sequence-similar structures within different protein folds. Protein Sci. 10:285-292.
13. Crennell SJ, Garman EF, Laver WG, Vimr ER, Taylor GL. 1993. Crystal structure of a bacterial sialidase (from Salmonella typhimurium LT2) shows the same fold as an influenza virus neuraminidase. Proc. Natl. Acad. Sci. U. S. A. 90:9852-9856.
14. Crowley JF, Goldstein IJ, Arnarp J, Lonngren J. 1984. Carbohydrate binding studies on the lectin from Datura stramonium seeds. Arch. Biochem. Biophys. 231:524-533.
15. 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.
16. Du J, et al. 2009. Metabolic glycoengineering: sialic acid and beyond. Glycobiology 19:1382-1401.
17. Ferrero MA, Aparicio LR. 2010. Biosynthesis and production of polysialic acids in bacteria. Appl. Microbiol. Biotechnol. 86:1621-1635.
18. Fletcher HM, et al. 1995. Virulence of a Porphyromonas gingivalis W83 mutant defective in the prtH gene. Infect. Immun. 63:1521-1528.
19. Gabriel MO, Grunheid T, Zentner A. 2005. Glycosylation pattern and cell attachment-inhibiting property of human salivary mucins. J. Periodontol. 76:1175-1181.
20. Galen JE, et al. 1992. Role of Vibrio cholerae neuraminidase in the function of cholera toxin. Infect. Immun. 60:406-415.
21. Gonzalez D, Tzianabos AO, Genco CA, Gibson FCIII. 2003. Immunization with Porphyromonas gingivalis capsular polysaccharide prevents P. gingivalis-elicited oral bone loss in a murine model. Infect. Immun. 71:2283-2287.
22. Grenier D, et al. 2003. Effect of inactivation of the Arg-and/or Lysgingipain gene on selected virulence and physiological properties of Porphyromonas gingivalis. Infect. Immun. 71:4742-4748.
23. Gut H, King SJ, Walsh MA. 2008. Structural and functional studies of Streptococcus pneumoniae neuraminidase B: an intramolecular transsialidase. FEBS Lett. 582:3348-3352.
24. Haase EM, Bonstein T, Palmer RJ, Jr, Scannapieco FA. 2006. Environmental influences on Actinobacillus actinomycetemcomitans biofilm formation. Arch. Oral Biol. 51:299-314.
25. Haase EM, Stream JO, Scannapieco FA. 2003. Transcriptional analysis of the 5' terminus of the flp fimbrial gene cluster from Actinobacillus actinomycetemcomitans. Microbiology 149:205-215.
26. Hamada N, Sojar HT, Cho MI, Genco RJ. 1996. Isolation and characterization of a minor fimbria from Porphyromonas gingivalis. Infect. Immun. 64:4788-4794.
27. Holt SC, Ebersole JL. 2005. Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the "red complex", a prototype polybacterial pathogenic consortium in periodontitis. Periodontol. 2000 38:72-122.
28. Honma K, Mishima E, Sharma A. 2011. Role of Tannerella forsythia NanH sialidase in epithelial cell attachment. Infect. Immun. 79:393-401.
29. Hsiao YS, Parker D, Ratner AJ, Prince A, Tong L. 2009. Crystal structures of respiratory pathogen neuraminidases. Biochem. Biophys. Res. Commun. 380:467-471.
30. Kesavalu L, Holt SC, Ebersole JL. 1997. Porphyromonas gingivalis virulence in a murine lesion model: effects of immune alterations. Microb. Pathog. 23:317-326.
31. Krapp S, et al. 2003. The crystal structure of murine CMP-5-Nacetylneuraminic acid synthetase. J. Mol. Biol. 334:625-637.
32. Kremer JR, Mastronarde DN, McIntosh JR. 1996. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116:71-76.
33. Kruse S, Kleineidam RG, Roggentin P, Schauer R. 1996. Expression and purification of a recombinant "small" sialidase from Clostridium perfringens A99. Protein Expr. Purif. 7:415-422.
34. Laine ML, Van Winkelhoff AJ. 1998. Virulence of six capsular serotypes of Porphyromonas gingivalis in a mouse model. Oral Microbiol. Immunol. 13:322-325.
