Membrane morphology and leukotoxin secretion are associated with a novel membrane protein of Aggregatibacter actinomycetemcomitans

Journal of Bacteriology

Volumn 190, Issue 17, 2008, Pages 5972-5980

  Gallant, Claude V ^a   Sedic, Maja ^a   Chicoine, Erin A ^a   Ruiz, Teresa ^b   Mintz, Keith P ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LEUKOTOXIN; MORPHOGENESIS PROTEIN C; PROTEIN; UNCLASSIFIED DRUG;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; ARTICLE; BACTERIAL GROWTH; BIOGENESIS; CONTROLLED STUDY; GENE ACTIVATION; GENE CONVERSION; GENE IDENTIFICATION; GENE INSERTION; HAEMOPHILUS INFLUENZAE; HYDROPHOBICITY; NONHUMAN; OPERON; PASTEURELLA MULTOCIDA; PRIORITY JOURNAL;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CELL MEMBRANE; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EXOTOXINS; HYDROPHOBICITY; IMMUNOBLOTTING; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; OPERON; PROMOTER REGIONS (GENETICS); REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

ACTINOBACILLUS; ACTINOBACILLUS ACTINOMYCETEMCOMITANS; BACTERIA (MICROORGANISMS); HAEMOPHILUS INFLUENZAE; NEGIBACTERIA; PASTEURELLA MULTOCIDA;

