Transcriptional and translational analysis of biofilm determinants of Aggregatibacter actinomycetemcomitans in response to environmental perturbation

Infection and Immunity

Volumn 77, Issue 7, 2009, Pages 2896-2907

  Amarasinghe, Jayaleka J ^a   Scannapieco, Frank A ^a   Haase, Elaine M ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL PROTEIN EPS; BACTERIAL PROTEIN ORF8; BACTERIAL PROTEIN PGAC; BACTERIAL PROTEIN RMLB; FIMBRIA PROTEIN; FIMBRIA PROTEIN TADV; IRON; LIPOPOLYSACCHARIDE; UNCLASSIFIED DRUG;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; AEROBIC CELL CULTURE; ANAEROBIC CELL CULTURE; ARTICLE; BACTERIAL GROWTH; BIOFILM; CARBOHYDRATE SYNTHESIS; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FIMBRIA; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; IRON CHELATION; NONHUMAN; OXYGEN TENSION; PHENOTYPE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RNA TRANSLATION; WESTERN BLOTTING;

ANIMALS; BACTERIAL PROTEINS; BIOFILMS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; PASTEURELLACEAE; POLYSACCHARIDES, BACTERIAL; RNA, BACTERIAL; RNA, MESSENGER; STRESS, PHYSIOLOGICAL;

EID: 67650082693     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00126-09     Document Type: Article

References (77)

1. Amano, K., T. Nishihara, N. Shibuya, T. Noguchi, and T. Koga. 1989. Immunochemical and structural characterization of a serotype-specific polysaccharide antigen from Actinobacillus actinomycetemcomitans Y4 (serotype b). Infect. Immun. 57:2942-2946.
2. Asikainen, S., C. Chen, and J. Slots. 1995. Actinobacillus actinomycetemcomitans genotypes in relation to serotypes and periodontal status. Oral Microbiol. Immunol. 10:65-68.
3. Boman, H. G. 1995. Peptide antibiotics and their role in innate immunity. Annu. Rev. Immunol. 13:61-92.
4. Camprubí, S., S. Merino, J. F. Guillot, and J. M. Tomas. 1993. The role of the O-antigen lipopolysaccharide on the colonization in vivo of the germfree chicken gut by Klebsiella pneumoniae. Microb. Pathog. 14:433-440.
5. Colombo, A. V., C. M. da Silva, A. Haffajee, and A. P. Colombo. 2007. Identification of intracellular oral species within human crevicular epithelial cells from subjects with chronic periodontitis by fluorescence in situ hybridization. J. Periodontal Res. 42:236-243.
6. Costerton, J. W., Z. Lewandowski, D. E. Caldwell, D. R. Korber, and H. M. Lappin-Scott. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49:711-745.
7. Cramton, S. E., M. Ulrich, F. Gotz, and G. Doring. 2001. Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis. Infect. Immun. 69:4079-4085.
8. Das, M., A. D. Badley, F. R. Cockerill, J. M. Steckelberg, and W. R. Wilson. 1997. Infective endocarditis caused by HACEK microorganisms. Annu. Rev. Med. 48:25-33.
9. Deighton, M., and R. Borland. 1993. Regulation of slime production in Staphylococcus epidermidis by iron limitation. Infect. Immun. 61:4473-4479.
10. Donlan, R. M. 2002. Biofilms: microbial life on surfaces. Emerg. Infect. Dis. 8:881-890.
11. Donlan, R. M., and J. W. Costerton. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15:167-193.
12. Ernst, R. K., D. M. Dombroski, and J. M. Merrick. 1990. Anaerobiosis, type 1 fimbriae, and growth phase are factors that affect invasion of HEp-2 cells by Salmonella typhimurium. Infect. Immun. 58:2014-2016.
13. Fine, D. H., D. Furgang, J. Kaplan, J. Charlesworth, and D. H. Figurski. 1999. Tenacious adhesion of Actinobacillus actinomycetemcomitans strain CU1000 to salivary-coated hydroxyapatite. Arch. Oral Biol. 44:1063-1076.
