Single dose novel salmonella vaccine enhances resistance against visceralizing L. major and L. donovani infection in susceptible BALB/c mice

PLoS Neglected Tropical Diseases

Volumn 5, Issue 12, 2011, Pages

  Schroeder, Juliane ^a   Brown, Najmeeyah ^b   Kaye, Paul ^b   Aebischer, Toni ^a,c  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

^c ROBERT KOCH INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

SALMONELLOSIS VACCINE; DRUG CARRIER; LEISHMANIA VACCINE; PARASITE ANTIGEN; RECOMBINANT VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; BAGG ALBINO MOUSE; CONTROLLED STUDY; DOSE RESPONSE; FEMALE; HUMORAL IMMUNITY; INFECTION PREVENTION; INFECTION RESISTANCE; LEISHMANIA DONOVANI; LEISHMANIA MAJOR; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; SALMONELLA TYPHIMURIUM; SINGLE DRUG DOSE; VISCERAL LEISHMANIASIS; ANIMAL; DISEASE MODEL; GENE VECTOR; GENETICS; IMMUNOLOGY; PARASITOLOGY;

ANIMALS; ANTIGENS, PROTOZOAN; DISEASE MODELS, ANIMAL; DRUG CARRIERS; FEMALE; GENETIC VECTORS; LEISHMANIA DONOVANI; LEISHMANIA MAJOR; LEISHMANIASIS VACCINES; LEISHMANIASIS, VISCERAL; MICE; MICE, INBRED BALB C; SALMONELLA TYPHIMURIUM; VACCINES, SYNTHETIC;

EID: 84855256646     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001406     Document Type: Article

References (73)

