Two-component systems in Haemophilus influenzae: A regulatory role for arcA in serum resistance

Infection and Immunity

Volumn 71, Issue 1, 2003, Pages 163-172

  De Souza Hart, J A ^a,b   Blackstock, W ^c,f   Di Modugno, V ^d   Holland, I B ^a   Kok, M ^b,e  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^c GLAXOSMITHKLINE   (United Kingdom)

^d GSK   (Italy)

^e ERASMUS MEDICAL CENTER   (Netherlands)

^f Cellzome AG   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEOME;

ANTIBODY TITER; ARCA GENE; ARTICLE; BACTERIAL CELL WALL; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERICIDAL ACTIVITY; BLOOD; CELL SURVIVAL; COMPLEMENT ACTIVATION; ESCHERICHIA COLI; GENE; HAEMOPHILUS INFLUENZAE TYPE B; HUMAN; INFECTION; MUTATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SERUM; SYNTHESIS; VIRULENCE;

ANIMALS; BACTERIAL CAPSULES; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BLOOD BACTERICIDAL ACTIVITY; CELL LINE; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HAEMOPHILUS INFECTIONS; HAEMOPHILUS INFLUENZAE TYPE B; HUMANS; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED BALB C; MUTATION; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; VIRULENCE;

EID: 0037222910     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.1.163-172.2003     Document Type: Article

References (61)

