Structural determinants of the interaction between the Haemophilus influenzae Hap autotransporter and fibronectin

Microbiology (United Kingdom)

Volumn 160, Issue PART 6, 2014, Pages 1182-1190

  Spahich, Nicole A ^a,d   Kenjale, Roma ^a   McCann, Jessica ^a   Meng, Guoyu ^b   Ohashi, Tomoo ^a   Erickson, Harold P ^a   St Geme III, Joseph W ^c  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b SHANGHAI SECOND MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FIBRONECTIN; FIBRONECTIN BINDING PROTEIN; HAP PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING ASSAY; CRYSTAL STRUCTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; HAEMOPHILUS INFLUENZAE; MUTATIONAL ANALYSIS; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; WESTERN BLOTTING;

EID: 84901725893     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.077784-0     Document Type: Article

References (39)

1. Anderson, P., Johnston, R. B., Jr & Smith, D. H. (1972). Human serum activities against Hemophilus influenzae, type b. J Clin Invest 51, 31-38.
2. Bingham, R. J., Rudiño-Piñera, E., Meenan, N. A., Schwarz-Linek, U., Turkenburg, J. P., Höök, M., Garman, E. F. & Potts, J. R. (2008). Crystal structures of fibronectin-binding sites from Staphylococcus aureus FnBPA in complex with fibronectin domains. Proc Natl Acad Sci U S A 105, 12254-12258.
3. Carlone, G. M., Thomas, M. L., Rumschlag, H. S. & Sottnek, F. O. (1986). Rapid microprocedure for isolating detergent-insoluble outer membrane proteins from Haemophilus species. J Clin Microbiol 24, 330-332.
4. de Bentzmann, S., Plotkowski, C. & Puchelle, E. (1996). Receptors in the Pseudomonas aeruginosa adherence to injured and repairing airway epithelium. Am J Respir Crit Care Med 154, S155-S162.
5. Fink, D. L. & St. Geme, J. W., (2003). Chromosomal expression of the Haemophilus influenzae Hap autotransporter allows fine-tuned regulation of adhesive potential via inhibition of intermolecular autoproteolysis. J Bacteriol 185, 1608-1615.
6. Fink, D. L., Green, B. A. & St. Geme, J. W., (2002). The Haemophilus influenzae Hap autotransporter binds to fibronectin, laminin, and collagen IV. Infect Immun 70, 4902-4907.
7. Fink, D. L., Buscher, A. Z., Green, B., Fernsten, P. & St. Geme, J. W., (2003). The Haemophilus influenzae Hap autotransporter mediates microcolony formation and adherence to epithelial cells and extracellular matrix via binding regions in the C-terminal end of the passenger domain. Cell Microbiol 5, 175-186.
8. Foster, T. J. & Höök, M. (1998). Surface protein adhesins of Staphylococcus aureus. Trends Microbiol 6, 484-488.
9. Henderson, I. R. & Nataro, J. P. (2001). Virulence functions of autotransporter proteins. Infect Immun 69, 1231-1243.
10. 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.
11. Jönsson, K., Signäs, C., Müller, H. P. & Lindberg, M. (1991). Two different genes encode fibronectin binding proteins in Staphylococcus aureus. The complete nucleotide sequence and characterization of the second gene. Eur J Biochem 202, 1041-1048.
12. Kingsley, R. A., Santos, R. L., Keestra, A. M., Adams, L. G. & Bäumler, A. J. (2002). Salmonella enterica serotype Typhimurium ShdA is an outer membrane fibronectin-binding protein that is expressed in the intestine. Mol Microbiol 43, 895-905.
13. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
14. Lindgren, P. E., Speziale, P., McGavin, M., Monstein, H. J., Höök, M., Visai, L., Kostiainen, T., Bozzini, S. & Lindberg, M. (1992). Cloning and expression of two different genes from Streptococcus dysgalactiae encoding fibronectin receptors. J Biol Chem 267, 1924-1931.
15. Lindgren, P. E., Signäs, C., Rantamäki, L. & Lindberg, M. (1994). A fibronectin-binding protein from Streptococcus equisimilis: characterization of the gene and identification of the binding domain. Vet Microbiol 41, 235-247.
16. Meng, G., Spahich, N., Kenjale, R., Waksman, G. & St Geme, J. W., (2011). Crystal structure of the Haemophilus influenzae Hap adhesin reveals an intercellular oligomerization mechanism for bacterial aggregation. EMBO J 30, 3864-3874.
17. Mosher, D. F. & McKeown-Longo, P. J. (1985). Assembly of fibronectin-containing extracellular matrix: a glimpse of the machinery. Biopolymers 24, 199-210.
