Immunization with the Haemophilus ducreyi hemoglobin receptor HgbA protects against infection in the swine model of chancroid

Infection and Immunity

Volumn 74, Issue 4, 2006, Pages 2224-2232

  Afonina, Galyna ^a   Leduc, Isabelle ^a   Nepluev, Igor ^a   Jeter, Chrystina ^a   Routh, Patty ^b   Almond, Glen ^b   Orndorff, Paul E ^b   Hobbs, Marcia ^a   Elkins, Christopher ^a  

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

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIUM ANTIBODY; HAEMOPHILUS VACCINE; HEME; HEMOGLOBIN; HEMOGLOBIN RECEPTOR; HGBA PROTEIN; IMMUNOGLOBULIN G; IRON; PROTEIN SUBUNIT; RECEPTOR; TDHA PROTEIN; TONB PROTEIN; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ANTIGEN BINDING; ARTICLE; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; BACTERIUM MUTANT; CONTROLLED STUDY; HAEMOPHILUS DUCREYI; HAEMOPHILUS DUCREYI 35000HP; HAEMOPHILUS DUCREYI CIP542; IMMUNITY; IMMUNIZATION; IRON DEPLETION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BLOCKING; SWINE; ULCUS MOLLE;

ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL PROTEINS; BINDING SITES, ANTIBODY; CARRIER PROTEINS; CHANCROID; DISEASE MODELS, ANIMAL; HAEMOPHILUS DUCREYI; HAEMOPHILUS VACCINES; HEMOGLOBINS; IMMUNOGLOBULIN G; PROTEIN BINDING; SWINE;

EID: 33645530403     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.74.4.2224-2232.2006     Document Type: Article

References (67)