35. Lamont RJ, et al. 1995. Porphyromonas gingivalis invasion of gingival epithelial cells. Infect. Immun. 63:3878-3885.
36. Lamont RJ, Jenkinson HF. 1998. Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol. Mol. Biol. Rev. 62:1244-1263.
37. Lamont RJ, Jenkinson HF. 2000. Subgingival colonization by Porphyromonas gingivalis. Oral Microbiol. Immunol. 15:341-349.
38. Leprat R, Michel-Briand Y. 1980. Extracellular neuraminidase production by a strain of Pseudomonas aeruginosa isolated from cystic fibrosis. Ann. Microbiol. (Paris) 131B:209-222.
39. Limberger RJ, Slivienski LL, Izard J, Samsonoff WA. 1999. Insertional inactivation of Treponema denticola tap1 results in a nonmotile mutant with elongated flagellar hooks. J. Bacteriol. 181:3743-3750.
40. Liu J, et al. 2009. Intact flagellar motor of Borrelia burgdorferi revealed by cryo-electron tomography: evidence for stator ring curvature and rotor/ C-ring assembly flexion. J. Bacteriol. 191:5026-5036.
41. Lundholm M, et al. 2010. Variation in the Cd3 zeta (Cd247) gene correlates with altered T cell activation and is associated with autoimmune diabetes. J. Immunol. 184:5537-5544.
42. Mizanur RM, Pohl NL. 2008. Bacterial CMP-sialic acid synthetases: production, properties, and applications. Appl. Microbiol. Biotechnol. 80:757-765.
43. Moncla BJ, Braham P. 1989. Detection of sialidase (neuraminidase) activity in Actinomyces species by using 2'-(4-methylumbelliferyl)α-D-Nacetylneuraminic acid in a filter paper spot test. J. Clin. Microbiol. 27:182-184.
44. Moncla BJ, Braham P, Hillier SL. 1990. Sialidase (neuraminidase) activity among gram-negative anaerobic and capnophilic bacteria. J. Clin. Microbiol. 28:422-425.
45. Nelson KE, et al. 2003. Complete genome sequence of the oral pathogenic bacterium Porphyromonas gingivalis strain W83. J. Bacteriol. 185:5591-5601.
46. Olczak T, Wojtowicz H, Ciuraszkiewicz J, Olczak M. 2010. Species specificity, surface exposure, protein expression, immunogenicity, and participation in biofilm formation of Porphyromonas gingivalis HmuY. BMC Microbiol. 10:134.
47. Parker D, et al. 2009. The NanA neuraminidase of Streptococcus pneumoniae is involved in biofilm formation. Infect. Immun. 77:3722-3730.
48. Pihlstrom BL, Michalowicz BS, Johnson NW. 2005. Periodontal diseases. Lancet 366:1809-1820.
49. Powell LD, Varki AP. 2001. Sialidases. Curr. Protoc. Mol. Biol. Chapter 17:Unit 17.
50. Roggentin P, Schauer R, Hoyer LL, Vimr ER. 1993. The sialidase superfamily and its spread by horizontal gene transfer. Mol. Microbiol. 9:915-921.
51. Roy S, Douglas CW, Stafford GP. 2010. A novel sialic acid utilization and uptake system in the periodontal pathogen Tannerella forsythia. J. Bacteriol. 192:2285-2293.
52. Schauer R. 2009. Sialic acids as regulators of molecular and cellular interactions. Curr. Opin. Struct. Biol. 19:507-514.
53. Severi E, Hood DW, Thomas GH. 2007. Sialic acid utilization by bacterial pathogens. Microbiology 153:2817-2822.
54. Sheets SM, Robles-Price AG, McKenzie RM, Casiano CA, Fletcher HM. 2008. Gingipain-dependent interactions with the host are important for survival of Porphyromonas gingivalis. Front. Biosci. 13:3215-3238.
55. Sillanaukee P, Ponnio M, Jaaskelainen IP. 1999. Occurrence of sialic acids in healthy humans and different disorders. Eur. J. Clin. Invest. 29:413-425.
56. Simons RW, Houman F, Kleckner N. 1987. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53:85-96.
57. 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.
58. Socransky SS, Haffajee AD. 2005. Periodontal microbial ecology. Periodontol. 2000 38:135-187.
59. Soong G, et al. 2006. Bacterial neuraminidase facilitates mucosal infection by participating in biofilm production. J. Clin. Invest. 116:2297-2305.
60. Steenbergen SM, Vimr ER. 2003. Functional relationships of the sialyltransferases involved in expression of the polysialic acid capsules of Escherichia coli K1 and K92 and Neisseria meningitidis groups B or C. J. Biol. Chem. 278:15349-15359.
