Secretion of the Haemophilus influenzae HMW1 and HMW2 adhesins involves a periplasmic intermediate and requires the HMWB and HMWC proteins

Molecular Microbiology

Volumn 27, Issue 3, 1998, Pages 617-630

  St Geme III, Joseph W ^a,b,c   Grass, Susan ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ST LOUIS CHILDREN S HOSPITAL   (United States)

^c St Louis Children's Hospital ^*

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN;

ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; CYTOPLASM; HAEMOPHILUS INFLUENZAE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN SECRETION; UPPER RESPIRATORY TRACT;

ADHESINS, BACTERIAL; ARTIFICIAL GENE FUSION; BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CELL FRACTIONATION; CELL LINE; CELL MEMBRANE; CRYOPRESERVATION; EPITHELIAL CELLS; GENE DELETION; GENES, BACTERIAL; HAEMOPHILUS INFLUENZAE; MICROSCOPY, IMMUNOELECTRON; MUTAGENESIS; PERIPLASM; RESTRICTION MAPPING;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HAEMOPHILUS INFLUENZAE; NEGIBACTERIA;

EID: 0031963491     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1998.00711.x     Document Type: Article

References (63)

1. Amann, E., Ochs, B., and Abel, K.J. (1988) Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Eschehchia coli. Gene 69: 301-315.
2. Anderson, P., Johnston, Jr, R.B., and Smith, D.H. (1972) Human serum activity against Haemophilus influenzae type b. J Clin Invest 51: 31-38.
3. Angus, B.L., Carey, A.M., Caron, D.A., Kropinski, A.M., and Hancock, R.E. (1982) Outer membrane permeability in Pseudomonas aeruginosa: comparison of a wild-type with an antibiotic-supersusceptible mutant. Antimicrob Agents Chemother 21: 299-309.
4. Barenkamp, S.J., and Bodor, F.F. (1989) Development of serum bactericidal activity following non-typable Haemophilus influenzas acute otitis media. Pediatr Infect Dis J 9: 333-339.
5. Barenkamp, S.J., and Leininger, E. (1992) Cloning, expression, and DNA sequence analysis of genes encoding non typeable Haemophilus influenzae high-molecular-weight surface-exposed proteins related to filamentous hemagglutinin of Bordetella pertussis. Infect Immun 60: 1302-1313.
6. Barenkamp, S.J., and St Geme, III, J.W. (1994) Genes encoding high-molecular-weight adhesion proteins of non-typeable Haemophilus influenzae are part of gene clusters. Infect Immun 62: 3320-3328.
7. Beachey, E.H. (1981) Bacterial adherence: adhesin-receptor interactions mediating the attachment of bacteria to mucosal surfaces. J Infect Dis 143: 325-345.
8. Bosch, D., Sholten, M., Verhagen, C., and Tommassen, J. (1989) The role of the carboxy-terminal membrane-spanning fragment in the biogenesis of Escherichia coli K12 outer membrane protein PhoE. Mol Gen Genet 216: 144-148.
9. Boukamp, P., Petrussevska, R.T., Breitkreutz, D., Hornung, J., Markham, A., and Fusenig, N.E. (1988) Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106: 761-771.
10. Chang, A.C., and Cohen, S.N. (1978) Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 134: 1141-1156.
11. Clouthier, S.C., Muller, K.H., Doran, J.L., Collinson, S.K., and Kay, W.W. (1993) Characterization of three fimbrial genes, sefABC, of Salmonella enteritidis. J Bacteriol 175: 2523-2533.
12. Cope, L.D., Yogev, R., Muller-Eberhard, U., and Hansen, E.J. (1995) A gene cluster involved in the utilization of both free heme and heme: hemopexin by Haemophilus influenzae type b. J Bacteriol 177: 2644-2653.
13. Cosma, C.L., Danese, P.N., Carlson, J.H., Silhavy, T.J., and Snyder, W.B. (1995) Mutational activation of the Cpx signal transduction pathway of Escherichia coli suppresses the toxicity conferred by certain envelope-associated stresses. Mol Microbiol 18: 491-505.
14. Danese, P.N., Snyder, W.B., Cosma, C.L., Davis, L.J.B., and Silhavy, T.J. (1995) The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP. Genes Dev 9: 387-398.
15. Dodson, K.W., Jacob-Dubuisson, F., Striker, R.T., and Hultgren, S.J. (1993) Outer membrane PapC usher discriminately recognizes periplasmic chaperone-pilus subunit complexes. Proc Natl Acad Sci USA 90: 3670-3674.
16. Dower, W.J., Miller, J.F., and Ragsdale, C.W. (1988) High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res 16: 6127-6145.
17. Fath, M.J., and Kolter, R. (1993) ABC transporters: bacterial exporters. Microbiol Rev 57: 995-1017.