1. Appel, R. D., P. M. Palagi, D. Walther, J. R. Vargas, J.-C. Sanchez, F. Ravier, C. Pasquali, and D. F. Hochstrasser. 1997. Melanie II - A third-generation software package for analysis of two-dimensional electrophoresis images. I. Features and user interface. Electrophoresis 18:2724-2734.
2. Bajaj, V., R. L. Lucas, C. Hwang, and C. A. Lee. 1996. Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol. Microbiol. 22:703-714.
3. Barcak, G. J., M. S. Chandler, R. J. Redfield, and J.-F. Tomb. 1991. Genetic systems in Haemophilus influenzae, Methods Enzymol. 204:321-342.
4. Barra, A., R. Dagan, J. L. Preud'homme, A. Bajart, B. Danve, and B. Fritzell. 1993. Characterization of the serum antibody response induced by Haemophilus influenzae type b tetanus protein-conjugate vaccine in infants receiving a DTP-combined vaccine from 2 months of age. Vaccine 11:1003-1006.
5. Bernardini, M. L., A. Fontaine, and P. J. Sansonetti. 1990. The two-component regulatory system OmpR-EnvZ controls the virulence of Shigella flexneri. J. Bacteriol. 172:6274-6281.
6. Boyd, R. F., and B. G. Hoerl. 1986. Acquired immunity: Components and functions of the immune system, p. 335-372. In Basic Medical Microbiology, 3rd Ed. Little, Brown and Company, Boston, Mass.
7. Brodeur, B. R., P. S. Tsang, J. Hamel, Y. Larose, and S. Montplaisir. 1986. Mouse models of infection for Neisseria meningitidis B, 2b and Haemophilus influenzae type b diseases. Can. J. Microbiol 32:33-37.
8. Buckmire, F. L. A. 1982. Characterization of the capsular antigen isolated from Haemophilus influenzae type b and two spontaneous non-encapsulated mutants, p. 171-183. In S. H. Sell and P. F. Wright (ed.), Haemophilus Influenzae: Epidemiology, Immunology and Prevention of Disease. Elsevier Science Publishing Co., New York, N.Y.
9. Chambers, S. P., S. E. Prior, D. A. Barstow, and N. P. Minton. 1988. The pMTL nic-cloning vectors. I. Improved pUC polylinker regions to facilitate the use of sonicated DNA for nucleotide sequencing. Gene 68:139-149.
10. Coligan, J. E., A. M. Kruisbeek, D. H. Margulies, and W. Strober (ed.). 1994. Current Protocols in Immunology, p. 13.1.1-13.1.19. John Wiley & Sons, Inc., New York, N.Y.
11. Compan, I., and D. Touati. 1994. Anaerobic activation of arcA transcription in Escherichia coli: Roles of Fnr and ArcA. Mol. Microbiol. 11:955-964.
12. Dankert, J. R. 1991. Resistance of Escherichia coli to osmotically introduced complement component 9. Infect. Immun. 59:109-113.
13. Davison, J., M. Heusterspreute, N. Chevalier, V. Ha-Thi, and F. Brunel. 1987.Vectors with restriction site banks. V. pJRD215, a wide-host-range cosmid vector with multiple cloning sites. Gene 51:275-280.
14. D'Mello, R. A., P. R. Langford, and J. S. Kroll. 1997. Role of bacterial Mn-cofactored superoxide dismutase in oxidative stress responses, nasopharyngeal colonization, and sustained bacteremia caused by Haemophilus influenzae type b. Infect. Immun. 65:2700-2706.
15. Elsbach, P. 1998. The bactericidal/permeability-increasing protein (BPI) in antibacterial host defense. J. Leukoc. Biol. 64:14-18.
16. Finney, D. J. 1952. Probit Analysis, A Statistical Treatment of the Sigmoid Response Curve, 2nd Ed. Cambridge University Press, London, United Kingdom.
17. Fleischmann, R. D., M. D. Adams, O. White, R. A. Clayton, E. F. Kirkness, A. R. Kerlavage, C. J. Bult, J.-F. Tomb, et al. 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496-512.
18. Garcia Vescovi, E., F. C. Soncini, and E. A. Groisman. 1994. The role of the PhoP/PhoQ regulon in Salmonella virulence. Res. Microbiol. 145:473-480.
19. Gennis, R. B., and V. Stewart. 1996. Respiration, p. 217-261. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia Coli and Salmonella: Cellular and Molecular Biology, 2nd ed. ASM Press, Washington, D.C.
20. Gilsdorf, J. R., M. Tucci, L. J. Forney, W. Watson, C. F. Marrs, and E. J. Hansen. 1993. Paradoxical effect of pilus expression on binding of antibodies by Haemophilus influenzae. Infect. Immun. 61:3375-3381.
21. Gold, R. 1999. Epidemiology of bacterial meningitis. Infect. Dis. Clin. North. Am. 13:515-525.
22. Gorg, A., C. Obermaier, G. Boguth, and W. Weiss. 1999. Recent developments in two-dimensional gel electrophoresis with immobilized pH gradients: Wide pH gradients up to pH 12, longer separation distances and simplified procedures. Electrophoresis 20:712-717.
23. Green, B. A., J. E. Farley, T. Quinn-Dey, R. A. Deich, and G. W. Zlotnick. 1991. The e(P4) outer membrane protein of Haemophilus influenzae: Biologic activity of anti-e serum and cloning and sequencing of the structural gene. Infect. Immun. 59:3191-3198.
24. Guerina, N. G., S. Langermann, G. K. Schoolnik, T. W. Kessler, and D. A. Goldmann. 1985. Purification and characterization of Haemophilus influenzae pili, and their structural and serological relatedness to Escherichia coli P and mannose-sensitive pili. J. Exp. Med. 161:145-159.
25. Gunsalus, R. P., and S. J. Park. 1994. Aerobic-anaerobic gene regulation in Escherichia coli: Control by the ArcAB and Fnr regulons. Res. Microbiol. 145:437-450.
26. Gwinn, M. L., D. Yi, H. O. Smith, and J.-F. Tomb. 1996. Role of the two-component signal transduction and the phosphoenolpyruvate: Carbohydrate phosphotransferase systems in competence development of Haemophilus influenzae Rd. J. Bacteriol. 178:6366-6368.
27. Jarosik, G. P., J. D. Sanders, L. D. Cope, U. Muller-Eberhard, and E. J. Hansen. 1994. A functional tonB gene is required for both utilization of heme and virulence expression by Haemophilus influenzae type b. Infect. Immun 62:2470-2477.
28. Herbert, B. 1999. Advances in protein solubilization for two-dimensional electrophoresis. Electrophoresis 20:660-663.
29. Hetherington, S. V., C. C. Patrick, and E. J. Hansen. 1993. Outer membrane protein binding sites of complement component 3 during opsonization of Haemophilus influenzae. Infect. Immun. 61:5157-5163.
