Identification of a novel trimeric autotransporter adhesin in the cryptic genospecies of Haemophilus

Journal of Bacteriology

Volumn 190, Issue 12, 2008, Pages 4313-4320

  Sheets, Amanda J ^a   Grass, Susan A ^a   Miller, Sara E ^a   St Geme III, Joseph W ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; CHA PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM CULTURE; BACTERIUM DETECTION; BACTERIUM ISOLATE; BACTERIUM MUTANT; CARBOXY TERMINAL SEQUENCE; CELL LINE; CELL SURFACE; FEMALE GENITAL TRACT INFECTION; GENE SEQUENCE; GENETIC CONSERVATION; HAEMOPHILUS; HAEMOPHILUS INFLUENZAE; HUMAN; HUMAN CELL; NEWBORN INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PATHOGENESIS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; STRUCTURAL HOMOLOGY; TRANSPOSON; WESTERN BLOTTING;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; BLOTTING, SOUTHERN; CELL LINE; DIMERIZATION; HAEMOPHILUS; HELA CELLS; HUMANS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MUTATION; POLYMERASE CHAIN REACTION;

BACTERIA (MICROORGANISMS); HAEMOPHILUS; HAEMOPHILUS INFLUENZAE;

EID: 44949085632     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01963-07     Document Type: Article

References (53)