18. Fleischmann, R.D., Adams, M.D., White, O., Clayton, R.A., Kirkness, E.F., Kerlavage, A.R., et al. (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269: 496-512.
19. Furste, J.P., Pansegrau, W., Frank, R., Blocker, H., Scholz, P., Bagdasarian, M., et al. (1986) Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector. Gene 48: 119-131.
20. Griffiths, G., McDowall, A., Back, R., and Dubochet, J. (1984) On the preparation of cryosections for immunochemistry. J Ultrastruct Res 89: 65-78.
21. Herriott, R.M., Meyer, E.M., and Vogt, M. (1970) Defined non-growth media for stage Il competence in Haemophilus influenzae. J Bacteriol 101: 517-524.
22. Higuchi, R. (1990) Recombinant PCR. In PCR Protocols: A Guide to Methods and Applications. Innis, M.A., Gelfand, D.H., Sninsky, J.J., and White, T.J. (eds). San Diego: Academic Press, pp. 177-183.
23. Hultgren, S.J., Abraham, S., Caparon, M., Falk, P., St. Geme, III, J.W., and Normark, S. (1993) Pilus and non-pilus bacterial adhesins: assembly and function in cell recognition. Cell 73: 887-901.
24. Hultgren, S.J., Jones, C.H., and Normark, S.N. (1996) Bacterial adhesins and their assembly. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt, F.C. (ed.). Washington, DC: American Society for Microbiology Press. pp. 2730-2756.
25. Hung, D.L., Knight, S.D., Woods, R.M., Pinkner, J.S., and Hultgren, S.J. (1996) Molecular basis of two subfamilies of immunoglobulin-like chaperones. EMBO J 15: 3792-3805.
26. Jacob-Dubuisson, F., Buisine, C., Willery, E., Renauld-Mongeniw, G., and Locht, C. (1997) Lack of functional complementation between Bordetella pertussis filamentous hemagglutinin and Proteus mirabilis HpmA nemolysin secretion machineries. J Bacteriol 179: 775-783.
27. Korangy, F., and Julin, D.A. (1992) Alteration by site-directed mutagenesis of the conserved lysine residue in the ATP-binding consensus sequence of the RecD subunit of the Escherichia coli RecBCD enzyme. J Biol Chem 267: 1727-1732.
28. Kuehn, M., Normark, S., and Hultgren, S.J. (1991) Immunoglobulin-like PapD chaperone caps and uncaps interactive surfaces of nascently translocated pilus subunits. Proc Natl Acad Sci USA 88: 10586-10590.
29. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
30. Lipinski, B., Zylicz, M., and Georgopoulos, C. (1990) The HtrA (DegP) protein, essential for Escherichia coli survival at high temperatures, is an endopeptidase. J Bacteriol 172: 1791-1797.
31. Malamy, M.H., and Horecker, B.L. (1964) Release of alkaline phosphatase from cells of Escherichia coli upon lysozyme spheroplast formation. Biochemistry 3: 1889-1893.
32. E, an Escherichia coli heat-inducible σ-factor, is modulated by expression of outer membrane proteins. Genes Dev 7: 2618-2628.
33. Mitchell, C., and Oliver, D. (1993) Two distinct ATP-binding domains are needed to promote protein export by Escherichia coli SecA ATPase. Mol Microbiol 10: 483-497.
34. Murphy, T.F., Bernstein, J.M., Dryja, D.M., Campagnari, A.A., and Apicella, M.A. (1987) Outer membrane protein and lipooligosaccharide analysis of paired nasopharyngeal and middle ear isolates in otitis media due to non typeable Haemophilus influenzae: pathogenic and epidemiologic observations. J Infect Dis 5: 723-731.
35. Nunn, D.N., and Lory, S. (1991) Product of the Pseudomonas aeruginosa gene PilD is a prepilin peptidase. Proc Natl Acad Sci USA 88: 3281-3285.
36. Osborn, M.J., Bander, J.E., Parisi, E., and Carson, J. (1972) Mechanism of assembly of the outer membrane of Salmonella typhimurium. Isolation and characterization of cytoplasmic and outer membrane. J Biol Chem 12: 3962-3972.
37. Palmer, K.L., and Munson, Jr, R.S. (1995) Cloning and characterization of the genes encoding the haemolysin of Haemophilus ducreyi. Mol Microbiol 18: 821-830.
38. Perez-Casal, J., Caparon, M.G., and Scott, J.R. (1991) Mry, a trans-acting positive regulator of the M protein gene of Streptococcus pyogenes with similarity to the receptor proteins of two-component regulatory systems. J Bacteriol 173: 2617-2624.
39. Poole, K., Schiebel, E., and Braun, V. (1988) Molecular characterization of the hemolysin determinant of Serratia marcescens. J Bacteriol 170: 3177-3188.
40. Possot, O.M., Letellier, L., and Pugsley, A.P. (1997) Energy requirement for pullulanase secretion by the main terminal branch of the general secretory pathway. Mol Microbiol 24: 457-464.