30. Hetherington, S. V., and M. L. Lepow. 1992. Correlation between antibody affinity and serum bactericidal activity in infants. J. Infect. Dis. 165:753-756.
31. Hitchcock, P. J., and T. M. Brown. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J. Bacteriol. 154:269-277.
32. Hochstrasser, D. F., M. G. Harrington, A.-C. Hochstrasser, M. J. Miller, and C. R. Merril. 1988. Methods for increasing the resolution of two-dimensional protein electrophoresis. Anal. Biochem. 173:424-435.
33. Iovine, N. M., P. Elsbach, and J. Weiss. 1997. An opsonic function of the neutrophil bactericidal/permeability-increasing protein depends on both its N- and C-terminal domains. Proc. Natl. Acad. Sci. USA 94:10973-10978.
34. Iuchi, S., and E. C. C. Lin. 1993. Adaptation of Escherichia coli to redox environments by gene expression. Mol. Microbiol. 9:9-15.
35. Kroll, H. P., S. Bhakdi, and P. W. Taylor. 1983. Membrane changes induced by exposure of Escherichia coli to human serum. Infect. Immun. 42:1055-1066.
36. Kroll, J. S. 1992. The genetics of encapsulation in Haemophilus influenzae. J. Infect. Dis. 165(Suppl. 1):S93-S96.
37. Kroll, J. S., and E. R. Moxon. 1988. Capsulation and gene copy number at the cap locus of Haemophilus influenzae type b. J. Bacteriol. 170:859-864.
38. Leclerc, G. J., C. Tartera, and E. S. Metcalf. 1998. Environmental regulation of Salmonella typhi invasion-defective mutants. Infect. Immun. 66:682-691.
39. Lynch, A. S., and E. C. C. Lin. 1996. Responses to molecular oxygen, p. 1526-1535. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia Coli and Salmonella: Cellular and Molecular Biology, 2nd Ed. ASM Press, Washington, D.C.
40. Mellies, J., T. Rudel, and T. F. Meyer. 1997. Transcriptional regulation of pilC2 in Neisseria gonorrhoeae: Response to oxygen availability and evidence for growth-phase regulation in Escherichia coli. Mol. Gen. Genet. 255:285-293.
41. Miyazaki, S., T. Matsumoto, N. Furuya, K. Tateda, and K. Yamaguchi. 1999. The pathogenic role of fimbriae of Haemophilus influenzae type b in murine bacteraemia and meningitis. J. Med. Microbiol. 48:383-388.
42. Moxon, E. R. 1992. Molecular basis of invasive Haemophilus influenzae type b disease. J. Infect. Dis. 165(Suppl. 1):S77-S81.
43. Munson, R., Jr., B. Brodeur, P. Chong, S. Grass, D. Martin, and C. Proulx. 1992. Outer membrane proteins P1 and P2 of Haemophilus influenzae type b: Structure and identification of surface-exposed epitopes. J. Infect. Dis. 165(Suppl. 1):S86-S89.
44. Munson, R. S., Jr., and D. M. Granoff. 1985. Purification and partial characterization of outer membrane proteins P5 and P6 from Haemophilus influenzae type b. Infect. Immun. 49:544-549.
45. Noel, G. J., D. Bauer, and P. J. Edelson. 1992. The role of complement and murine monoclonal antibodies in binding and ingestion of Haemophilus influenzae type b by murine macrophages. J. Infect. Dis. 165(Suppl. 1):S74-S75.
46. Noel, G. J., D. M. Mosser, and P. J. Edelson. 1990. Role of complement in mouse macrophage binding of Haemophilus influenzae type b. J. Clin. Investig. 85:208-218.
47. O'Farrell, P. H. 1975. High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250:4007-4021.
48. Qi, S. Y., Y. Li, A. Szyroki, I. G. Giles, A. Moir, and C. D. O'Connor. 1995. Salmonella typhimurium responses to a bactericidal protein from human neutrophils. Mol. Microbiol. 17:523-531.
49. Santoni, V., T. Rabilloud, P. Doumas, D. Rouquie, M. Mansion, S. Kieffer, J. Garin, and M. Rossignol. 1999. Towards the recovery of hydrophobic proteins on two-dimensional electrophoresis gels. Electrophoresis 20:705-711.
50. Schrieber, J. R., C. J. Basker, and G. R. Siber. 1987. Effect of complement depletion on anticapsular-antibody-mediated immunity to experimental infection with Haemophilus influenzae type b. Infect. Immun. 55:2830-2833.
51. Shann, F. 1999. Haemophilus influenzae pneumonia: Type b or non-type b? Lancet 354:1488-1490.
52. Shevchenko, A., M. Wilm, O. Vorm, and M. Mann. 1996. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68:850-858.
53. Skorupski, K., and R. K. Taylor. 1997. Control of the ToxR virulence regulon in Vibrio cholerae by environmental stimuli. Mol. Microbiol. 25:1003-1009.
54. Tatusov, R. L., A. R. Mushegian, P. Bork, N. P. Brown, W. S. Hayes, M. Borodovsky, K. E. Rudd, and E. V. Koonin. 1996. Metabolism and evolution of Haemophilus influenzae deduced from a whole-genome comparison with Escherichia coli. Curr. Biol. 6:279-291.
55. Taylor, P. W. 1992. Complement-mediated killing of susceptible Gramnegative bacteria: An elusive mechanism. Exp. Clin. Immunogenet. 9:48-56.
56. Tosi, M. F., D. C. Anderson, J. Barrish, E. O. Mason, Jr., and S. L. Kaplan. 1985. Effect of piliation on interactions of H. influenzae type b with human polymorphonuclear leukocytes. Infect. Immun. 47:780-785.
57. Weiser, J. N. 1993. Relationship between colony morphology and the life cycle of Haemophilus influenzae: The contribution of lipopolysaccharide phase variation to pathogenesis. J. Infect. Dis. 168:672-680.
58. Wilm, M., A. Shevchenko, T. Houthaeve, S. Breit, L. Schweigerer, T. Fotsis, and M. Mann. 1996. Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 379:466-469.
59. Witholt, B., M. Boekhout, M. Brock, J. Kingma, H. V. Heerikhuizen, and L. D. Leij. 1976. An efficient and reproducible procedure for the formation of spheroplasts from variously grown Escherichia coli. Anal. Biochem. 74:160-170.
60. Yi, K., and T. F. Murphy. 1997. Importance of an immunodominant surface-exposed loop on outer membrane protein P2 of nontypeable Haemophilus influenzae. Infect. Immun. 65:150-155.
61. Zwahlen, A., J. S. Kroll, L. G. Rubin, and E. R. Moxon. 1989. The molecular basis of pathogenicity in Haemophilus influenzae: Comparative virulence of genetically related capsular transformants and correlation with changes at the capsulation locus cap. Microb. Pathog. 7:225-235.