14. Fine, D. H., D. Furgang, H. C. Schreiner, P. Goncharoff, J. Charlesworth, G. Ghazwan, P. Fitzgerald-Bocarsly, and D. H. Figurski. 1999. Phenotypic variation in Actinobacillus actinomycetemcomitans during laboratory growth: implications for virulence. Microbiology 145:1335- 1347.
15. Fine, D. H., P. Goncharoff, H. Schreiner, K. M. Chang, D. Furgang, and D. Figurski. 2001. Colonization and persistence of rough and smooth colony variants of Actinobacillus actinomycetemcomitans in the mouths of rats. Arch. Oral Biol. 46:1065-1078.
16. Fine, D. H., J. B. Kaplan, S. C. Kachlany, and H. C. Schreiner. 2006. How we got attached to Actinobacillus actinomycetemcomitans: a model for infectious diseases. Periodontol. 2000 42:114-157.
17. Fine, D. H., K. Markowitz, D. Furgang, K. Fairlie, J. Ferrandiz, C. Nasri, M. McKiernan, and J. Gunsolley. 2007. Aggregatibacter actinomycetemcomitans and its relationship to initiation of localized aggressive periodontitis: longitudinal cohort study of initially healthy adolescents. J. Clin. Microbiol. 45:3859-3869.
18. Fives-Taylor, P. M., D. H. Meyer, K. P. Mintz, and C. Brissette. 1999. Virulence factors of Actinobacillus actinomycetemcomitans. Periodontol. 2000 20:136-167.
19. Fujise, O., Y. Wang, W. Chen, and C. Chen. 2008. Adherence of Aggregatibacter actinomycetemcomitans via serotype-specific polysaccharide antigens in lipopolysaccharides. Oral Microbiol. Immunol. 23:226-233.
20. Gmür, R., H. McNabb, T. J. van Steenbergen, P. Baehni, A. Mombelli, A. J. van Winkelhoff, and B. Guggenheim. 1993. Seroclassification of hitherto nontypeable Actinobacillus actinomycetemcomitans strains: evidence for a new serotype e. Oral Microbiol. Immunol. 8:116-120.
21. Haase, E. M., T. Bonstein, R. J. Palmer, Jr., and F. A. Scannapieco. 2006. Environmental influences on Actinobacillus actinomycetemcomitans biofilm formation. Arch. Oral Biol. 51:299-314.
22. Haase, E. M., J. O. Stream, and F. A. Scannapieco. 2003. Transcriptional analysis of the 5′ terminus of the flp fimbrial gene cluster from Actinobacillus actinomycetemcomitans. Microbiology 149:205-215.
23. Haase, E. M., J. L. Zmuda, and F. A. Scannapieco. 1999. Identification and molecular analysis of rough-colony-specific outer membrane proteins of Actinobacillus actinomycetemcomitans. Infect. Immun. 67:2901-2908.
24. Hakalehto, E., J. Pesola, L. Heitto, A. Narvanen, and A. Heitto. 2007. Aerobic and anaerobic growth modes and expression of type 1 fimbriae in Salmonella. Pathophysiology 14:61-69.
25. Harvill, E. T., A. Preston, P. A. Cotter, A. G. Allen, D. J. Maskell, and J. F. Miller. 2000. Multiple roles for Bordetella lipopolysaccharide molecules during respiratory tract infection. Infect. Immun. 68:6720-6728.
26. Hayes, E. T., J. C. Wilks, P. Sanfilippo, E. Yohannes, D. P. Tate, B. D. Jones, M. D. Radmacher, S. S. BonDurant, and J. L. Slonczewski. 2006. Oxygen limitation modulates pH regulation of catabolism and hydrogenases, multidrug transporters, and envelope composition in Escherichia coli K-12. BMC Microbiol. 6:89.
27. Hitchcock, P. J., and T. M. Brown. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J. Bacteriol. 154:269-277.
28. Inoue, T., R. Shingaki, N. Sogawa, C. A. Sogawa, J. Asaumi, S. Kokeguchi, and K. Fukui. 2003. Biofilm formation by a fimbriae-deficient mutant of Actinobacillus actinomycetemcomitans. Microbiol. Immunol. 47:877-881.
