Leukotoxin production by Actinobacillus actinomycetemcomitans

Toxin Reviews

Volumn 25, Issue 1, 2006, Pages 1-18

  Inoue, Tetsuyoshi ^a   Fukui, Kazuhiro ^a   Ohta, Hiroyuki ^b  

^a OKAYAMA UNIVERSITY   (Japan)

^b IBARAKI UNIVERSITY   (Japan)

Author keywords

Actinobacillus actinomycetemcomitans; Expression; Leukotoxin; Secretion; Vesicle

Indexed keywords

BICARBONATE; CYTOTOXIN; LEUKOTOXIN; VIRULENCE FACTOR;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM CULTURE; CELL VACUOLE; ENVIRONMENTAL FACTOR; GRAM NEGATIVE BACTERIUM; HEREDITY; MEMBRANE VESICLE; NONHUMAN; OUTER MEMBRANE; PERIODONTITIS; PH; PROMOTER REGION; REVIEW; TOXIN STRUCTURE;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 32844462748     PISSN: 15569543     EISSN: 15569551     Source Type: Journal    
DOI: 10.1080/15569540500320839     Document Type: Review

References (83)

1. Baehni, P. C., Tsai, C. C., McArthur, W. P., Hammond, B. F., Taichman, N. S. (1979). Interaction of inflammatory cells and oral microorganisms. VIII. Detection of leukotoxic activity of a plaque-derived gram-negative microorganism. Infect. Immun. 24:233-243.
2. Baehni, P. C., Tsai, C. C., McArthur, W. P., Hammond, B. F., Shenker, B. J., Taichman, N. S. (1981). Leukotoxic activity in different strains of the bacterium Actinobacillus actinomycetemcomitans isolated from juvenile periodontitis in man. Arch. Oral Biol. 26:671-676.
3. Berthold, P., Forti, D., Kieba, I. R., Rosenbloom, J., Taichman, N. S., Lally, E. T. (1992). Electron immunocytochemical localization of Actinobacillus actinomycetemcomitans leukotoxin. Oral Microbiol. Immunol. 7:24-27.
4. Beveridge, T. J. (1999). Structures of gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 181:4725-4733.
5. Brogan, J. M., Lally, E. T., Poulsen, K., Kilian, M., Demuth, D. R. (1994). Regulation of Actinobacillus actinomycetemcomitans leukotoxin expression: analysis of the promoter regions of leukotoxic and minimally leukotoxic strains. Infect. Immun. 62:501-508.
6. Coote, J. G. (1992). Structural and functional relationships among the RTX toxin determinants of gram-netgative bacteria. FEMS Microbiol. Rev. 8:137-161.
7. Demuth, D. R., James, D., Kowashi, Y., Kato, S. (2003). Interaction of Actinobacillus actinomycetemcomitans outer membrane vesicles with HL60 cells does not require leukotoxin. Cell. Microbiol. 5:111-121.
8. DiRienzo J. M., Tsai, C. C., Shenker, B. J., Taichman, N. S., Lally, E. T. (1985). Moloclonal antibodies to leukotoxin of Actinobacillus actinomycetemcomitans. Infect. Immun. 47:31-36.
9. Dzink, J. L., Tanner, A. C., Haffajee, A. D., Socransky, S. S. (1985). Gram negative species associated with active destructive periodontal lesions. J. Clin. Periodontol. 12:648-659.
10. Felmlee, T., Pellett, S., Welch, R. A. (1985). Nucleotide sequence of an Escherichia coli chromosomal hemolysin. J. Bacteriol. 163:94-105.
11. Fong, K. P., Chung, W. O., Lamont, R. J., Demuth, D. R. (2001). Intra- and interspecies regulation of gene expression by Actinobacillus actinomycetemcomitans luxS. Infect. Immun. 69:7625-7634.
12. Frey, J., Beck, M., Stucki, U., Nicolet, J. (1993). Analysis of hemolysin operons in Actinobacillus pleuropneumoniae. Gene 123:51-58.
13. Frias, J., Olle, E., Alsina, M. (2001). Periodontal pathogens produce quorum sensing signal molecules. Infect. Immun. 69:3431-3434.
14. Fuqua, C., Parsek, M. R., Greenberg, E. P. (2001). Cell-to-cell communication: acyl-homoserine lactone quorum sensing. Ann. Rev. Genet. 35:439-468.