1. Albritton, W. L., J. L. Brunton, M. Meier, M. N. Bowman, and L. A. Slaney. 1982. Haemophilus influenzae: comparison of respiratory tract isolates with genitourinary tract isolates. J. Clin. Microbiol. 16:826-831.
2. Bateman, A., E. Birney, L. Cerruti, R. Durbin, L. Etwiller, S. R. Eddy, S. Griffiths-Jones, K. L. Howe, M. Marshall, and E. L. Sonnhammer. 2002. The Pfam protein families database. Nucleic Acids Res. 30:276-280.
3. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
4. Bruant, G., N. Gousset, R. Quentin, and A. Rosenau. 2002. Fimbrial ghf gene cluster of genital strains of Haemophilus spp. Infect. Immun. 70:5438-5445.
5. Bullard, B., S. Lipski, and E. R. Lafontaine. 2007. Regions important for the adhesin activity of Moraxella catarrhalis Hag. BMC Microbiol. 7:65.
6. Bullard, B., S. L. Lipski, and E. R. Lafontaine. 2005. Hag directly mediates the adherence of Moraxella catarrhalis to human middle ear cells. Infect. Immun. 73:5127-5136.
7. Campognone, P., and D. B. Singer. 1986. Neonatal sepsis due to nontypable Haemophilus influenzae. Am. J. Dis. Child. 140:117-121.
8. Carlone, G. M., M. L. Thomas, H. S. Rumschlag, and F. O. Sottnek. 1986. Rapid microprocedure for isolating detergent-insoluble outer membrane proteins from Haemophilus species. J. Clin. Microbiol. 24:330-332.
9. Clemans, D. L., C. F. Marrs, R. J. Bauer, M. Patel, and J. R. Gilsdorf. 2001. Analysis of pilus adhesins from Haemophilus influenzae biotype IV strains. Infect. Immun. 69:7010-7019.
10. 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.
11. 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.
12. Dower, W. J., J. F. Miller, and C. W. Ragsdale. 1988. High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res. 16:6127-6145.
13. El Tahir, Y., and M. Skurnik. 2001. YadA, the multifaceted Yersinia adhesin. Int. J. Med. Microbiol. 291:209-218.
14. Friesen, C. A., and C. T. Cho. 1986. Characteristic features of neonatal sepsis due to Haemophilus influenzae. Rev. Infect. Dis. 8:777-780.
15. Geme, J. W., III, and D. Cutter. 1995. Evidence that surface fibrils expressed by Haemophilus influenzae type b promote attachment to human epithelial cells. Mol. Microbiol. 15:77-85.
16. Gill, M. V., P. E. Schoch, J. M. Musser, and B. A. Cunha. 1995. Bacteremia and chorioamnionitis due to cryptic genospecies of Haemophilus Influenzae biotype I. Eur. J. Clin. Microbiol. Infect. Dis. 14:1088-1090.
17. Gousset, N., A. Rosenau, P. Y. Sizaret, and R. Quentin. 1999. Nucleotide sequences of genes coding for fimbrial proteins in a cryptic genospecies of Haemophilus spp. isolated from neonatal and genital tract infections. Infect. Immun. 67:8-15.
18. Gravekamp, C., D. L. Kasper, J. L. Michel, D. E. Kling, V. Carey, and L. C. Madoff. 1997. Immunogenicity and protective efficacy of the alpha C protein of group B streptococci are inversely related to the number of repeats. Infect. Immun. 65:5216-5221.
19. Gravekamp, C., B. Rosner, and L. C. Madoff. 1998. Deletion of repeats in the alpha C protein enhances the pathogenicity of group B streptococci in immune mice. Infect. Immun. 66:4347-4354.
20. Hendrixson, D. R., B. J. Akerley, and V. J. DiRita. 2001. Transposon mutagenesis of Campylobacter jejuni identifies a bipartite energy taxis system required for motility. Mol. Microbiol. 40:214-224.
21. Herriott, R. M., E. M. Meyer, and M. Vogt. 1970. Defined nongrowth media for stage II development of competence in Haemophilus influenzae. J. Bacteriol. 101:517-524.
22. 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.
23. Kehl-Fie, T. E., and J. W. St. Geme III. 2007. Identification and characterization of an RTX toxin in the emerging pathogen Kingella kingae. J. Bacteriol. 189:430-436.
24. 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.
25. Linke, D., T. Riess, I. B. Autenrieth, A. Lupas, and V. A. Kempf. 2006. Trimeric autotransporter adhesins: variable structure, common function. Trends Microbiol. 14:264-270.
26. Martel, A. Y., G. St-Laurent, L. A. Dansereau, and M. G. Bergeron. 1989. Isolation and biochemical characterization of Haemophilus species isolated simultaneously from the oropharyngeal and anogenital areas. J. Clin. Microbiol. 27:1486-1489.
27. Martínez, M. A., A. Ovalle, M. T. Ulloa, and R. M. Vidal. 1999. Role of Haemophilus influenzae in intra-amniotic infection in patients with preterm rupture of membranes. Eur. J. Clin. Microbiol. Infect. Dis. 18:890-892.
28. Murphy, T. F., C. Kirkham, and D. J. Sikkema. 1992. Neonatal, urogenital isolates of biotype 4 nontypeable Haemophilus influenzae express a variant P6 outer membrane protein molecule. Infect. Immun. 60:2016-2022.