29. Inoue, T., I. Tanimoto, H. Ohta, K. Kato, Y. Murayama, and K. Fukui. 1998. Molecular characterization of low-molecular-weight component protein, Flp, in Actinobacillus actinomycetemcomitans fimbriae. Microbiol. Immunol. 42:253-258.
30. Inouye, T., H. Ohta, S. Kokeguchi, K. Fukui, and K. Kato. 1990. Colonial variation and fimbriation of Actinobacillus actinomycetemcomitans. FEMS Microbiol. Lett. 57:13-17.
31. Itoh, Y., X. Wang, B. J. Hinnebusch, J. F. Preston III, and T. Romeo. 2005. Depolymerization of β-1,6-N-acetyl-D- glucosamine disrupts the integrity of diverse bacterial biofilms. J. Bacteriol. 187:382-387.
32. Izano, E. A., M. A. Amarante, W. B. Kher, and J. B. Kaplan. 2008. Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl. Environ. Microbiol. 74:470-476.
33. Izano, E. A., H. Wang, C. Ragunath, N. Ramasubbu, and J. B. Kaplan. 2007. Detachment and killing of Aggregatibacter actinomycetemcomitans biofilms by dispersin B and SDS. J. Dent. Res. 86:618-622.
34. Johnson, M., A. Cockayne, P. H. Williams, and J. A. Morrissey. 2005. Iron-responsive regulation of biofilm formation in Staphylococcus aureus involves fur-dependent and fur-independent mechanisms. J. Bacteriol. 187:8211-8215.
35. Kachlany, S. C., P. J. Planet, R. DeSalle, D. H. Fine, and D. H. Figurski. 2001. Genes for tight adherence of Actinobacillus actinomycetemcomitans: from plaque to plague to pond scum. Trends Microbiol. 9:429-437.
36. Kachlany, S. C., P. J. Planet, R. Desalle, D. H. Fine, D. H. Figurski, and J. B. Kaplan. 2001. flp-1, the first representative of a new pilin gene subfamily, is required for non-specific adherence of Actinobacillus actinomycetemcomitans. Mol. Microbiol. 40:542-554.
37. Kaplan, J. B., M. B. Perry, L. L. MacLean, D. Furgang, M. E. Wilson, and D. H. Fine. 2001. Structural and genetic analyses of O polysaccharide from Actinobacillus actinomycetemcomitans serotype f. Infect. Immun. 69:5375-5384.
38. Kaplan, J. B., K. Velliyagounder, C. Ragunath, H. Rohde, D. Mack, J. K. Knobloch, and N. Ramasubbu. 2004. Genes involved in the synthesis and degradation of matrix polysaccharide in Actinobacillus actinomycetemcomitans and Actinobacillus pleuropneumoniae biofilms. J. Bacteriol. 186:8213-8220.
39. Kozarov, E. V., B. R. Dorn, C. E. Shelburne, W. A. Dunn, Jr., and A. Progulske-Fox. 2005. Human atherosclerotic plaque contains viable invasive Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. Arterioscler. Thromb. Vasc. Biol. 25:e17-e18.
40. Lafontaine, E. R., L. D. Cope, C. Aebi, J. L. Latimer, G. H. McCracken, Jr., and E. J. Hansen. 2000. The UspA1 protein and a second type of UspA2 protein mediate adherence of Moraxella catarrhalis to human epithelial cells in vitro. J. Bacteriol. 182:1364-1373.
41. Lakio, L., S. Paju, G. Alfthan, T. Tiirola, S. Asikainen, and P. J. Pussinen. 2003. Actinobacillus actinomycetemcomitans serotype d-specific antigen contains the O antigen of lipopolysaccharide. Infect. Immun. 71:5005-5011.
42. Listgarten, M. A. 1972. Normal development, structure, physiology and repair of gingival epithelium. Oral Sci. Rev. 1:3-67.
43. Loo, C. Y., D. A. Corliss, and N. Ganeshkumar. 2000. Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes. J. Bacteriol. 182:1374-1382.
44. Merril, C. R., D. Goldman, and M. L. Van Keruen. 1982. Simplified silver protein detection and image enhancement methods in polyacrylamide gels. Electrophoresis 3:17-23.