15. Gentschev, I., Dietrich, G., Goebel, W. (2002). The E. coli α-hemolysin secretion system and its use in vaccine development. Trends Microbiol. 10:39-45.
16. Glaser, P., Sakamoto, H., Bellalou, J., Ullmann, A., Danchin, A. (1988). Secretion of cytolysin, the calmodulin-sensitive adenylate cyclase-haemolysin bifunctional protein of Bordetella pertussis. EMBO J. 7:3997-4004.
17. Grenier, D., Mayrand, D. (1987). Functional characterization of extracellular vesicles produced by Bacteroides gingivalis. Infect. Immun. 55:111-117.
18. Guest, J. R. (1992). Oxygen-regulated gene expression in Escherichia coli. J. Gen. Microbiol. 138:2253-2263.
19. Guthmiller, J. M., Kolodrubetz, D., Cagle, M. P., Kraig, E. (1990a). Sequence of the IktB gene from Actinobacillus actinomycetemcomitans. Nucleic Acids Res. 18:5291.
20. Guthmiller, J. M., Kraig, E., Cagle, M. P., Kolodrubetz, D. (1990b). Sequence of the IktD gene from Actinobacillus actinomycetemcomitans. Nucleic Acids Res. 18:5292.
21. Guthmiller, J. M., Kolodrubetz, D., Kraig, E. (1995). Mutational analysis of the putative leukotoxin transport genes in Actinobacillus actinomycetemcomitans. Microb. Pathog. 18:307-321.
22. Hasse, E. M., Zmuda, J. L., Scannapieco, F. A. (1999). Identification and molecular analysis of rough-colony-specific outer membrane proteins of Actinobacillus actinomycetemcomitans. Infect. Immun. 67:2901-2908.
23. He, T., Nishihara, T., Demuth, D. R., Ishikawa, I. (1999). A novel insertion sequence increases the expression of leukotoxicity in Actinobacillus actinomycetemcomitans. clinical isolates. J. Periodontol. 70:1261-1268.
24. Henderson, B., Nair, S. P., Ward, J. M., Wilson, M. (2003). Molecular pathogenesis of the oral opportunistic pathogen Actinobacillus actinomycetemcomitans. Ann. Rev. Microbiol. 57:29-55.
25. Henderson, I. R., Navarro-Garcia, F., Desvaux, M., Fernandez, R. C., Ala'Aldeen, D. (2004). Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 68:692-744.
26. Horstman, A. L., Kuehn, M. J. (2000). Enterotoxigenic Escherichia coli secretes active heat-labile enterotoxin via outer membrane vesicles. J. Biol. Chem. 275:12489-12469.
27. Hritz, M., Fisher, E., Demuth, D. R. (1996). Differential regulation of the leukotoxin operon in highly leukotoxic and minimally leukotoxic strains of Actinobacillus actinomycetemcomitans. Infect. Immun. 64:2724-2729.
28. Inoue, T., Tanimoto, I., Ohta, H., Murayama, Y., Fukui, K. (1998). Molecular characterization of low-molecular-weight component protein, Flp, in Actinobacillus actinomycetemcomitans fimbriae. Microbiol. Immunol. 253-258.
29. Inoue, T., Tanimoto, I., Tada, T., Ohashi, T., Fukui, K., Ohta, H. (2001). Fermentable-sugar-level-dependent regulation of leukotoxin synthesis in a variably toxic strain of Actinobacillus actinomycetemcomitans. Microbiology 147:2749-2756.
30. Inoue, T., Shingaki, R., Sogawa, N., Sogawa, C. A., Asaumi, J., Kokoguchi, S., Fukui, K. (2003). Biofilm formation by a fimbriae-deficient mutant of Actinobacillus actinomycetemcomitans. Microbiol. Immunol. 41:877-881.
31. Iuchi, S., Weiner, L. (1996). Cellular and molecular physiology of Escherichia coli in the adaptation to aerobic environments. J. Biochem. 120:1055-1063.
32. Kachlany, S. C., Fine, D. H., Figurski, D. H. (2000a). Secretion of RTX leukotoxin by Actinobacillus actinomycetemcomitans. Infect. Immun. 68:6094-6100.
