HadA is an atypical new multifunctional trimeric coiled-coil adhesin of Haemophilus influenzae biogroup aegyptius, which promotes entry into host cells

Cellular Microbiology

Volumn 11, Issue 7, 2009, Pages 1044-1063

  Serruto, Davide ^a   Spadafina, Tiziana ^a   Scarselli, Maria ^a   Bambini, Stefania ^a   Comanducci, Maurizio ^a   Höhle, Sonja ^b   Kilian, Mogens ^b   Veiga, Esteban ^c,d,e   Cossart, Pascale ^c,d,e   Oggioni, Marco R ^f   Savino, Silvana ^a   Ferlenghi, Ilaria ^a   Taddei, Anna Rita ^g   Rappuoli, Rino ^a   Pizza, Mariagrazia ^a   Masignani, Vega ^a   Aricò, Beatrice ^a  

^a NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

^b AARHUS UNIVERSITY   (Denmark)

^c INSTITUT PASTEUR   (France)

^d INSERM   (France)

^e USC 2020   (France)

^f UNIVERSITY OF SIENA   (Italy)

^g UNIVERSITY OF TUSCIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; CLATHRIN; CYTOSKELETON PROTEIN; HAEMOPHILUS ADHESIN A; OLIGOMERIC COILED COIL ADHESIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM ISOLATION; BINDING AFFINITY; BRAZILIAN PURPURIC FEVER; CELL INVASION; CONTROLLED STUDY; DNA SEQUENCE; ESCHERICHIA COLI; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE STRUCTURE; HAEMOPHILUS INFLUENZAE; HOST CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; RECEPTOR BINDING; SEQUENCE HOMOLOGY;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; BACTERIAL PROTEINS; BINDING SITES; CELL LINE; COMPUTATIONAL BIOLOGY; DNA, BACTERIAL; GENOMICS; HAEMOPHILUS INFLUENZAE; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, QUATERNARY; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HAEMOPHILUS; HAEMOPHILUS INFLUENZAE BIOTYPE AEGYPTIUS; MAMMALIA; NEISSERIA MENINGITIDIS; OXALIS TUBEROSA; YERSINIA ENTEROCOLITICA;

EID: 66749138696     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2009.01306.x     Document Type: Article

References (64)