45. Meyer, D. H., P. K. Sreenivasan, and P. M. Fives-Taylor. 1991. Evidence for invasion of a human oral cell line by Actinobacillus actinomycetemcomitans. Infect. Immun. 59:2719-2726.
46. Nakano, K., H. Inaba, R. Nomura, H. Nemoto, K. Tamura, E. Miyamoto, H. Yoshioka, K. Taniguchi, A. Amano, and T. Ooshima. 2007. Detection and serotype distribution of Actinobacillus actinomycetemcomitans in cardiovascular specimens from Japanese patients. Oral Microbiol. Immunol. 22:136-139.
47. Nakano, K., H. Nemoto, R. Nomura, H. Inaba, H. Yoshioka, K. Taniguchi, A. Amano, and T. Ooshima. 2009. Detection of oral bacteria in cardiovascular specimens. Oral Microbiol. Immunol. 24:64-68.
48. Nesper, J., C. M. Lauriano, K. E. Klose, D. Kapfhammer, A. Kraiss, and J. Reidl. 2001. Characterization of Vibrio cholerae O1 El tor galU and galE mutants: influence on lipopolysaccharide structure, colonization, and biofilm formation. Infect. Immun. 69:435-445.
49. Nika, J. R., J. L. Latimer, C. K. Ward, R. J. Blick, N. J. Wagner, L. D. Cope, G. G. Mahairas, R. S. Munson, Jr., and E. J. Hansen. 2002. Haemophilus ducreyi requires the flp gene cluster for microcolony formation in vitro. Infect. Immun. 70:2965-2975.
50. Paju, S., P. Carlson, H. Jousimies-Somer, and S. Asikainen. 2000. Heterogeneity of Actinobacillus actinomycetemcomitans strains in various human infections and relationships between serotype, genotype, and antimicrobial susceptibility. J. Clin. Microbiol. 38:79-84.
51. Piliero, P., P. E. Harnick, G. S. Rosenbaum, N. C. Klein, and B. A. Cunha. 1989. Infection due to Actinobacillus actinomycetemcomitans. Rev. Infect. Dis. 11:1033-1034.
52. Roosendaal, B., P. M. van Bergen en Henegouwen, and F. K. de Graaf. 1986. Subcellular localization of K99 fimbrial subunits and effect of temperature on subunit synthesis and assembly. J. Bacteriol. 165:1029-1032.
53. Rosan, B., J. Slots, R. J. Lamont, M. A. Listgarten, and G. M. Nelson. 1988. Actinobacillus actinomycetemcomitans fimbriae. Oral Microbiol. Immunol. 3:58-63.
54. Rudney, J. D., R. Chen, and G. J. Sedgewick. 2001. Intracellular Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in buccal epithelial cells collected from human subjects. Infect. Immun. 69:2700-2707.
55. Saarela, M., S. Asikainen, S. Alaluusua, L. Pyhala, C. H. Lai, and H. Jousimies-Somer. 1992. Frequency and stability of mono- or poly-infection by Actinobacillus actinomycetemcomitans serotypes a, b, c, d or e. Oral Microbiol. Immunol. 7:277-279.
56. Scannapieco, F. A., S. J. Millar, H. S. Reynolds, J. J. Zambon, and M. J. Levine. 1987. Effect of anaerobiosis on the surface ultrastructure and surface proteins of Actinobacillus actinomycetemcomitans (Haemophilus actinomycetemcomitans). Infect. Immun. 55:2320-2323.
57. Schreiner, H. C., K. Sinatra, J. B. Kaplan, D. Furgang, S. C. Kachlany, P. J. Planet, B. A. Perez, D. H. Figurski, and D. H. Fine. 2003. Tight-adherence genes of Actinobacillus actinomycetemcomitans are required for virulence in a rat model. Proc. Natl. Acad. Sci. USA 100:7295-7300.
58. Slots, J., H. S. Reynolds, and R. J. Genco. 1980. Actinobacillus actinomycetemcomitans in human periodontal disease: a cross-sectional microbiological investigation. Infect. Immun. 29:1013-1020.
