Screen for leukotoxin mutants in Aggregatibacter actinomycetemcomitans: Genes of the phosphotransferase system are required for leukotoxin biosynthesis

Infection and Immunity

Volumn 76, Issue 8, 2008, Pages 3561-3568

  Isaza, Maria P ^a   Duncan, Matthew S ^a   Kaplan, Jeffrey B ^a   Kachlany, Scott C ^a,b  

^a RUTGERS SCHOOL OF DENTAL MEDICINE   (United States)

^b UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LEUKOTOXIN; PHOSPHOTRANSFERASE; CYCLIC AMP; EXOTOXIN; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM MUTANT; BIOSYNTHESIS; GENE MAPPING; GENE MUTATION; NONHUMAN; PHENOTYPE; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; WILD TYPE; AMINO ACID SEQUENCE; CHEMISTRY; CULTURE MEDIUM; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; HEMOLYSIS; HUMAN; MOLECULAR GENETICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; TRANSPOSON;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; AMINO ACID SEQUENCE; CULTURE MEDIA; CYCLIC AMP; DNA TRANSPOSABLE ELEMENTS; EXOTOXINS; GENE EXPRESSION PROFILING; GENETIC COMPLEMENTATION TEST; HEMOLYSIS; HUMANS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE SYSTEM; POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT;

EID: 48849093368     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01687-07     Document Type: Article

References (53)