41. Pugsley, A.P. (1993) The complete general secretory pathway in Gram-negative bacteria. Microbiol Rev 57: 50-108.
42. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
43. Schatz, P.J., and Beckwith, J. (1990) Genetic analysis of protein export in Escherichia coli. Annu Rev Genet 24: 215-248.
44. Schiebel, E., Schwarz, H., and Braun, V. (1989) Subcellular location and unique secretion of the hemolysin of Serratia marcescens. J Biol Chem 264: 16311-16320.
45. Schonherr, R., Tsolis, R., Focareta, T., and Braun, V. (1993) Amino acid replacements in the Serratia marcescens hemolysin ShIA define sites involved in activation and secretion. Mol Microbiol 6: 1229-1237.
46. Slonim, L.N., Pinkner, J.S., Branden, C.-I., and Hultgren, S.J. (1992) Interactive surface in the PapD chaperone cleft is conserved in pilus chaperone superfamily and essential in subunit recognition and assembly. EMBO J 11: 4747-4756.
47. Slot, J.W., and Geuze, H.J. (1988) Localization of macromolecular components by application of the immunogold technique on cryosectioned bacteria. Methods Microbiol 20: 211-236.
48. Slot, J.W., Geuze, H.J., Gigengack, S., Lienhard, G.E., and James, D.E. (1991) Immuno-localization of the insulin regulatable glucose transporter (GLUT4) in brown adipose tissue of the rat. J Cell Biol 113: 123-135.
49. St Geme, III, J.W. (1993) Non typeable Haemophilus influenzae disease: epidemiology, pathogenesis, and prospects for prevention. Infect Agents Dis 2: 1-16.
50. St Geme, III, J.W. (1994) Early events in the pathogenesis of Haemophilus influenzae disease. In Molecular Genetics of Bacterial Pathogenesis. Miller, V.L., Kaper, J.B., Portnoy, D.A., and Isberg, R.R. (eds). Washington, DC: American Society for Microbiology Press.
51. St Geme, III, J.W., and Cutter, D. (1996) Influence of pili, fibrils, and capsule on in vitro adherence by Haemophilus influenzae type b. Mol Microbiol 21: 21-31.
52. St Geme, III, J.W., Falkow, S., and Barenkamp, S.J. (1993) High-molecular-weight proteins of non typable Haemophilus influenzae mediate attachment to human epithelial cells. Proc Natl Acad Sci USA 90: 2875-2879.
53. Strauch, K.L., Johnson, K., and Beckwith, J. (1989) Characterization of degP, a gene required for proteolysis in the cell envelope and essential for growth of Escherichia coli at high temperature. J Bacteriol 171: 2689-2696.
54. Studier, F.W., and Moffatt, B.A. (1986) Use of bacteriophage T7 RNA polymerase to direct high-level expression of cloned genes. J Mol Biol 189: 113-130.
55. Tabor, S., and Richardson, C.C. (1985) A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci USA. 82: 1074-1078.
56. Tokuyasu, K.T. (1980) Immunochemistry on ultrathin frozen sections. Histochem J 12: 381-403.
57. Turk, D.C. (1984) The pathogenicity of Haemophilus influenzae. J Med Microbiol 18: 1-16.
58. Turner, L.R., Lara, J.C., Nunn, D.N., and Lory, S. (1993) Mutations in the consensus ATP-binding sites of XcpR and PilB eliminate extracellular protein secretion and pilus biogenesis in Pseudomonas aeruginosa. J Bacteriol 175: 4962-4969.
59. Uphoff, T.S., and Welch, R.A. (1990) Nucleotide sequencing of the Proteus mirabilis calcium-independent hemolysin genes (hpmA and hpmB) reveals sequence similarity with the Serratia marcescens hemolysin genes (shlA and shlB). J Bacteriol 172: 1206-1216.
60. Walker, J.E., Saraste, M., Runswick, M.J., and Gay, N.J. (1982) Distantly related sequences in the alpha and beta subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1: 945-951.
61. Watson, W.J., Gilsdorf, J.R., Tucci, M.A., McCrea, K.W., Forney, L.J., and Marrs, C.F. (1994) Identification of a gene essential for piliation in Haemophilus influenzae type b with homology to the pilus assembly platform genes of Gram-negative bacteria. Infect Immun 62: 468-475.
62. Welch, R.A., Hull, R., and Falkow, S. (1983) Molecular cloning and physical characterization of a chromosomal hemolysin from Escherichia coli. Infect Immun 42: 178-186.
63. Willems, R.J.L., Geuijen, C., van der Heide, H.G.J., Renauld, G., Bertin, P., van den Akker, W.M.R., et al. (1994) Mutational analysis of the Bordetella pertussis fim/fha gene cluster: identification of a gene with sequence similarities to haemolysin accessory genes involved in export of FHA. Mol Microbiol 11: 337-347.