1. Abu el-Asrar, A.M., Geboes, K., al-Kharashi, S.A., al-Mosallam, A.A., Tabbara, K.F., al-Rajhi, A.A., and Missotten, L. (1998) An immunohistochemical study of collagens in trachoma and vernal keratoconjunctivitis. Eye 12: 1001-1006.
2. Abu El-Asrar, A.M., Meersschaert, A., Al-Kharashi, S.A., Missotten, L., and Geboes, K. (2003) Immuno-histochemical evaluation of conjunctival remodelling in vernal keratoconjunctivitis. Eye 17: 767-771.
3. Bliska, J.B., Copass, M.C., and Falkow, S. (1993a) The Yersinia pseudotuberculosis adhesin YadA mediates intimate bacterial attachment to and entry into HEp-2 cells. Infect Immun 61: 3914-3921.
4. Bliska, J.B., Galan, J.E., and Falkow, S. (1993b) Signal transduction in the mammalian cell during bacterial attachment and entry. Cell 73: 903-920.
5. Brenner, D.J., Mayer, L.W., Carlone, G.M., Harrison, L.H., Bibb, W.F., Brandileone, M.C., et al. (1988) Biochemical, genetic, and epidemiologic characterization of Haemophilus influenzae biogroup aegyptius (Haemophilus aegyptius) strains associated with Brazilian purpuric fever. J Clin Microbiol 26: 1524-1534.
6. Capecchi, B., Adu-Bobie, J., Di Marcello, F., Ciucchi, L., Masignani, V., Taddei, A., et al. (2005) Neisseria meningitidis NadA is a new invasin which promotes bacterial adhesion to and penetration into human epithelial cells. Mol Microbiol 55: 687-698.
7. Carlone, G.M., Thomas, M.L., Rumschlag, H.S., and Sottnek, F.O. (1986) Rapid microprocedure for isolating detergent-insoluble outer membrane proteins from Haemophilus species. J Clin Microbiol 24: 330-332.
8. CDC (1985) Preliminary report: Epidemic fatal purpuric fever among children -Brazil. MMWR Morb Mortal Wkly Rep 34: 217-219.
9. Comanducci, M., Bambini, S., Brunelli, B., Adu-Bobie, J., Arico, B., Capecchi, B., et al. (2002) NadA, a novel vaccine candidate of Neisseria meningitidis. J Exp Med 195: 1445-1454.
10. Cornelis, G.R., Boland, A., Boyd, A.P., Geuijen, C., Iriarte, M., Neyt, C., et al. (1998) The virulence plasmid of Yersinia, an antihost genome. Microbiol Mol Biol Rev 62: 1315-1352.
11. Cossart, P., and Sansonetti, P.J. (2004) Bacterial invasion: The paradigms of enteroinvasive pathogens. Science 304: 242-248.
12. Cotter, S.E., Surana, N.K., and St Geme, J.W., 3rd (2005) Trimeric autotransporters: A distinct subfamily of autotransporter proteins. Trends Microbiol 13: 199-205.
13. Davies, R.L., Wall, R.A., and Borriello, S.P. (1990) Comparison of methods for the analysis of outer membrane antigens of Neisseria meningitidis by western blotting. J Immunol Meth 134: 215-225.
14. Desvaux, M., Parham, N.J., and Henderson, I.R. (2004) The autotransporter secretion system. Res Microbiol 155: 53-60.
15. Dubochet, J., Adrian, M., Chang, J.J., Homo, J.C., Lepault, J., McDowall, A.W., and Schultz, P. (1988) Cryo-electron microscopy of vitrified specimens. Q Rev Biophys 21: 129-228.
16. Eitel, J., and Dersch, P. (2002) The YadA protein of Yersinia pseudotuberculosis mediates high-efficiency uptake into human cells under environmental conditions in which invasin is repressed. Infect Immun 70: 4880-4891.
17. El Tahir, Y.S.M. (2001) YadA, the multifaceted Yersinia adhesin. Int J Med Microbiol 291: 209-218.
18. Farley, M.M., Whitney, A.M., Spellman, P., Quinn, F.D., Weyant, R.S., Mayer, L., and Stephens, D.S. (1992) Analysis of the attachment and invasion of human epithelial cells by Haemophilus influenzae biogroup aegyptius. J Infect Dis 165 (Suppl. 1): S111-S114.
19. Frankel, G., Lider, O., Hershkoviz, R., Mould, A.P., Kachalsky, S.G., Candy, D.C., et al. (1996) The cell-binding domain of intimin from enteropathogenic Escherichia coli binds to beta1 integrins. J Biol Chem 271: 20359-20364.
20. Girard, V., and Mourez, M. (2006) Adhesion mediated by autotransporters of Gram-negative bacteria: Structural and functional features. Res Microbiol 157: 407-416.
21. Group, T.B.P.F.S. (1992) Brazilian purpuric fever identified in a new region of Brazil. The Brazilian Purpuric Fever Study Group. J Infect Dis 165 (Suppl. 1): S16-S19.
22. Harrison, L.H., Simonsen, V., and Waldman, E.A. (2008) Emergence and disappearance of a virulent clone of Haemophilus influenzae biogroup aegyptius, cause of Brazilian purpuric fever. Clin Microbiol Rev 21: 594-605.