18. Oberhauser, A. F., Badilla-Fernandez, C., Carrion-Vazquez, M. & Fernandez, J. M. (2002). The mechanical hierarchies of fibronectin observed with single-molecule AFM. J Mol Biol 319, 433-447.
19. Ohashi, T. & Erickson, H. P. (2005). Domain unfolding plays a role in superfibronectin formation. J Biol Chem 280, 39143-39151.
20. Ohashi, T. & Erickson, H. P. (2011). Fibronectin aggregation and assembly: the unfolding of the second fibronectin type III domain. J Biol Chem 286, 39188-39199.
21. Pankov, R. & Yamada, K. M. (2002). Fibronectin at a glance. J Cell Sci 115, 3861-3863.
22. Peters, D. M. & Mosher, D. F. (1987). Localization of cell surface sites involved in fibronectin fibrillogenesis. J Cell Biol 104, 121-130.
23. Petersen, T. E., Thøgersen, H. C., Skorstengaard, K., Vibe-Pedersen, K., Sahl, P., Sottrup-Jensen, L. & Magnusson, S. (1983). Partial primary structure of bovine plasma fibronectin: three types of internal homology. Proc Natl Acad Sci U S A 80, 137-141.
24. Potts, J. R. & Campbell, I. D. (1994). Fibronectin structure and assembly. Curr Opin Cell Biol 6, 648-655.
25. Read, R. C., Wilson, R., Rutman, A., Lund, V., Todd, H. C., Brain, A. P., Jeffery, P. K. & Cole, P. J. (1991). Interaction of nontypable Haemophilus influenzae with human respiratory mucosa in vitro. J Infect Dis 163, 549-558.
26. Read, R. C., Rutman, A. A., Jeffery, P. K., Lund, V. J., Brain, A. P., Moxon, E. R., Cole, P. J. & Wilson, R. (1992). Interaction of capsulate Haemophilus influenzae with human airway mucosa in vitro. Infect Immun 60, 3244-3252.
27. Schwarz-Linek, U., Werner, J. M., Pickford, A. R., Gurusiddappa, S., Kim, J. H., Pilka, E. S., Briggs, J. A., Gough, T. S., Höök, M. & other authors (2003). Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature 423, 177-181.
28. Setlow, J. K., Randolph, M. L., Boling, M. E., Mattingly, A., Price, G. & Gordon, M. P. (1968). Repair of DNA in Haemophilus influenzae. II. Excision, repair of single-strand breaks, defects in transformation, and host cell modification in UV-sensitive mutants. Cold Spring Harb Symp Quant Biol 33, 209-218.
29. Signäs, C., Raucci, G., Jönsson, K., Lindgren, P. E., Anantharamaiah, G. M., Höök, M. & Lindberg, M. (1989). Nucleotide sequence of the gene for a fibronectin-binding protein from Staphylococcus aureus: use of this peptide sequence in the synthesis of biologically active peptides. Proc Natl Acad Sci U S A 86, 699-703.
30. Sottile, J. & Wiley, S. (1994). Assembly of amino-terminal fibronectin dimers into the extracellular matrix. J Biol Chem 269, 17192-17198.
31. Spahich, N. A. & St Geme, J. W., (2011). Structure and function of the Haemophilus influenzae autotransporters. Front Cell Infect Microbiol 1, 5.
32. Steinhart, W. L. & Herriott, R. M. (1968). Genetic integration in the heterospecific transformation of Haemophilus influenzae cells by Haemophilus parainfluenzae deoxyribonucleic acid. J Bacteriol 96, 1725-1731.
33. Steukers, L., Glorieux, S., Vandekerckhove, A. P., Favoreel, H. W. & Nauwynck, H. J. (2012). Diverse microbial interactions with the basement membrane barrier. Trends Microbiol 20, 147-155.
34. Tomb, J. F., Barcak, G. J., Chandler, M. S., Redfield, R. J. & Smith, H. O. (1989). Transposon mutagenesis, characterization, and cloning of transformation genes of Haemophilus influenzae Rd. J Bacteriol 171, 3796-3802.
35. Turk, D. C. (1984). The pathogenicity of Haemophilus influenzae. J Med Microbiol 18, 1-16.
36. Vakonakis, I., Staunton, D., Rooney, L. M. & Campbell, I. D. (2007). Interdomain association in fibronectin: insight into cryptic sites and fibrillogenesis. EMBO J 26, 2575-2583.
37. Valentin-Weigand, P., Talay, S. R., Timmis, K. N. & Chhatwal, G. S. (1993). Identification of a fibronectin-binding protein as adhesin of Streptococcus pyogenes. Zentralbl Bakteriol 278, 238-245.
38. Westerlund, B. & Korhonen, T. K. (1993). Bacterial proteins binding to the mammalian extracellular matrix. Mol Microbiol 9, 687-694.
39. Willson, P. J., Albritton, W. L., Slaney, L. & Setlow, J. K. (1989). Characterization of a multiple antibiotic resistance plasmid from Haemophilus ducreyi. Antimicrob Agents Chemother 33, 1627-1630.