Functional mapping of an oligomeric autotransporter adhesin of Aggregatibacter actinomycetemcomitans

Journal of Bacteriology

Volumn 190, Issue 9, 2008, Pages 3098-3109

  Yu, Chunxiao ^a   Ruiz, Teresa ^b   Lenox, Christopher ^a   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

ADHESIN; ADHESIN A; AMINO ACID; CARRIER PROTEIN; COLLAGEN; OLIGOMER; SCLEROPROTEIN; UNCLASSIFIED DRUG;

ACTINOBACILLUS; AGGREGATIBACTER ACTINOMYCETEMCOMITANS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; DELETION MUTANT; EMAA GENE; GENE LOCATION; MOUTH FLORA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY;

ADHESINS, BACTERIAL; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACTERIAL ADHESION; BINDING SITES; COLLAGEN TYPE V; CONSENSUS SEQUENCE; DNA MUTATIONAL ANALYSIS; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; PASTEURELLACEAE; PROTEIN STRUCTURE, TERTIARY; SEQUENCE DELETION;

EID: 42549117252     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01709-07     Document Type: Article

References (43)

1. Aebi, C., E. R. Lafontaine, L. D. Cope, J. L. Latimer, S. L. Lumbley, G. H. McCracken, Jr., and E. J. Hansen. 1998. Phenotypic effect of isogenic uspA1 and uspA2 mutations on Moraxella catarrhalis 035E. Infect. Immun. 66:3113-3119.
2. Aebi, C., I. Maciver, J. L. Latimer, L. D. Cope, M. K. Stevens, S. E. Thomas, G. H. McCracken, Jr., and E. J. Hansen. 1997. A protective epitope of Moraxella catarrhalis is encoded by two different genes. Infect. Immun. 65: 4367-4377.
3. Cotter, S. E., N. K. Surana, S. Grass, and J. W. St Geme III. 2006. Trimeric autotransporters require trimerization of the passenger domain for stability and adhesive activity. J. Bacteriol. 188:5400-5407.
4. Cotter, S. E., N. K. Surana, and J. W. St Geme III. 2005. Trimeric autotransporters: a distinct subfamily of autotransporter proteins. Trends Microbiol. 13:199-205.
5. Duguid, J. P., I. W. Smith, G. Dempster, and P. N. Edmunds. 1955. Non-flagellar filamentous appendages (fimbriae) and haemagglutinating activity in Bacterium coli. J. Pathol. Bacteriol. 70:335-348.
6. Emody, L., J. Heesemann, H. Wolf-Watz, M. Skurnik, G. Kapperud, P. O'Toole, and T. Wadstrom. 1989. Binding to collagen by Yersinia enterocolitica and Yersinia pseudotuberculosis: evidence for YopA-mediated and chromosomally encoded mechanisms. J. Bacteriol. 171:6674-6679.
7. Fives-Taylor, P., D. Meyer, and K. Mintz. 1995. Characteristics of Actinobacillus actinomycetemcomitans invasion of and adhesion to cultured epithelial cells. Adv. Dent. Res. 9:55-62.
8. Fothergill-Gilmore, L. A., and P. A. Michels. 1993. Evolution of glycolysis. Prog. Biophys. Mol. Biol. 59:105-235.
9. Grant, S. G., J. Jessee, F. R. Bloom, and D. Hanahan. 1990. Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc. Natl. Acad. Sci. USA 87:4645-4649.
10. Haubek, D., O. K. Ennibi, L. Abdellaoui, N. Benzarti, and S. Poulsen. 2002. Attachment loss in Moroccan early onset periodontitis patients and infection with the JP2-type of Actinobacillus actinomycetemcomitans. J. Clin. Periodontal 29:657-660.
11. Henderson, I. R., F. Navarro-Garcia, and J. P. Nataro. 1998. The great escape: structure and function of the autotransporter proteins. Trends Microbiol. 6:370-378.
12. 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.
13. Hultgren, S. J., S. Abraham, M. Caparon, P. Falk, J. W. St Geme III, and S. Normark. 1993. Pilus and nonpilus bacterial adhesins: assembly and function in cell recognition. Cell 73:887-901.
14. Hultgren, S. J., S. Normark, and S. N. Abraham. 1991. Chaperone-assisted assembly and molecular architecture of adhesive pili. Annu. Rev. Microbiol. 45:383-415.
15. Jose, J., F. Jahnig, and T. F. Meyer. 1995. Common structural features of IgA1 protease-like outer membrane protein autotransporters. Mol. Microbiol. 18:378-380.
16. Koretke, K. K., P. Szczesny, M. Gruber, and A. N. Lupas. 2006. Model structure of the prototypical non-fimbrial adhesin YadA of Yersinia enterocolitica. J. Struct. Biol. 155:154-161.
17. Laarmann, S., D. Cutter, T. Juehne, S. J. Barenkamp, and J. W. St Geme. 2002. The Haemophilus influenzae Hia autotransporter harbours two adhesive pockets that reside in the passenger domain and recognize the same host cell receptor. Mol. Microbiol. 46:731-743.
18. 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.
19. Leininger, E., M. Roberts, J. G. Kenimer, I. G. Charles, N. Fairweather, P. Novotny, and M. J. Brennan. 1991. Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc. Natl. Acad. Sci. USA 88:345-349.