1. Abdullah, M., I. Nepluev, G. Afonina, S. Ram, P. Rice, W. Cade, and C. Elkins. 2005. Killing of dsrA mutants of Haemophilus ducreyi by normal human serum occurs via the classical complement pathway and is initiated by immunoglobulin M binding. Infect. Immun. 73:3431-3439.
2. Ahmed, H. J., A. Frisk, J. E. Mansson, E. K. Schweda, and T. Lagergard. 1997. Structurally defined epitopes of Haemophilus ducreyi lipooligosaccharides recognized by monoclonal antibodies. Infect. Immun. 65:3151-3158.
3. Al-Tawfiq, J. A., K. R. Fortney, B. P. Katz, A. F. Hood, C. Elkins, and S. M. Spinola. 2000. An isogenic hemoglobin receptor-deficient mutant of Haemophilus ducreyi is attenuated in the human model of experimental infection. J. Infect. Dis. 181:1049-1054.
4. Bauer, B. A., M. K. Stevens, and E. J. Hansen. 1998. Involvement of the Haemophilus ducreyi gmhA gene product in lipooligosaccharide expression and virulence. Infect. Immun. 66:4290-4298.
5. Bauer, M. E., M. P. Goheen, C. A. Townsend, and S. M. Spinola. 2001. Haemophilus ducreyi associates with phagocytes, collagen, and fibrin and remains extracellular throughout infection of human volunteers. Infect. Immun. 69:2549-2557.
6. Bauer, M. E., and S. M. Spinola. 2000. Localization of Haemophilus ducreyi at the pustular stage of disease in the human model of infection. Infect. Immun. 68:2309-2314.
7. Behets, F. M., A. R. Brathwaite, T. Hylton-Kong, C. Y. Chen, I. Hoffman, J. B. Weiss, S. A. Morse, G. Dallabetta, M. S. Cohen, and J. P. Figueroa. 1999. Genital ulcers: etiology, clinical diagnosis, and associated human immunodeficiency virus infection in Kingston, Jamaica. Clin. Infect. Dis. 28:1086-1090.
8. Bong, C. T., M. E. Bauer, and S. M. Spinola. 2002. Haemophilus ducreyi: clinical features, epidemiology, and prospects for disease control. Microbes Infect. 4:1141-1148.
9. Caulfield, M. J., and D. Shaffer. 1984. A computer program for the evaluation of ELISA data obtained using an automated microtiter plate absorbance reader. J. Immunol. Methods 74:205-215.
10. Chen, C. Y., R. C. Ballard, C. M. Beck-Sague, Y. Dangor, F. Radebe, S. Schmid, J. B. Weiss, V. Tshabalala, G. Fehler, Y. Htun, and S. A. Morse. 2000. Human immunodeficiency virus infection and genital ulcer disease in South Africa: the herpetic connection. Sex. Transm. Dis. 27:21-29.
11. Chen, C. Y., K. J. Mertz, S. M. Spinola, and S. A. Morse. 1997. Comparison of enzyme immunoassays for antibodies to Haemophilus ducreyi in a community outbreak of chancroid in the United States. J. Infect. Dis. 175:1390-1395.
12. Cohen, M. 1998. Sexually transmitted diseases enhance HIV transmission: no longer a hypothesis. Lancet 351:5-7.
13. Cole, L. E., T. H. Kawula, K. L. Toffer, and C. Elkins. 2002. The Haemophilus ducreyi serum resistance antigen DsrA confers attachment to human keratinocyte. Infect. Immun. 70:6158-6165.
14. Cole, L. E., K. L. Toffer, R. A. Fulcher, L. R. San Mateo, P. E. Orndorff, and T. H. Kawula. 2003. A humoral immune response confers protection against Haemopliilus ducreyi infection. Infect. Immun. 71:6971-6977.
15. Desjardins, M., L. G. Filion, S. Robertson, and D. W. Cameron. 1995. Inducible immunity with a pilus preparation booster vaccination in an animal model of Haemophilus ducreyi infection and disease. Infect. Immun. 63:2012-2020.
16. Desjardins, M., L. G. Filion, S. Robertson, L. Kobylinski, and D. W. Cameron. 1996. Evaluation of humoral and cell-mediated inducible immunity to Haemophilus ducreyi in an animal model of chancroid. Infect. Immun. 64:1778-1788.
17. Dickerson, M. C., J. Johnston, T. E. Delca, A. White, and E. Andrews. 1996. The causal role for genital ulcer disease as a risk factor for transmission of human immunodeficiency virus. An application of the Bradford Hill criteria. Sex. Transm. Dis. 23:429-440.
18. Dutro, S. M., G. Wood, and P. Totten. 1999. Prevalence of, antibody response to, and immunity induced by Haemophilus ducreyi hemolysin. Infect. Immun. 67:3317-3328.
19. Elkins, C. 1995. Identification and purification of a conserved heme-regulated hemoglobin-binding outer membrane protein from Haemophilus ducreyi. Infect. Immun. 63:1241-1245.
20. Elkins, C., N. H. Carbonetti, V. A. Varela, D. Stirewalt, D. G. Klapper, and P. F. Sparling. 1992. Antibodies to N-terminal peptides of gonococcal porin are bactericidal when gonococcal lipopolysaccharide is not sialylated. Mol. Microbiol. 5:2617-2628.