61. Steenbergen SM, Wrona TJ, Vimr ER. 1992. Functional analysis of the sialyltransferase complexes in Escherichia coli K1 and K92. J. Bacteriol. 174:1099-1108.
62. Sundqvist G, Carlsson J, Herrmann B, Tarnvik A. 1985. Degradation of human immunoglobulinsGandMand complement factors C3 and C5 by black-pigmented Bacteroides. J. Med. Microbiol. 19:85-94.
63. Sundqvist G, Johansson E. 1982. Bactericidal effect of pooled human serum on Bacteroides melaninogenicus, Bacteroides asaccharolyticus, and Actinobacillus actinomycetemcomitans. Scand. J. Dent. Res. 90:29-36.
64. Swords WE, et al. 2004. Sialylation of lipooligosaccharides promotes biofilm formation by nontypeable Haemophilus influenzae. Infect. Immun. 72:106-113.
65. Sze CW, Li C. 2011. Inactivation of bb0184, which encodes carbon storage regulator A, represses the infectivity of Borrelia burgdorferi. Infect. Immun. 79:1270-1279.
66. Thompson H, Homer KA, Rao S, Booth V, Hosie AH. 2009. An orthologue of Bacteroides fragilis NanH is the principal sialidase in Tannerella forsythia. J. Bacteriol. 191:3623-3628.
67. Traving C, Schauer R. 1998. Structure, function, and metabolism of sialic acids. Cell Mol. Life Sci. 54:1330-1349.
68. Typas A, Stella S, Johnson RC, Hengge R. 2007. The-35 sequence location and the Fis-sigma factor interface determine σs selectivity of the proP (P2) promoter in Escherichia coli. Mol. Microbiol. 63:780-796.
69. Uchiyama S, et al. 2009. The surface-anchored NanA protein promotes pneumococcal brain endothelial cell invasion. J. Exp. Med. 206:1845-1852.
70. Varki A. 2007. Glycan-based interactions involving vertebrate sialic-acidrecognizing proteins. Nature 446:1023-1029.
71. Varki NM, Varki A. 2007. Diversity in cell surface sialic acid presentations: implications for biology and disease. Lab. Invest. 87:851-857.
72. Vimr E, Lichtensteiger C. 2002. To sialylate, or not to sialylate: that is the question. Trends Microbiol. 10:254-257.
73. Vimr ER. 1994. Microbial sialidases: does bigger always mean better? Trends Microbiol. 2:271-277.
74. Vimr ER, Kalivoda KA, Deszo EL, Steenbergen SM. 2004. Diversity of microbial sialic acid metabolism. Microbiol. Mol. Biol. Rev. 68:132-153.
75. Vogel U, Claus H, Heinze G, Frosch M. 1999. Role of lipopolysaccharide sialylation in serum resistance of serogroup B and C meningococcal disease isolates. Infect. Immun. 67:954-957.
76. Vogel U, Frosch M. 1999. Mechanisms of neisserial serum resistance. Mol. Microbiol. 32:1133-1139.
77. Wang BY, Kuramitsu HK. 2005. Interactions between oral bacteria: inhibition of Streptococcus mutans bacteriocin production by Streptococcus gordonii. Appl. Environ. Microbiol. 71:354-362.
78. Whitfield C. 2006. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu. Rev. Biochem. 75:39-68.
79. Whitfield C, Roberts IS. 1999. Structure, assembly, and regulation of expression of capsules in Escherichia coli. Mol. Microbiol. 31:1307-1319.
80. Xie H, Cai S, Lamont RJ. 1997. Environmental regulation of fimbrial gene expression in Porphyromonas gingivalis. Infect. Immun. 65:2265-2271.
81. Xie H, Chung WO, Park Y, Lamont RJ. 2000. Regulation of the Porphyromonas gingivalis fimA (fimbrillin) gene. Infect. Immun. 68:6574-6579.
82. Xu G, et al. 2008. Crystal structure of the NanB sialidase from Streptococcus pneumoniae. J. Mol. Biol. 384:436-449.
83. Xu H, Raddi G, Liu J, Charon NW, 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.
84. Yesilkaya H, Soma-Haddrick S, Crennell SJ, Andrew PW. 2006. Identification of amino acids essential for catalytic activity of pneumococcal neuraminidase A. Res. Microbiol. 157:569-574.