29. Musser, J. M., S. J. Barenkamp, D. M. Granoff, and R. K. Selander. 1986. Genetic relationships of serologically nontypable and serotype b strains of Haemophilus influenzae. Infect. Immun. 52:183-191.
30. 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.
31. Quentin, R., A. Goudeau, R. J. Wallace, Jr., A. L. Smith, R. K. Selander, and J. M. Musser. 1990. Urogenital, maternal and neonatal isolates of Haemophilus influenzae: identification of unusually virulent serologically non-typable clone families and evidence for a new Haemophilus species. J. Gen. Microbiol. 136:1203-1209.
32. Quentin, R., C. Martin, J. M. Musser, N. Pasquier-Picard, and A. Goudeau. 1993. Genetic characterization of a cryptic genospecies of Haemophilus causing urogenital and neonatal infections. J. Clin. Microbiol. 31:1111-1116.
33. Quentin, R., J. M. Musser, M. Mellouet, P. Y. Sizaret, R. K. Selander, and A. Goudeau. 1989. Typing of urogenital, maternal, and neonatal isolates of Haemophilus influenzae and Haemophilus parainfluenzae in correlation with clinical source of isolation and evidence for a genital specificity of H. influenzae biotype IV. J. Clin. Microbiol. 27:2286-2294.
34. Quentin, R., R. Ruimy, A. Rosenau, J. M. Musser, and R. Christen. 1996. Genetic identification of cryptic genospecies of Haemophilus causing urogenital and neonatal infections by PCR using specific primers targeting genes coding for 16S rRNA. J. Clin. Microbiol. 34:1380-1385.
35. 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.
36. Riess, T., S. G. Andersson, A. Lupas, M. Schaller, A. Schafer, P. Kyme, J. Martin, J.-H. Wälzlein, 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.
37. 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.
38. Rosenau, A., P. Y. Sizaret, J. M. Musser, A. Goudeau, and R. Quentin. 1993. Adherence to human cells of a cryptic Haemophilus genospecies responsible for genital and neonatal infections. Infect. Immun. 61:4112-4118.
39. Rusin, P., R. D. Adam, E. A. Peterson, K. J. Ryan, N. A. Sinclair, and L. Weinstein. 1991. Haemophilus influenzae: an important cause of maternal and neonatal infections. Obstet. Gynecol. 77:92-96.
40. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. Setlow, J. K., D. C. Brown, M. E. Boling, A. Mattingly, and M. P. Gordon. 1968. Repair of deoxyribonucleic acid in Haemophilus influenzae. I. X-ray sensitivity of ultraviolet-sensitive mutants and their behavior as hosts to ultraviolet-irradiated bacteriophage and transforming deoxyribonucleic acid. J. Bacteriol. 95:546-558.
42. St. Geme, J. W., III. 2002. Molecular and cellular determinants of non-typeable Haemophilus influenzae adherence and invasion. Cell. Microbiol. 4:191-200.
43. St. Geme, J. W., III. 1993. Nontypeable Haemophilus influenzae disease: epidemiology, pathogenesis, and prospects for prevention. Infect. Agents Dis. 2:1-16.
44. 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.
45. St. Geme, J. W., III, D. Cutter, and S. J. Barenkamp. 1996. Characterization of the genetic locus encoding Haemophilus influenzae type b surface fibrils. J. Bacteriol. 178:6281-6287.
46. St. Geme, J. W., III, and S. Falkow. 1990. Haemophilus influenzae adheres to and enters cultured human epithelial cells. Infect. Immun. 58:4036-4044.
47. St. Geme, J. W., III, S. Falkow, and S. J. Barenkamp. 1993. High-molecular-weight proteins of nontypable Haemophilus influenzae mediate attachment to human epithelial cells. Proc. Natl. Acad. Sci. USA 90:2875-2879.
48. St. Geme, J. W., III, V. V. Kumar, D. Cutter, and S. J. Barenkamp. 1998. Prevalence and distribution of the hmw and hia genes and the HMW and Hia adhesins among genetically diverse strains of nontypeable Haemophilus influenzae. Infect. Immun. 66:364-368.
49. 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.
50. Tiyawisutsri, R., M. T. Holden, S. Tumapa, S. Rengpipat, S. R. Clarke, S. J. Foster, W. C. Nierman, N. P. Day, and S. J. Peacock. 2007. Burkholderia Hep_Hag autotransporter (BuHA) proteins elicit a strong antibody response during experimental glanders but not human melioidosis. BMC Microbiol. 7:19.
51. Turk, D. C. 1984. The pathogenicity of Haemophilus influenzae. J. Med. Microbiol. 18:1-16.
52. Wallace, R. J., Jr., C. J. Baker, F. J. Quinones, D. G. Hollis, R. E. Weaver, and K. Wiss. 1983. Nontypable Haemophilus influenzae (biotype 4) as a neonatal, maternal, and genital pathogen. Rev. Infect. Dis. 5:123-136.
53. 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.