23. Hasman, H., Chakraborty, T., and Klemm, P. (1999) Antigen-43-mediated autoaggregation of Escherichia coli is blocked by fimbriation. J Bacteriol 181: 4834-4841.
24. van Heel, M., Harauz, G., Orlova, E.V., Schmidt, R., and Schatz, M. (1996) A new generation of the IMAGIC image processing system. J Struct Biol 116: 17-24.
25. Heise, T., and Dersch, P. (2006) Identification of a domain in Yersinia virulence factor YadA that is crucial for extracellular matrix-specific cell adhesion and uptake. Proc Natl Acad Sci USA 103: 3375-3380.
26. Hill, D.J., and Virji, M. (2003) A novel cell-binding mechanism of Moraxella catarrhalis ubiquitous surface protein UspA: Specific targeting of the N-domain of carcinoembryonic antigen-related cell adhesion molecules by UspA1. Mol Microbiol 48: 117-129.
27. Hill, D.J., Edwards, A.M., Rowe, H.A., Virji M. (2005) Carcinoembryonic antigen-related cell adhesion molecule (CEACAM)-binding recombinant polypeptide confers protection against infection by respiratory and urogenital pathogens. Mol Microbiol 55: 1515-1527.
28. Hoiczyk, E., Roggenkamp, A., Reichenbecher, M., Lupas A., and Heesemann, J. (2000) Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J 19: 5989-5999.
29. Iriarte, M., and Cornelis, G.R. (1996) Molecular determinants of Yersinia pathogenesis. Microbiologia 12: 267-280.
30. Kilian, M., Poulsen, K., and Lomholt, H. (2002) Evolution of the paralogous hap and iga genes in Haemophilus influenzae: Evidence for a conserved hap pseudogene associated with microcolony formation in the recently diverged Haemophilus aegyptius and H.influenzae biogroup aegyptius. Mol Microbiol 46: 1367-1380.
31. Klemm, P., Vejborg, R.M., and Sherlock, O. (2006) Self-associating autotransporters, SAATs: Functional and structural similarities. Int J Med Microbiol 296: 187-195.
32. Laarmann, S., Cutter, D., Juehne, T., Barenkamp S.J., and St Geme, J.W., III (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.
33. Lafontaine, E.R., Cope, L.D., Aebi, C., Latimer, J.L., and McCracken, G.H., Jr, Hansen, E.J. (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.
34. Li, L., Matevski, D., Aspiras, M., Ellen, R.P., and Lepine, G. (2004) Two epithelial cell invasion-related loci of the oral pathogen Actinobacillus actinomycetemcomitans. Oral Microbiol Immunol 19: 16-25.
35. Li, M.S., Farrant, J.L., Langford, P.R., and Kroll, J.S. (2003) Identification and characterization of genomic loci unique to the Brazilian purpuric fever clonal group of H.influenzae biogroup aegyptius: Functionality explored using meningococcal homology. Mol Microbiol 47: 1101-1111.
36. Linke, D., Riess, T., Autenrieth, I.B., Lupas, A., and Kempf, V.A. (2006) Trimeric autotransporter adhesins: Variable structure, common function. Trends Microbiol 14: 264-270.
37. Ludtke, S.J., Baldwin, P.R., and Chiu, W. (1999) EMAN: Semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128: 82-97.
38. McMichael, J.C., Fiske, M.J., Fredenburg, R.A., Chakravarti, D.N., VanDerMeid, K.R., Barniak, V., et al. (1998) Isolation and characterization of two proteins from Moraxella catarrhalis that bear a common epitope. Infect Immun 66: 4374-4381.
39. Nykvist, P., Tasanen, K., Viitasalo, T., Kapyla, J., Jokinen, J., Bruckner-Tuderman, L., and Heino, J. (2001) The cell adhesion domain of type XVII collagen promotes integrin-mediated cell spreading by a novel mechanism. J Biol Chem 276: 38673-38679.
40. Ochiai, K., Kurita-Ochiai, T., Kamino, Y., and Ikeda, T. (1993) Effect of co-aggregation on the pathogenicity of oral bacteria. J Med Microbiol 39: 183-190.
41. Quinn, F.D., Weyant, R.S., Worley, M.J., White, E.H., Utt, E.A., and Ades, E.A. (1995) Human microvascular endothelial tissue culture cell model for studying pathogenesis of Brazilian purpuric fever. Infect Immun 63: 2317-2322.
42. Ray, S.K., Rajeshwari, R., Sharma, Y., and Sonti, R.V. (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 Microbiology 46: 637-647.
43. Relman, D., Tuomanen, E., Falkow, S., Golenbock, D.T., Saukkonen, K., and Wright, S.D. (1990) Recognition of a bacterial adhesion by an integrin: Macrophage CR3 (alpha M beta 2, CD11b/CD18) binds filamentous hemagglutinin of Bordetella pertussis. Cell 61: 1375-1382.