33. Kachlany, S. C., Planet, P. J., Bhattacharjee, M. K., Kollia, F., Desalle, R., Fine, D. H., Figurski, D. H. (2000b). Nonspecific adherence by Actinobacillus actinomycetemcomitans requires genes widespread in bacteria and archaea. J. Bacteriol. 182:6169-6176.
34. Kadurugamuwa, J. L., Beveridge, T. J. (1995). Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J. Bacteriol. 177:3998-4008.
35. Kaplan, J. B., Meyenhofer, M. F., Fine, D. H. (2003). Biofilm growth and detachment of Actinobacillus actinomycetemcomitans. J. Bacteriol. 185:1399-1404.
36. Kato, S., Kowashi, Y., Demuth, D. R. (2002). Outer membrane-like vesicles secreted by Actinobacillus actinomycetemcomitans are enriched in leukotoxin. Microb. Pathog. 32:1-13.
37. Keenan, J., Day, T., Neal, S., Cook, B., Perez-Perez, G., Allardyce, R., Bagshaw, P. (2000). A role for the bacterial outer membrane in the pathogenesis of Helicobacter pylori, infection. FEMS Microbiol. Lett. 182:259-264.
38. Kolenbrander, P. E., Andersen, R. N., Blehert, D. S., Egland, P. G., Foster, J. S., Palmer, R. J. Jr., (2002). Communication among oral bacteria. Microbiol. Mol. Biol. Rev. 66:486-505.
39. Kolling, G. L., Matthews, K. R. (1999). Export of virulence genes and shiga toxin by membrane vesicles of Escherichia coli O157:H7. Appl. Environ. Microbiol. 65:1843-1848.
40. Kolodrubetz, D., Spitznagel, Wang, B., Phillips, L. H., Jacobs, C., Kraig, E. (1996). cis Elements and trans factors are both important in strain-specific regulation of the leukotoxin gene in Actinobacillus actinomycetemcomitans. Infect. Immun. 64:3451-3460.
41. Kolodrubetz, D., Phillips, L., Jacobs, C., Burgum, A., Kraig, E. (2003). Anaerobic regulation of Actinobacillus actinomycetemcomitans leukotoxin transcription is ArcA/FnrA-independent and requires a novel promoter element. Res. Microbiol. 154:645-653.
42. Koronakis, V., Eswaran, J., Hughes, C. (2004). Structure and function of TolC: the bacterial exit duct for proteins and drugs. Ann. Rev. Biochem. 73:467-489.
43. Korostoff, J., Wang, J. F., Kieba, I., Miller, M., Shenker, B. J., Lally, E. T. (1998). Actinobacillus actinomycetemcomitans leukotoxin induces apoptosis in HL-60 cells. Infect. Immun. 66:4474-4483.
44. Kraig, E., Dailey, T., Kolodrubetz, D. (1990). Nucleotide sequence of the leukotoxin gene from Actinobacillus actinomycetemcomitans: homology to the alpha-hemolysin/leukotoxin gene family. Infect. Immun. 58:920-929.
45. Lai, C.-H., Listgarten, M. A., Hammond, B. F. (1981). Comparative ultrastructure of leukotoxic and nonleukotoxic strains of Actinobacillus actinomycetemcomitans. J. Periodontal Res. 16:379-389.
46. Lally, E. T., Golub, E. E., Kieba, I. R., Taichman, N. S., Rosenbloom, J., Rosenbloom, J. C., Gibson, C. W., Demuth, D. R. (1989a). Analysis of the Actinobacillus actinomycetemcomitans leukotoxin gene. Delineation of unique features and comparison to homologous toxins. J. Biol. Chem. 264:15451-15456.
47. Lally, E. T., Kieba, I. R., Demuth, D. R., Rosenbloom, J., Golub, E. E., Taichman, N. S., Gibson, C. W. (1989b). Identification and expression of the Actinobacillus actinomycetemcomitans leukotoxin gene. Biochem. Biophys. Res. Commun. 159:256-262.
48. Lally, E. T., Golub, E. E., Kieba, I. R., Taichman, N. S., Decker, S., Berthold, P., Gibson, C. W., Demuth, D. R., Rosenbloom, J. (1991). Structure and function of the B and D genes of the Actinobacillus actinomycetemcomitans leukotoxin complex. Microb. Pathog. 11:111-121.