21. Elkins, C., C. J. Chen, and C. E. Thomas. 1995. Characterization of the hgbA locus of Haemophilus ducreyi. Infect. Immun. 63:2194-2200.
22. Elkins, C., K. J. Morrow, Jr., and B. Olsen. 2000. Serum resistance in Haemophilus ducreyi requires outer membrane protein DsrA. Infect. Immun. 68:1608-1619.
23. Elkins, C., P. A. Totten, B. Olsen, and C. E. Thomas. 1998. Role of the Haemophilus ducreyi Ton system in internalization of heme from hemoglobin. Infect. Immun. 66:151-160.
24. Elkins, C., K. Yi, B. Olsen, C. Thomas, K. Thomas, and S. Morse. 2000. Development of a serological test for Haemophihis ducreyi for seroprevalence studies. J. Clin. Microbiol. 38:1520-1526.
25. Frisk, A., H. J. Ahmed, E. Van Dyck, and T. Lagergard. 1998. Antibodies specific to surface antigens are not effective in complement-mediated killing of Haemophilus ducreyi. Microb. Pathog. 25:67-75.
26. Frisk, A., E. L. Roggen, and T. Lagergard. 1995. Localisation and immunological properties of a 24-kDa surface protein of Haemophilus ducreyi. J. Med. Microbiol. 43:192-200.
27. Gelfanova, V., T. L. Humphreys, and S. M. Spinola. 2001. Characterization of Haemophilus ducreyi-specific T-cell lines from lesions of experimentally infected human subjects. Infect. Immun. 69:4224-4231.
28. Gray, R. H., M. J. Wawer, N. K. Sewankambo, D. Serwadda, C. Li, L. H. Moulton, T. Lutalo, F. Wabwire-Mangen, M. P. Meehan, S. Ahmed, L. A. Paxton, N. Kiwanuka, F. Nalugoda, E. L. Korenromp, T. C. Quinn, et al. 1999. Relative risks and population attributable fraction of incident HIV associated with symptoms of sexually transmitted diseases and treatable symptomatic sexually transmitted diseases in Rakai District, Uganda. AIDS 13:2113-2123.
29. Hansen, E. J., S. R. Lumbley, J. A. Richardson, B. K. Purcell, M. K. Stevens, L. D. Cope, J. Datte, and J. D. Radolf. 1994. Induction of protective immunity to Haemophilus ducreyi in the temperature-dependent rabbit model of experimental chancroid. J. Immunol. 152:184-192.
30. Hayes, R., K. Schulz, and F. Plummer. 1995. The cofactor effect of genital ulcers on the per-exposure risk of HIV transmission in sub-Saharan Africa. J. Trop. Med. Hyg. 98:1-8.
31. Hobbs, M. M., L. R. S. Mateo, P. E. Orndorff, G. Almond, and T. H. Kawula. 1995. Swine model of Haemophilus ducreyi infection. Infect. Immun. 63:3094-3100.
32. Janeway, C. A., Jr. 2001. How the immune system protects the host from infection. Microbes Infect. 3:1167-1171.
33. Lagergard, T. 1995. Haemophilus ducreyi: pathogenesis and protective immunity. Trends Microbiol. 3:87-92.
34. Lagergard, T. 1992. The role of Haemophilus ducreyi bacteria, cytotoxin, endotoxin and antibodies in animal models for study of chancroid. Microb. Pathog. 13:203-217.
35. Lagergard, T., A. Frisk, M. Purven, and L. A. Nilsson. 1995. Serum bactericidal activity and phagocytosis in host defence against Haemophilus ducreyi. Microb. Pathog. 18:37-51.
36. Leduc, I. 2001. Strain typing and vaccine development for chancroid. Ph.D. thesis. University of Ottawa, Ottawa, Canada.
37. Mateo, L. R. S., K. L. Toffer, P. E. Orndorff, and T. H. Kawula. 1999. Immune cells are required for cutaneous ulceration in a swine model of chancroid. Infect. Immun. 67:4963-4967.
38. Morse, S. A. 1989. Chancroid and Haemophilus ducreyi. Clin. Microbiol. Rev. 2:137-157.
39. O'Farrell, N. 2002. Genital ulcers, stigma, HIV, and STI control in sub-Saharan Africa. Sex. Transm. Infect. 78:143-146.
40. O'Farrell, N. 2001. Sector-wide approaches and STI control in Africa. Sex. Transm. Infect. 77:156-157.
41. O'Farrell, N. 2001. Targeted interventions required against genital ulcers in African countries worst affected by HIV infection. Bull. W. H. O. 79:569-577.
42. O'Farrell, N., A. A. Hoosen, K. D. Coetzee, and J. van den Ende. 1991. Genital ulcer disease in men in Durban, South Africa. Genitourin. Med. 67:327-330.
43. Otto, B. R., A. M. Verweij-van Vught, and D. M. MacLaren. 1992. Transferrins and heme-compounds as iron sources for pathogenic bacteria. Crit. Rev. Microbiol. 18:217-233.
44. Patterson, K., B. Olsen, C. Thomas, D. Norn, M. Tam, and C. Elkins. 2002. Development of a rapid immunodiagnostic field test for Haemophilus ducreyi. J. Clin. Microbiol. 40:3694-3702.