20. Li, L. J., G. Dougan, P. Novotny, and I. G. Charles. 1991. P.70 pertactin, an outer-membrane protein from Bordetella parapertussis: cloning, nucleotide sequence and surface expression in Escherichia coli. Mol. Microbiol. 5:409-417.
21. 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.
22. Mintz, K. P., and P. M. Fives-Taylor. 1994. Adhesion of Actinobacillus actinomycetemcomitans to a human oral cell line. Infect. Immun. 62:3672-3678.
23. Mintz, K. P., and P. M. Fives-Taylor. 1999. Binding of the periodontal pathogen Actinobacillus actinomycetemcomitans to extracellular matrix proteins. Oral Microbiol. Immunol. 14:109-116.
24. Nikaido, H. 1994. Isolation of outer membranes. Methods Enzymol. 235: 225-234.
25. Nummelin, H., M. C. Merckel, J. C. Leo, H. Lankinen, M. Skurnik, and A. Goldman. 2004. The Yersinia adhesin YadA collagen-binding domain structure is a novel left-handed parallel beta-roll. EMBO J. 23:701-711.
26. 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.
27. Pohlner, J., R. Halter, K. Beyreuther, and T. F. Meyer. 1987. Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325:458-462.
28. Ray, S. K., R. Rajeshwari, Y. Sharma, and R. V. Sonti. 2002. A high-molecular-weight outer membrane protein of Xanthomonas oryzae pv. oryzae exhibits similarity to non-fimbrial adhesins of animal pathogenic bacteria and is required for optimum virulence. Mol. Microbiol. 46:637-647.
29. Riess, T., S. G. Andersson, A. Lupas, M. Schaller, A. Schafer, P. Kyme, J. Martin, J. H. Walzlein, U. Ehehalt, H. Lindroos, M. Schirle, A. Nordheim, I. B. Autenrieth, and V. A. Kempf. 2004. Bartonella adhesin a mediates a proangiogenic host cell response. J. Exp. Med. 200:1267-1278.
30. Roggenkamp, A., N. Ackermann, C. A. Jacobi, K. Truelzsch, H. Hoffmann, and J. Heesemann. 2003. Molecular analysis of transport and oligomerization of the Yersinia enterocolitica adhesin YadA. J. Bacteriol. 185:3735-3744.
31. 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.
32. 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.
33. 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.
34. Sreenivasan, P. K., D. J. LeBlanc, L. N. Lee, and P. Fives-Taylor. 1991. Transformation of Actinobacillus actinomycetemcomitans by electroporation, utilizing constructed shuttle plasmids. Infect. Immun. 59:4621-4627.
35. St Geme, J. W., III, and D. Cutter. 2000. The Haemophilus influenzae Hia adhesin is an autotransporter protein that remains uncleaved at the C terminus and fully cell associated. J. Bacteriol. 182:6005-6013.
36. Surana, N. K., D. Cutter, S. J. Barenkamp, and J. W. St Geme III. 2004. The Haemophilus influenzae Hia autotransporter contains an unusually short trimeric translocator domain. J. Biol. Chem. 279:14679-14685.
37. Tahir, Y. E., P. Kuusela, and M. Skurnik. 2000. Functional mapping of the Yersinia enterocolitica adhesin YadA: identification of eight NSVAIG-S motifs in the amino-terminal half of the protein involved in collagen binding. Mol. Microbiol. 37:192-206.
38. Tamm, A., A. M. Tarkkanen, T. K. Korhonen, P. Kuusela, P. Toivanen, and M. Skurnik. 1993. Hydrophobic domains affect the collagen-binding specificity and surface polymerization as well as the virulence potential of the YadA protein of Yersinia enterocolitica. Mol. Microbiol. 10:995-1011.
39. Tang, G., T. Ruiz, R. Barrantes-Reynolds, and K. P. Mintz. 2007. Molecular heterogeneity of EmaA, an oligomeric autotransporter adhesin of Aggregatibacter (Actinobacillus) actinomycetemcomitans. Microbiology 153:2447-2457.
40. Thornley, M. J., and R. W. Horne. 1962. Electron microscope observations on the structure of fimbriae, with particular reference to Klebsiella strains, by the use of the negative staining technique. J. Gen. Microbiol. 28:51-56.
41. Wickner, W., A. J. Driessen, and F. U. Hartl. 1991. The enzymology of protein translocation across the Escherichia coli plasma membrane. Annu. Rev. Biochem. 60:101-124.
42. Yeo, H. J., S. E. Cotter, S. Laarmann, T. Juehne, J. W. St Geme III, and G. Waksman. 2004. Structural basis for host recognition by the Haemophilus influenzae Hia autotransporter. EMBO J. 23:1245-1256.
43. Zhang, P., B. B. Chomel, M. K. Schau, J. S. Goo, S. Droz, K. L. Kelminson, S. S. George, N. W. Lerche, and J. E. Koehler. 2004. A family of variably expressed outer-membrane proteins (Vomp) mediates adhesion and autoaggregation in Bartonella quintana. Proc. Natl. Acad. Sci. USA 101:13630-13635.