49. Lally, E. T., Kieba, I. R. (1994). Molecular biology of Actinobacillus actinomycetemcomitans leukotoxin. In: Genco, R., Hamada, S., Lehner, T., McGhee, J., Mergenhagen, S., eds., Molecular Pathogenesis of Periodontal Disease, ASM Press: Washington, DC.
50. Lally, E. T., Hill, R. B., Kieba, I. R., Korostoff, J. (1999). The interaction between RTX toxins and target cells. Trends Microbiol. 7:356-361.
51. Lee, V. T., Schneewind, O. (2001). Protein secretion and the pathogenesis of bacterial infections. Genes Dev. 15:1725-1752.
52. Li, Z., Clarke, A. J., Beveridge, T. J. (1998). Gram-negative bacteria produce membrane vesicles which are capable of killing other bacteria. J. Bacteriol. 180:5478-5483.
53. Loesche, W.J., Gusberti, F., Mettraux, G., Higgins, T., Syed, S. (1983). Relationship between oxygen tension and subgingival bacterial flora in untreated human periodontal pockets. Infect. Immun. 42:659-667.
54. Mayrand, D., Grenier, D. (1989). Biological activities of outer membrane vesicles. Can. J. Microbiol. 35:607-613.
55. Miller, M. B., Bassler, B. L. (2001). Quorum-sensing in bacteria. Ann. Rev. Microbiol. 55:165-199.
56. Mitchell, C., Gao, L., Demuth, D. R. (2003). Positive and negative cis-acting regulatory sequences control expression of leukotoxin in Actinobacillus actinomycetemcomitans 652. Infect. Immun. 71:5640-5649.
57. Mizoguchi, K., Ohta, H., Miyagi, A., Kurihara, H., Takashiba, S., kato, K., Murayama, Y., Fukui, K. (1997). The regulatory effect of fermentable sugar levels on the production of leukotoxin by Actinobacillus actinomycetemcomitans. FEMS Microbiol. Lett. 146:161-166.
58. Negrete-Abascal, E., Garcia, R. M., Reyes, M. E., Godinez, D., Garza, M. (2000). Membrane vesicles released by Actinobacillus pleuropneumoniae contain proteases and Apx toxins. FEMS Microbiol. Lett. 191:109-113.
59. Ohta, H., Fukui, K., Kato, K. (1989). Effect of bicarbonate on the growth of Actinobacillus actinomycetemcomitans in anaerobic fructose-limited chemostat culture. J. Gen. Microbiol. 135:3485-3495.
60. Ohta, H., Kato, K., Kokeguchi, S., Hara, K., Fukui, K., Murayama, Y. (1991). Nuclease-sensitive binding of an Actinobacillus actinomycetemcomitans leukotoxin to the bacterial cell surface. Infect. Immun. 59:4599-4605.
61. Ohta, H., Hara, K., Fukui, K., Kurihara, H., Murayama, Y., Kato, K. (1993). Association of Actinobacillus actinomycetemcomitans leukotoxin with nucleic acids on the bacterial cell surface. Infect. Immun. 61:4878-4884.
62. Ohta, H., Miyagi, A., Kato, K., Fukui, K. (1996a). The relationships between leukotoxin production, growth rate and the bicarbonate concentration in a toxin-production-variable strain of Actinobacillus actinomycetemcomitans. Microbiology 142:963-970.
63. Ohta, H., Moriki, D., Miyagi, A., Watanabe, T., Kato, K., Fukui, K. (1996b). Microaerophilic property of Actinobacillus actinomycetemcomitans in fructose-limited chemostat cultures. FEMS Microbiol. Lett. 138:191-196.
64. Paturel, L., Casalta, J. P., Habib, G., Nezri, M., Raoult, D. (2004). Actinobacillus actinomycetemcomitans endocarditis. Clin. Microbiol. Infect. 10:98-118.
65. Poulsen, K., Theilade, E., Lally, E. T., Demuth, D. R., Kilian, M. (1994). Population structure of Actinobacillus actinomycetemcomitans: a framework for studies of disease-associated properties. Microbiology 140:2049-2060.