44. Riess, T., Andersson, S.G., Lupas, A., Schaller, M., Schafer, A., Kyme, P., et al. (2004) Bartonella adhesin a mediates a proangiogenic host cell response. J Exp Med 200: 1267-1278.
45. Roggenkamp, A., Ackermann, N., Jacobi, C.A., Truelzsch, K., Hoffmann, H., and Heesemann, J. (2003) Molecular analysis of transport and oligomerization of the Yersinia enterocolitica adhesin YadA. J Bacteriol 185: 3735-3744.
46. Rosenshine, I., Donnenberg, M.S., Kaper, J.B., and Finlay, B.B. (1992a) Signal transduction between enteropathogenic Escherichia coli (EPEC) and epithelial cells: EPEC induces tyrosine phosphorylation of host cell proteins to initiate cytoskeletal rearrangement and bacterial uptake. Embo J 11: 3551-3560.
47. Rosenshine, I., Duronio, V., and Finlay, B.B. (1992b) Tyrosine protein kinase inhibitors block invasin-promoted bacterial uptake by epithelial cells. Infect Immun 60: 2211-2217.
48. Rosenshine, I., Ruschkowski, S., and Finlay, B.B. (1994) Inhibitors of cytoskeletal function and signal transduction to study bacterial invasion. Meth Enzymol 236: 467-476.
49. Scarselli, M., Serruto, D., Montanari, P., Capecchi, B., Adu-Bobie, J., Veggi, D., et al. (2006) Neisseria meningitidis NhhA is a multifunctional trimeric autotransporter adhesin. Mol Microbiol 61: 631-644.
50. Segada, L.M., and Lesse, A.J. (1997) Creation of an isogenic P1-deficient mutant of Haemophilus influenzae biogroup aegyptius. Gene 204: 185-194.
51. Sherlock, O., Schembri, M.A., Reisner, A., and Klemm, P. (2004) Novel roles for the AIDA adhesin from diarrheagenic Escherichia coli: Cell aggregation and biofilm formation. J Bacteriol 186: 8058-8065.
52. Sherlock, O., Vejborg, R.M., and Klemm, P. (2005) The TibA adhesin/ invasin from enterotoxigenic Escherichia coli is self recognizing and induces bacterial aggregation and biofilm formation. Infect Immun 73: 1954-1963.
53. Skurnik, M., el Tahir, Y., Saarinen, M., Jalkanen, S., and Toivanen, P. (1994) YadA mediates specific binding of enteropathogenic Yersinia enterocolitica to human intestinal submucosa. Infect Immun 62: 1252-1261.
54. Smoot, L.M., Franke, D.D., McGillivary, G., and Actis, L.A. (2002) Genomic analysis of the F3031 Brazilian purpuric fever clone of Haemophilus influenzae biogroup aegyptius by PCR-based subtractive hybridization. Infect Immun 70: 2694-2699.
55. St Geme, J.W., 3rd, Gilsdorf J.R., and Falkow, S. (1991) Surface structures and adherence properties of diverse strains of Haemophilus influenzae biogroup aegyptius. Infect Immun 59: 3366-3371.
56. Surana, N.K. Cutter, D., Barenkamp S.J., and St Geme, J.W., III (2004) The Haemophilus influenzae Hia autotransporter contains an unusually short trimeric translocator domain. J Biol Chem 279: 14679-14685.
57. Szczesny, P., and Lupas, A. (2008) Domain annotation of trimeric autotransporter adhesins -daTAA. Bioinformatics (Oxford, England) 24: 1251-1256.
58. Veiga, E., and Cossart, P. (2005) Listeria hijacks the clathrin-dependent endocytic machinery to invade mammalian cells. Nature Cell Biology 7: 894-900.
59. Veiga, E., and Cossart, P. (2006) The role of clathrin-dependent endocytosis in bacterial internalization. Trends Cell Biology 16: 499-504.
60. Veiga, E., Guttman, J.A., Bonazzi, M., Boucrot, E., Toledo-Arana, A., Lin, A.E., et al. (2007) Invasive and adherent bacterial pathogens co-Opt host clathrin for infection. Cell Host Microbe 2: 340-351.
61. Weyant, R.S., Bibb, W.F., Stephens, D.S., Holloway, B.P., Moo-Penn, W.F., Birkness, K.A., et al. (1990) Purification and characterization of a pilin specific for Brazilian purpuric fever-associated Haemophilus influenzae biogroup aegyptius (H.aegyptius) strains. J Clin Microbiol 28: 756-763.
62. Whitney, A.M., and Farley, M.M. (1993) Cloning and sequence analysis of the structural pilin gene of Brazilian purpuric fever-associated Haemophilus influenzae biogroup aegyptius. Infect Immun 61: 1559-1562.
63. Yang, Y., and Isberg, R.R. (1993) Cellular internalization in the absence of invasin expression is promoted by the Yersinia pseudotuberculosis yadA product. Infect Immun 61: 3907-3913.
64. Zhang, P., Chomel, B.B., Schau, M.K., Goo, J.S., Droz, S., Kelminson, K.L., et al. (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.