59. Suzuki, N., Y. Nakano, Y. Yoshida, H. Nakao, Y. Yamashita, and T. Koga. 2000. Genetic analysis of the gene cluster for the synthesis of serotype a-specific polysaccharide antigen in Actinobacillus actinomycetemcomitans. Biochim. Biophys. Acta 1517:135-138.
60. Taylor, P. W. 1983. Bactericidal and bacteriolytic activity of serum against gram-negative bacteria. Microbiol. Rev. 47:46-83.
61. Tomich, M., D. H. Fine, and D. H. Figurski. 2006. The TadV protein of Actinobacillus actinomycetemcomitans is a novel aspartic acid prepilin peptidase required for maturation of the Flp1 pilin and TadE and TadF pseudopilins. J. Bacteriol. 188:6899-6914.
62. van Winkelhoff, A. J., and J. Slots. 1999. Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in nonoral infections. Periodontol. 2000 20:122-135.
63. Venketaraman, V., A. K. Lin, A. Le, S. C. Kachlany, N. D. Connell, and J. B. Kaplan. 2008. Both leukotoxin and poly-N-acetylglucosamine surface polysaccharide protect Aggregatibacter actinomycetemcomitans cells from macrophage killing. Microb. Pathog. 45:173-180.
64. Wai, S. N., Y. Mizunoe, A. Takade, S. I. Kawabata, and S. I. Yoshida. 1998. Vibrio cholerae O1 strain TSI-4 produces the exopolysaccharide materials that determine colony morphology, stress resistance, and biofilm formation. Appl. Environ. Microbiol. 64:3648-3655.
65. Wang, X., J. F. Preston III, and T. Romeo. 2004. The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J. Bacteriol. 186:2724-2734.
66. Wang, Y., and C. Chen. 2005. Mutation analysis of the flp operon in Actinobacillus actinomycetemcomitans. Gene 351:61-71.
67. Wang, Y., A. Liu, and C. Chen. 2005. Genetic basis for conversion of rough-to-smooth colony morphology in Actinobacillus actinomycetemcomitans. Infect. Immun. 73:3749-3753.
68. Westling, K., and M. Vondracek. 2008. Actinobacillus (Aggregatibacter) actinomycetemcomitans (HACEK) identified by PCR/16S rRNA sequence analysis from the heart valve in a patient with blood negative endocarditis Scand. J. Infect. Dis. 40:981-983.
69. Westphal, O., and K. Jann. 1965. Bacterial lipopolysaccharides: extraction with phenol-water and further applications of the procedure, vol. 5. Academic Press, New York, NY.
70. Winer, J., C. K. Jung, I. Shackel, and P. M. Williams. 1999. Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal. Biochem. 270:41-49.
71. Wrangstadh, M., P. L. Conway, and S. Kjelleberg. 1986. The production and release of an extracellular polysaccharide during starvation of a marine Pseudomonas sp. and the effect thereof on adhesion. Arch. Microbiol. 145:220-227.
72. Yamamoto, M., K. Saeki, and K. Utsumi. 1991. Isolation of human salivary polymorphonuclear leukocytes and their stimulation-coupled responses. Arch. Biochem. Biophys. 289:76-82.
73. Yang, Y., P. K. Sreenivasan, R. Subramanyam, and D. Cummins. 2006. Multiparameter assessments to determine the effects of sugars and antimicrobials on a polymicrobial oral biofilm. Appl. Environ. Microbiol. 72:6734-6742.
74. Yoshida, A., and H. K. Kuramitsu. 2002. Multiple Streptococcus mutans genes are involved in biofilm formation. Appl. Environ. Microbiol. 68:6283-6291.
75. Yoshida, Y., Y. Nakano, Y. Yamashita, and T. Koga. 1998. Identification of a genetic locus essential for serotype b-specific antigen synthesis in Actinobacillus actinomycetemcomitans. Infect. Immun. 66:107-114.
76. Zambon, J. J. 1985. Actinobacillus actinomycetemcomitans in human periodontal disease. J. Clin. Periodontol. 12:1-20.
77. Zambon, J. J., J. Slots, and R. J. Genco. 1983. Serology of oral Actinobacillus actinomycetemcomitans and serotype distribution in human periodontal disease. Infect. Immun. 41:19-27.