1. Baehni, P. C., C. C. Tsai, W. P. McArthur, B. F. Hammond, B. J. Shenker, and N. S. Taichman. 1981. Leukotoxic activity in different strains of the bacterium Actinobacillus actinomycetemcomitans isolated from juvenile periodontitis in man. Arch. Oral Biol. 26:671-676.
2. Balashova, N. V., J. A. Crosby, L. Al Ghofaily, and S. C. Kachlany. 2006. Leukotoxin confers beta-hemolytic activity to Actinobacillus actinomycetemcomitans. Infect. Immun. 74:2015-2021.
3. Balashova, N. V., R. Diaz, S. V. Balashov, J. A. Crosby, and S. C. Kachlany. 2006. Regulation of Aggregatibacter (Actinobacillus) actinomycetemcomitans leukotoxin secretion by iron. J. Bacteriol. 188:8658-8661.
4. Berbari, E. F., F. R. Cockerill III, and J. M. Steckelberg. 1997. Infective endocarditis due to unusual or fastidious microorganisms. Mayo Clin. Proc. 72:532-542.
5. Crosby, J. A., and S. C. Kachlany. 2007. TdeA, a TolC-like protein required for toxin and drug export in Aggregatibacter (Actinobacillus) actinomycetemcomitans. Gene 388:83-92.
6. 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.
7. Delepelaire, P. 2004. Type I secretion in gram-negative bacteria. Biochim. Biophys. Acta 1694:149-161.
8. Deutscher, J., C. Francke, and P. W. Postma. 2006. How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol. Mol. Biol. Rev. 70:939-1031.
9. Diaz, R., L. A. Ghofaily, J. Patel, N. V. Balashova, A. C. Freitas, I. Labib, and S. C. Kachlany. 2006. Characterization of leukotoxin from a clinical strain of Actinobacillus actinomycetemcomitans. Microb. Pathog. 40:48-55.
10. Feucht, B. U., and M. H. Saier, Jr. 1980. Fine control of adenylate cyclase by the phosphoenolpyruvate:sugar phosphotransferase systems in Escherichia coli and Salmonella typhimurium. J. Bacteriol. 141:603-610.
11. 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.
12. 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.
13. 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.
14. Flores, N., R. de Anda, S. Flores, A. Escalante, G. Hernandez, A. Martinez, O. T. Ramirez, G. Gosset, and F. Bolivar. 2004. Role of pyruvate oxidase in Escherichia coli strains lacking the phosphoenolpyruvate: carbohydrate phosphotransferase system. J. Mol. Microbiol. Biotechnol. 8:209-221.
15. Fong, K. P., W. O. Chung, R. J. Lamont, and D. R. Demuth. 2001. Intra- and interspecies regulation of gene expression by Actinobacillus actinomycetemcomitans LuxS. Infect. Immun. 69:7625-7634.
16. Frey, J., and P. Kuhnert. 2002. RTX toxins in Pasteurellaceae. Int. J. Med. Microbiol. 292:149-158.
17. Gentschev, I., G. Dietrich, and W. Goebel. 2002. The E. coli alpha-hemolysin secretion system and its use in vaccine development. Trends Microbiol. 10:39-45.
18. Guthmiller, J. M., D. Kolodrubetz, M. P. Cagle, and E. Kraig. 1990. Sequence of the lktB gene from Actinobacillus actinomycetemcomitans. Nucleic Acids Res. 18:5291.
19. Guthmiller, J. M., D. Kolodrubetz, and E. Kraig. 1995. Mutational analysis of the putative leukotoxin transport genes in Actinobacillus actinomycetemcomitans. Microb. Pathog 18:307-321.
20. Guthmiller, J. M., E. Kraig, M. P. Cagle, and D. Kolodrubetz. 1990. Sequence of the lktD gene from Actinobacillus actinomycetemcomitans. Nucleic Acids Res. 18:5292.
21. Haraszthy, V. I., G. Hariharan, E. M. Tinoco, J. R. Cortelli, E. T. Lally, E. Davis, and J. J. Zambon. 2000. Evidence for the role of highly leukotoxic Actinobacillus actinomycetemcomitans in the pathogenesis of localized juvenile and other forms of early-onset periodontitis. J. Periodontol. 71:912-922.
22. Haubek, D., J. M. Dirienzo, E. M. Tinoco, J. Westergaard, N. J. Lopez, C. P. Chung, K. Poulsen, and M. Kilian. 1997. Racial tropism of a highly toxic clone of Actinobacillus actinomycetemcomitans associated with juvenile periodontitis. J. Clin. Microbiol. 35:3037-3042.
23. Haubek, D., O. K. Ennibi, K. Poulsen, S. Poulsen, N. Benzarti, and M. Kilian. 2001. Early-onset periodontitis in Morocco is associated with the highly leukotoxic clone of Actinobacillus actinomycetemcomitans. J. Dent. Res. 80:1580-1583.
24. Horstmann, N., G. Seidel, L. M. Aung-Hilbrich, and W. Hillen. 2007. Residues His-15 and Arg-17 of HPr participate differently in catabolite signal processing via CcpA. J. Biol. Chem. 282:1175-1182.
25. Inoue, T., I. Tanimoto, T. Tada, T. Ohashi, K. Fukui, and H. Ohta. 2001. Fermentable-sugar-level-dependent regulation of leukotoxin synthesis in a variably toxic strain of Actinobacillus actinomycetemcomitans. Microbiology 147:2749-2756.
26. Kachlany, S. C., D. H. Fine, and D. H. Figurski. 2000. Secretion of RTX leukotoxin by Actinobacillus actinomycetemcomitans. Infect. Immun. 68:6094-6100.
27. Kachlany, S. C., P. J. Planet, M. K. Bhattacharjee, E. Kollia, R. DeSalle, D. H. Fine, and D. H. Figurski. 2000. Nonspecific adherence by Actinobacillus actinomycetemcomitans requires genes widespread in bacteria and archaea. J. Bacteriol. 182:6169-6176.