EID: 50249144596     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00548-08     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. Bakaletz, L. O., B. D. Baker, J. A. Jurcisek, A. Harrison, L. A. Novotny, J. E. Bookwalter, R. Mungur, and R. S. Munson, Jr. 2005. Demonstration of type IV pilus expression and a twitching phenotype by Haemophilus influenzae. Infect. Immun. 73:1635-1643.
3. 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.
4. Bates, D. M., B. A. Lazazzera, and P. J. Kiley. 1995. Characterization of FNR* mutant proteins indicates two distinct mechanisms for altering oxygen regulation of the Escherichia coli transcription factor FNR. J. Bacteriol. 177:3972-3978.
5. 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.
6. Bhattacharjee, M. K., S. C. Kachlany, D. H. Fine, and D. H. Figurski. 2001. Nonspecific adherence and fibril biogenesis by Actinobacillus actinomycetemcomitans: TadA protein is an ATPase. J. Bacteriol. 183:5927-5936.
7. 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.
8. Darby, I., and M. Curtis. 2001. Microbiology of periodontal disease in children and young adults. Periodontol. 2000 26:33-53.
9. Darwin, A. J., and V. Stewart. 1995. Nitrate and nitrite regulation of the Fnr-dcpendent aeg-46.5 promoter of Escherichia coli K-12 is mediated by competition between homologous response regulators (NarL and NarP) for a common DNA-binding site. J. Mol. Biol. 251:15-29.
10. Dennis, J. J., and G. J. Zylstra. 1998. Improved antibiotic-resistance cassettes through restriction site elimination using Pfu DNA polymerase PCR. BioTechniques 25:772-774, 776.
11. Dinh, T., I. T. Paulsen, and M. H. Saier, Jr. 1994. A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of gram-negative bacteria. J. Bacteriol. 176:3825-3831.
12. Eichler, J., and F. Duong. 2004. Break on through to the other side - the Sec translocon. Trends Biochem. Sci. 29:221-223.
13. Eiglmeier, K., N. Honore, S. Iuchi, E. C. Lin, and S. T. Cole. 1989. Molecular genetic analysis of FNR-dependent promoters. Mol. Microbiol. 3:869-878.
14. 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.
15. 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.
16. Hoiczyk, E., A. Roggenkamp, M. Reichenbecher, A. Lupas, and J. Heesemann. 2000. Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J. 19:5989-5999.
17. Holt, S. C., A. C. Tanner, and S. S. Socransky. 1980. Morphology and ultrastructure of oral strains of Actinobacillus actinomycetemcomitans and Haemophilus aphrophilus. Infect. Immun. 30:588-600.
18. 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.
19. Kachlany, S. C., D. H. Fine, and D. H. Figurski. 2000. Secretion of RTX leukotoxin by Actinobacillus actinomycetemcomitam. Infect. Immun. 68:6094-6100.
20. 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.
21. Kolodrubetz, D., J. Spitznagel, Jr., B. Wang, L. H. Phillips, C. Jacobs, and E. Kraig. 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.
22. Kornberg, A. 1995. Inorganic polyphosphate: toward making a forgotten polymer unforgettable. J. Bacteriol. 177:491-496.
23. Kornberg, A., N. N. Rao, and D. Ault-Riche. 1999. Inorganic polyphosphate: a molecule of many functions. Annu. Rev. Biochem. 68:89-125.
24. Koronakis, V., C. Hughes, and E. Koronakis. 1991. Energetically distinct early and late stages of HlyB/HlyD-dependent secretion across both Escherichia coli membranes. EMBO J. 10:3263-3272.
25. Kraig, E., T. Dailey, and D. Kolodrubetz. 1990. Nucleotide sequence of the leukotoxin gene from Actinobacillus actinomycetemcomitans: homology to the alpha-hemolysin/leukotoxin gene family. Infect. Immun. 58:920-929.
26. Lally, E. T., E. E. Golub, I. R. Kieba, N. S. Taichman, S. Decker, P. Berthold, C. W. Gibson, D. R. Demuth, and J. Rosenbloom. 1991. Structure and function of the B and D genes of the Actinobacillus actinomycetemcomitans leukotoxin complex. Microb. Pathog. 11:111-121.
27. LeBlanc, D. J., L. N. Lee, and J. M. Inamine. 1991. Cloning and nucleotide base sequence analysis of a spectinomycin adenyltransferase AAD(9) determinant from Enterococcus faecalis. Antimicrob. Agents Chemother. 35:1804-1810.
28. Meyer, D. H., and P. M. Fives-Taylor. 1994. Characteristics of adherence of Actinobacillus actinomycetemcomitans to epithelial cells. Infect. Immun. 62: 928-935.
29. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
30. Mintz, K. P. 2004. Identification of an extracellular matrix protein adhesin, EmaA, which mediates the adhesion of Actinobacillus actinomycetemcomitans to collagen. Microbiology 150:2677-2688.
31. Mintz, K. P., and P. M. Fives-Taylor. 1994. Adhesion of Actinobacillus actinomycetemcomitans to a human oral cell line. Infect. Immun. 62:3672-3678.
32. Mintz, K. P., and P. M. Fives-Taylor. 2000. impA, a gene coding for an inner membrane protein, influences colonial morphology of Actinobacillus actinomycetemcomitans. Infect. Immun. 68:6580-6586.
33. Nikaido, H. 1994. Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science 264:382-388.
34. Paturel, L., J. P. Casalta, G. Habib, M. Nezri, and D. Raoult. 2004. Actinobacillus actinomycetemcomitans endocarditis. Clin. Microbiol. Infect. 10:98-118.
35. Pimenta, A., M. Blight, D. Clarke, and I. B. Holland. 1996. The gram-negative cell envelope "springs" to life: coiled-coil trans-envelope proteins. Mol. Microbiol. 19:643-645.
36. Rabin, R. S., and V. Stewart. 1993. Dual response regulators (NarL and NarP) interact with dual sensors (NarX and NarQ) to control nitrate- and nitrite-regulated gene expression in Escherichia coli K-12. J. Bacteriol. 175: 3259-3268.
37. Ravcheev, D. A., A. V. Gerasimova, A. A. Mironov, and M. S. Gelfand. 2007. Comparative genomic analysis of regulation of anaerobic respiration in ten genomes from three families of gamma-proteobacteria (Enterobacteriaceae, Pasteurellaceae, Vibrionaceae). BMC Genomics 8:54.
38. Rosan, B., J. Slots, R. J. Lamont, M. A. Listgarten, and G. M. Nelson. 1988. Actinobacillus actinomycetemcomitans fimbriae. Oral Microbiol. Immunol. 3:58-63.
39. Rosenberg, M., D. Gutnick, and E. Rosenberg. 1980. Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol. Lett. 9:29-33.
40. Ruiz, T., C. Lenox, M. Radermacher, and K. P. Mintz. 2006. Novel surface structures are associated with the adhesion of Actinobacillus actinomycetemcomitans to collagen. Infect. Immun. 74:6163-6170.
41. San Millan, R., J. Garaizar, and J. Bikandi. 2005. In silico simulation of fingerprinting techniques based on double endonuclease digestion of genomic DNA. In Silico Biol. 5:341-346.
42. 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.
43. 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.
44. Spiro, S., and J. R. Guest. 1990. FNR and its role in oxygen-regulated gene expression in Escherichia cob. FEMS Microbiol. Rev. 6:399-428.
45. Sreenivasan, P. K., and P. Fives-Taylor. 1994. Isolation and characterization of deletion derivatives of pDL282, an Actinobacillus actinomycetemcomitans/ Escherichia coli shuttle plasmid. Plasmid 31:207-214.
46. Stewart, V. 1993. Nitrate regulation of anaerobic respiratory gene expression in Escherichia coli. Mol. Microbiol. 9:425-434.
47. Stewart, V., and P. J. Bledsoe. 2005. Fnr-, NarP- and NarL-dependent regulation of transcription initiation from the Haemophilus influenzae Rd napF (periplasmic nitrate reductase) promoter in Escherichia coli K-12. J. Bacteriol. 187:6928-6935.
48. 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.
49. Tang, G., T. Kitten, C. L. Munro, G. C. Wellman, and K. P. Mintz. 2008. EmaA, a potential virulence determinant of Aggregatibacter (Actinobacillus) actinomycetemcomitans in infective endocarditis. Infect. Immun. 76:2316-2324.
50. Welch, R. A. 1991. Pore-forming cytolysins of gram-negative bacteria. Mol. Microbiol. 5:521-528.
51. Wimley, W. C. 2003. The versatile beta-barrel membrane protein. Curr. Opin. Struct. Biol. 13:404-411.
52. Yu, C., T. Ruiz, C. Lenox, and K. P. Mintz. 2008. Functional mapping of an oligomeric autotransporter adhesin of Aggregatibacter actinomycetemcomitans. J. Bacteriol. 190:3098-3109.
53. Zambon, J. J., L. A. Christersson, and R. J. Genco. 1986. Diagnosis and treatment of localized juvenile periodontitis. J. Am. Dent. Assoc. 113:295-299.