45. Pepin, J., D. Dunn, I. Gaye, P. Alonso, A. Egboga, R. Tedder, P. Piot, N. Berry, D. Schellenberg, H. Whittle, et al. 1991. HIV-2 infection among prostitutes working in The Gambia: association with serological evidence of genital ulcer diseases and with generalized lymphadcnopathy. AIDS 5:69-75.
46. Perkins-Balding, D., M. Ratliff-Griffin, and I. Stojiljkovic. 2004. Iron transport systems in Neisseria meningitidis. Microbiol. Mol. Biol. Rev. 68:154-171.
47. Playfair, J. H. L. 2004. Infection and immunity, 2nd ed. Oxford University Press, Oxford, England.
48. Plummer, F. A., J. N. Simonsen, D. W. Cameron, J. O. Ndinya-Achola, J. K. Kreiss, M. N. Gakinya, P. Waiyaki, M. Cheang, P. Piot, A. R. Ronald, and E. N. Ngugi. 1991. Cofactors in male-female sexual transmission of human immunodeficiency virus type 1. J. Infect. Dis. 163:233-239.
49. Purcell, B. K., J. A. Richardson, J. D. Radolf, and E. J. Hansen. 1991. A temperature-dependent rabbit model for production of dermal lesions by Haemophilus ducreyi. J. Infect. Dis. 164:359-367.
50. Rauschkolb, J. E. 1939. Circumcision in treatment of chancroidal lesions of male genitalia. Arch. Dermatol. Syphilol. 39:319.
51. Robinson, N. J., D. W. Mulder, B. Auvert, and R. J. Hayes. 1997. Proportion of HIV infections attributable to other sexually transmitted diseases in a rural Ugandan population: simulation model estimates. Int. J. Epidemiol. 26:180-189.
52. Ronald, A., and W. Albritton. 1999. Chancroid and Haemophilus ducreyi, p. 515-524. In K. K. Holmes, P. F. Sparling, P.-A. Mardh, S. Lemon, W. Stamm, P. Piot, and J. N. Wasserheit (ed.), Sexually transmitted diseases, 3rd ed. McGraw Hill, New York, N.Y.
53. Sachs, D. H. 1994. The pig as a potential xenograft donor. Vet. Immunol. Immunopathol. 43:185-191.
54. San Mateo, L. R., K. L. Toffer, P. E. Orndorff, and T. H. Kawula. 1999. Neutropenia restores virulence to an attenuated Cu,Zn superoxide dismutase-deficient Haemophilus ducreyi strain in the swine model of chancroid. Infect. Immun. 67:5345-5351.
55. Schneider, H., and J. M. Griffiss. 1982. A bactericidal microassay for testing serum sensitivity of Neisseria gonorrhoeae. J. Immunol. Methods 54:101-105.
56. Sparling, P. F. 1998. Iron and infection. Clin. Infect. Dis. 27:1367-1368.
57. Spinola, S. M., M. E. Bauer, and R. S. Munson. 2002. Immunopathogenesis of Haemophilus ducreyi infection (chancroid). Infect. Immun. 70:1667-1676.
58. Spinola, S. M., A. Orazi, J. N. Arno, K. Fortney, P. Kotylo, C. Y. Chen, A. A. Campagnari, and A. F. Hood. 1996. Haemophilus ducreyi elicits a cutaneous infiltrate of CD4 cells during experimental human infection. J. Infect. Dis. 173:394-402.
59. Spinola, S. M., L. M. Wild, M. A. Apicella, A. A. Gaspari, and A. A. Campagnari. 1994. Experimental human infection with Haemophilus ducreyi. J. Infect. Dis. 169:1146-1150.
60. Steen, R., B. Vuylsteke, T. DeCoito, S. Ralepeli, G. Fehler, J. Conley, L. Bruckers, G. Dallabetta, and R. Ballard. 2000. Evidence of declining STD prevalence in a South African mining community following a core-group intervention. Sex. Transm. Dis. 27:1-8.
61. Stevens, M. K., S. Porcella, J. Klesney-Tait, S. Lumbley, S. E. Thomas, M. V. Norgard, J. D. Radolf, and E. J. Hansen. 1996. A hemoglobin-binding outer membrane protein is involved in virulence expression by Haemophilus ducreyi in an animal model. Infect. Immun. 64:1724-1735.
62. Stojiljkovic, I., and D. Perkins-Balding. 2002. Processing of heme and heme-containing proteins by bacteria. DNA Cell Biol. 21:281-295.
63. Thomas, C. E., B. Olsen, and C. Elkins. 1998. Cloning and characterization of tdhA, a locus encoding a TonB-dependcnt heme receptor from Haemophilus ducreyi. Infect. Immun. 66:4254-4262.
64. Thomas, K. L., I. Leduc, B. Olsen, C. E. Thomas, D. W. Cameron, and C. Elkins. 2001. Cloning, overexpression, purification, and immunobiology of an 85-kilodalton outer membrane protein from Haemophilus ducreyi. Infect. Immun. 69:4438-4446.
65. Totten, P. A., D. V. Norn, and W. E. Stamm. 1995. Characterization of the hemolytic activity of Haemophilus ducreyi. Infect. Immun. 63:4409-4416.
66. White, C. D., I. Leduc, B. Olsen, C. Jeter, C. Harris, and C. Elkins. 2005. Haemophilus ducreyi outer membrane determinants, including DsrA, define two clonal populations. Infect. Immun. 73:2387-2399.
67. World Health Organization. 1995. Sexually transmitted diseases: three hundred and thirty-three million new, curable cases in 1995. AIDS Wkly. 1995(Sept. 18):15-16.