28. 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.
29. 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.
30. Kolodrubetz, D., T. Dailey, J. Ebersole, and E. Kraig. 1989. Cloning and expression of the leukotoxin gene from Actinobacillus actinomycetemcomitans. Infect. Immun. 57:1465-1469.
31. Koronakis, V. 2003. TolC - the bacterial exit duct for proteins and drugs. FEBS Lett. 555:66-71.
32. Krin, E., O. Sismeiro, A. Danchin, and P. N. Bertin. 2002. The regulation of Enzyme IIA(Glc) expression controls adenylate cyclase activity in Escherichia coli. Microbiology 148:1553-1559.
33. Lally, E. T., E. E. Golub, I. R. Kieba, N. S. Taichman, J. Rosenbloom, J. C. Rosenbloom, C. W. Gibson, and D. R. Demuth. 1989. Analysis of the Actinobacillus actinomycetemcomitans leukotoxin gene. Delineation of unique features and comparison to homologous toxins. J. Biol. Chem. 264:15451-15456.
34. Lally, E. T., I. R. Kieba, N. S. Taichman, J. Rosenbloom, C. W. Gibson, D. R. Demuth, G. Harrison, and E. E. Golub. 1991. Actinobacillus actinomycetemcomitans leukotoxin is a calcium-binding protein. J. Periodontal Res. 26:268-271.
35. Levy, S., G. Q. Zeng, and A. Danchin. 1990. Cyclic AMP synthesis in Escherichia coli strains bearing known deletions in the pts phosphotransferase operon. Gene 86:27-33.
36. Muller, W., N. Horstmann, W. Hillen, and H. Sticht. 2006. The transcription regulator RbsR represents a novel interaction partner of the phosphoprotein HPr-Ser46-P in Bacillus subtilis. FEBS J. 273:1251-1261.
37. Narayanan, S. K., T. G. Nagaraja, M. M. Chengappa, and G. C. Stewart. 2002. Leukotoxins of gram-negative bacteria. Vet. Microbiol. 84:337-356.
38. Nelson, S. O., B. J. Scholte, and P. W. Postma. 1982. Phosphoenolpyruvate: sugar phosphotransferase system-mediated regulation of carbohydrate metabolism in Salmonella typhimurium. J. Bacteriol. 150:604-615.
39. Nielsen, K. K., and M. Boye. 2005. Real-time quantitative reverse transcription-PCR analysis of expression stability of Actinobacillus pleuropneumoniae housekeeping genes during in vitro growth under iron-depleted conditions. Appl. Environ. Microbiol. 71:2949-2954.
40. Nothaft, H., S. Parche, A. Kamionka, and F. Titgemeyer. 2003. In vivo analysis of HPr reveals a fructose-specific phosphotransferase system that confers high-affinity uptake in Streptomyces coelicolor. J. Bacteriol. 185:929-937.
41. Oropeza-Wekerle, R. L., E. Muller, P. Kern, R. Meyermann, and W. Goebel. 1989. Synthesis, inactivation, and localization of extracellular and intracellular Escherichia coli hemolysins. J. Bacteriol. 171:2783-2788.
42. Paturel, L., J. P. Casalta, G. Habib, M. Nezri, and D. Raoult. 2004. Acti nobacillus actinomycetemcomitans endocarditis. Clin. Microbiol. Infect. 10:98-118.
43. Planet, P. J., S. C. Kachlany, D. H. Fine, R. DeSalle, and D. H. Figurski. 2003. The widespread colonization island of Actinobacillus actinomycetemcomitans. Nat. Genet. 34:193-198.
44. Reichenbach, B., D. A. Breustedt, J. Stulke, B. Rak, and B. Gorke. 2007. Genetic dissection of specificity determinants in the interaction of HPr with enzymes II of the bacterial phosphoenolpyruvate:sugar phosphotransferase system in Escherichia coli. J. Bacteriol. 189:4603-4613.
45. Slots, J., and M. Ting. 1999. Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in human periodontal disease: occurrence and treatment. Periodontol. 2000 20:82-121.
46. Taichman, N. S., R. T. Dean, and C. J. Sanderson. 1980. Biochemical and morphological characterization of the killing of human monocytes by a leukotoxin derived from Actinobacillus actinomycetemcomitans. Infect. Immun. 28:258-268.
47. Taichman, N. S., D. L. Simpson, S. Sakurada, M. Cranfield, J. DiRienzo, and J. Slots. 1987. Comparative studies on the biology of Actinobacillus actinomycetemcomitans leukotoxin in primates. Oral Microbiol. Immunol. 2:97-104.
48. Taichman, N. S., and J. M. Wilton. 1981. Leukotoxicity of an extract from Actinobacillus actinomycetemcomitans for human gingival polymorphonuclear leukocytes. Inflammation 5:1-12.
49. Thomson, V. J., M. K. Bhattacharjee, D. H. Fine, K. M. Derbyshire, and D. H. Figurski. 1999. Direct selection of IS903 transposon insertions by use of a broad-host-range vector: isolation of catalase-deficient mutants of Actinobacillus actinomycetemcomitans. I. Bacteriol. 181:7298-7307.
50. Tsai, C. C., B. J. Shenker, J. M. DiRienzo, D. Malamud, and N. S. Taichman. 1984. Extraction and isolation of a leukotoxin from Actinobacillus actinomycetemcomitans with polymyxin B. Infect. Immun. 43:700-705.
51. Welch, R. A. 2001. RTX toxin structure and function: a story of numerous anomalies and few analogies in toxin biology. Curr. Top. Microbiol. Immunol. 257:85-111.
52. Zambon, J. J. 1985. Actinobacillus actinomycetemcomitans in human periodontal disease. J. Clin. Periodontol. 12:1-20.
53. Zambon, J. J. 1996. Periodontal diseases: microbial factors. Ann. Periodontol. 1:879-925.