66. Shenker, B. J., McKay, T., Datar, S., Miller, M., Chowden, R., Demuth, D. R. (1999). Actinobacillus actinomycetemcomitans immunosuppressive protein is a member of the family of cytolethal distending toxins capable of causing G2 arrest in human T cells. J. Immunol. 162:4773-4780.
67. Slots, J., Reynolds, H. S., Genco, R. J. (1980). Actinobacillus actinomycetemcomitans in human periodontal disease: a cross-sectional microbiological investigation. Infect. Immun. 29:1013-1020.
68. Spitznagel, J., Kraig, E., Kolodrubetz, D. (1991). Regulation of leukotoxin in leukotoxic and nonleukotoxic strains of Actinobacillus actinomycetemcomitans. Infect. Immun. 59:1349-1401.
69. Strathdee, C. A., Lo, R. Y. (1989). Cloning, nucleotide sequence, and characterization of genes encoding the secretion function of the Pasteurella haemolytica leukotoxin determinant. J. Bacteriol. 171:916-928.
70. Sugai, M., Kawamoto, T., Peres, S. Y., Ueno, Y., Komatsuzawa, H., Fujiwara, T., Kurihara, H., Suginaka, H., Oswald, E. (1998). The cell cycle-specific growth-inhibitory factor produced by Actinobacillus actinomycetemcomitans is a cytolethal distending toxin. Infect. Immun. 66:5008-5019.
71. Surette, M. G., Bassler, B. L. (1998). Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 95:7046-7050.
72. Tervahartiala, V., Uitto, V.-J., Kari, K., Laasko, T. (1989). Outer membrane vesicles and leukotoxic activity of Actinobacillus actinomycetemcomitans from subjects with different periodontal status. Scand. J. Dent. Res. 97:33-42.
73. Thanabalu, T., Koronakis, E., Hughes, C., Koronakis, V. (1998). Substrate-induced assembly of a contiguous channel for protein export from E. coli: reversible bridging of an inner-membrane translocase to an outer membrane exit pore. EMBO J. 22:6487-6496.
74. Tsai, C. C., McArthur, W. P., Baehni, P. C., Hammond, B. F., Taichman, N. S. (1979). Extraction and partial characterization of a leukotoxin from a plaque-derived Gram-negative microorganism. Infect. Immun. 25:427-439.
75. Tsai, C. C., Shenker, B. J., DiRienzo, J. M., Malamud, D., Taichman, N. S. (1984). Extraction and isolation of a leukotoxin from Actinobacillus actinomycetemcomitans with polymyxin B. Infect. Immun. 43:700-705.
76. Uhlich, G. A., McNamara, P. J., Iandoro, J. J., Mosier, D. A. (2000). FnrP interactions with Pasteurella haemolytica leukotoxin promoter. FEMS Microbiol. Lett. 186:73-77.
77. Ushiba, Y., Ohta, H. (2004). Ecophysiology of the oral opportunistic pathogen Actinobacillus actinomycetemcomitans with special emphasis on leukotoxin production. Microbes Environ. 19:190-198.
78. Wai, S. N., Lindmark, B., Soderblom, T., Takade, A., Westermark, M., Oscarsson, J., Jass J., Richter-Dahlfors, A., Mizunoe, Y., Uhlin, B. E. (2003). Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell 115:25-35.
79. Wandersman, C., Delepelaire, P. (1990). TolC, an Escherichia coli outer membrane protein required for hemolysin secretion. Proc. Natl. Acad. Sci. USA 87:4776-4780.
80. Welch, R. A. (1991). Pore-forming cytolysins of gram-negative bacteria. Mol. Microbiol. 5:521-528.
81. Whitehead, N. A., Barnard, A. M. L., Slater, H., Simpson, N. J. L., Salmond, G. P. C. (2001). Quorum-sensing in gram-negative bacteria. FEMS Microbiol. Rev. 25:365-404.
82. Xavier, K. B., Bassler, B. L. (2003). LuxS quorum sensing: more than just a numbers game. Curr. Opin. Microbiol. 6:191-197.
83. Zhou, L., Srisatjaluk, R., Justus, D. E., Doyle, R. J. (1998). On the origin of membrane vesicles in gram negative bacteria. FEMS Microbiol. Lett. 163:223-228.