1. Herwaldt BL, (1999) Leishmaniasis. Lancet 354: 1191-1199.
2. Chappuis F, Sundar S, Hailu A, Ghalib H, Rijal S, et al. (2007) Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat Rev Microbiol 5: 873-882.
3. Polonio T, Efferth T, (2008) Leishmaniasis: drug resistance and natural products. Int J Mol Med 22: 277-286.
4. Lira R, Sundar S, Makharia A, Kenney R, Gam A, et al. (1999) Evidence that the high incidence of treatment failures in Indian kala-azar is due to the emergence of antimony-resistant strains of Leishmania donovani. J Infect Dis 180: 564-567.
5. Meheus F, Balasegaram M, Olliaro P, Sundar S, Rijal S, et al. (2010) Cost-Effectiveness analysis of combination therapies for visceral leishmaniasis in the Indian subcontinent. PLoS Negl Trop Dis 4 (9): e818.
6. Olliaro PL, Guerin PJ, Gerstl S, Haaskjold AA, Rottingen JA, et al. (2005) Treatment options for visceral leishmaniasis: a systematic review of clinical studies done in India, 1980-2004. Lancet Infect Dis 5: 763-774.
7. Nadim A, Javadian E, Tahvildar-Bidruni G, Ghorbani M, (1983) Effectiveness of leishmanization in the control of cutaneous leishmaniasis. Bull Soc Pathol Exot Filiales 76: 377-383.
8. Khamesipour A, Rafati S, Davoudi N, Maboudi F, Modabber F, (2006) Leishmaniasis vaccine candidates for development: a global overview. Indian J Med Res 123: 423-438.
9. Khamesipour A, Dowlati Y, Asilian A, Hashemi-Fesharki R, Javadi A, et al. (2005) Leishmanization: use of an old method for evaluation of candidate vaccines against leishmaniasis. Vaccine 23: 3642-3648.
10. Hosseini SM, Hatam GR, Ardehali S, (2005) Characterization of Leishmania isolated from unhealed lesions caused by leishmanization. East Mediterr Health J 11: 240-243.
11. Noazin S, Khamesipour A, Moulton LH, Tanner M, Nasseri K, et al. (2009) Efficacy of killed whole-parasite vaccines in the prevention of leishmaniasis: a meta-analysis. Vaccine 27: 4747-4753.
12. Kedzierski L, (2010) Leishmaniasis Vaccine: Where are We Today? J Glob Infect Dis 2: 177-185.
13. Okwor I, Uzonna J, (2009) Vaccines and vaccination strategies against human cutaneous leishmaniasis. Hum Vaccin 5: 291-301.
14. Costa CHN, Peters NC, Maruyama SR, de Brito EC Jr, de Miranda Santos IKF, et al. (2011) Vaccines for the Leishmaniases: Proposals for a Research Agenda. PLoS Negl Trop Dis 5: e943.
15. Stager S, Alexander J, Kirby AC, Botto M, Rooijen NV, et al. (2003) Natural antibodies and complement are endogenous adjuvants for vaccine-induced CD8+ T-cell responses. Nat Med 9: 1287-1292.
16. Basu R, Bhaumik S, Haldar AK, Naskar K, De T, et al. (2007) Hybrid cell vaccination resolves Leishmania donovani infection by eliciting a strong CD8+ cytotoxic T-lymphocyte response with concomitant suppression of interleukin-10 (IL-10) but not IL-4 or IL-13. Infect Immun 75: 5956-5966.
17. Muller I, Kropf P, Etges RJ, Louis JA, (1993) Gamma interferon response in secondary Leishmania major infection: role of CD8+ T cells. Infect Immun 61: 3730-3738.
18. Gurunathan S, Sacks DL, Brown DR, Reiner SL, Charest H, et al. (1997) Vaccination with DNA encoding the immunodominant LACK parasite antigen confers protective immunity to mice infected with Leishmania major. J Exp Med 186: 1137-1147.
19. Dumonteil E, (2009) Vaccine development against Trypanosoma cruzi and Leishmania species in the post-genomic era. Infect Genet Evol 9: 1075-1082.
20. Palatnik-de-Sousa CB, (2008) Vaccines for leishmaniasis in the fore coming 25 years. Vaccine 26: 1709-1724.
21. Coler RN, Reed SG, (2005) Second-generation vaccines against leishmaniasis. Trends Parasitol 21: 244-249.
22. Stober CB, Lange UG, Roberts MT, Gilmartin B, Francis R, et al. (2006) From genome to vaccines for leishmaniasis: screening 100 novel vaccine candidates against murine Leishmania major infection. Vaccine 24: 2602-2616.
23. Rappuoli R, (2000) Reverse vaccinology. Curr Opin Microbiol 3: 445-450.
24. Paape D, Lippuner C, Schmid M, Ackermann R, Barrios-Llerena ME, et al. (2008) Transgenic, fluorescent Leishmania mexicana allow direct analysis of the proteome of intracellular amastigotes. Mol Cell Proteomics 7: 1688-1701.
25. Yang DM, Fairweather N, Button LL, McMaster WR, Kahl LP, et al. (1990) Oral Salmonella typhimurium (AroA-) vaccine expressing a major leishmanial surface protein (gp63) preferentially induces T helper 1 cells and protective immunity against leishmaniasis. J Immunol 145: 2281-2285.
26. McSorley SJ, Xu D, Liew FY, (1997) Vaccine efficacy of Salmonella strains expressing glycoprotein 63 with different promoters. Infect Immun 65: 171-178.
27. Lange UG, Mastroeni P, Blackwell JM, Stober CB, (2004) DNA-Salmonella enterica serovar Typhimurium primer-booster vaccination biases towards T helper 1 responses and enhances protection against Leishmania major infection in mice. Infect Immun 72: 4924-4928.
28. Salerno-Goncalves R, Wyant TL, Pasetti MF, Fernandez-Vina M, Tacket CO, et al. (2003) Concomitant induction of CD4+ and CD8+ T cell responses in volunteers immunized with Salmonella enterica serovar Typhi strain CVD 908-htrA. J Immunol 170: 2734-2741.
29. Aebischer T, Bumann D, Epple HJ, Metzger W, Schneider T, et al. (2008) Correlation of T cell response and bacterial clearance in human volunteers challenged with Helicobacter pylori revealed by randomised controlled vaccination with Ty21a-based Salmonella vaccines. Gut 57: 1065-1072.
30. Bumann D, Hueck C, Aebischer T, Meyer TF, (2000) Recombinant live Salmonella spp. for human vaccination against heterologous pathogens. FEMS Immunol Med Microbiol 27: 357-364.
31. Rizos K, Lattemann CT, Bumann D, Meyer TF, Aebischer T, (2003) Autodisplay: efficacious surface exposure of antigenic UreA fragments from Helicobacter pylori in Salmonella vaccine strains. Infect Immun 71: 6320-6328.
32. Schroeder J, Aebischer T, (2009) Recombinant outer membrane vesicles to augment antigen-specific live vaccine responses. Vaccine 27: 6748-6754.
33. Dunstan SJ, Simmons CP, Strugnell RA, (1999) Use of in vivo-regulated promoters to deliver antigens from attenuated Salmonella enterica var. Typhimurium. Infect Immun 67: 5133-5141.
34. Jose J, Kramer J, Klauser T, Pohlner J, Meyer TF, (1996) Absence of periplasmic DsbA oxidoreductase facilitates export of cysteine-containing passenger proteins to the Escherichia coli cell surface via the Iga beta autotransporter pathway. Gene 178: 107-110.
35. Bumann D, (2002) Examination of salmonella gene expression in an infected mammalian host using the green fluorescent protein and two-colour flow cytometry. Mol Microbiol 43: 1269-1283.
36. Dieckmann-Schuppert A, Schnittler HJ, (1997) A simple assay for quantification of protein in tissue sections, cell cultures, and cell homogenates, and of protein immobilized on solid surfaces. Cell Tissue Res 288: 119-126.
37. Taswell C, (1981) Limiting dilution assays for the determination of immunocompetent cell frequencies. I. Data analysis. J Immunol 126: 1614-1619.
38. Smelt SC, Cotterell SE, Engwerda CR, Kaye PM, (2000) B cell-deficient mice are highly resistant to Leishmania donovani infection, but develop neutrophil-mediated tissue pathology. J Immunol 164: 3681-3688.
39. Beattie L, Phillips R, Brown N, Owens BM, Chauhan N, et al. (2010) IRF-7 contributes to the control of Leishmania donovani in the mouse liver. Infect Immun.
40. Sabarth N, Hurwitz R, Meyer TF, Bumann D, (2002) Multiparameter selection of Helicobacter pylori antigens identifies two novel antigens with high protective efficacy. Infect Immun 70: 6499-6503.
41. Basu R, Roy S, Walden P, (2007) HLA class I-restricted T cell epitopes of the kinetoplastid membrane protein-11 presented by Leishmania donovani-infected human macrophages. J Infect Dis 195: 1373-1380.
42. Basu R, Bhaumik S, Basu JM, Naskar K, De T, et al. (2005) Kinetoplastid membrane protein-11 DNA vaccination induces complete protection against both pentavalent antimonial-sensitive and-resistant strains of Leishmania donovani that correlates with inducible nitric oxide synthase activity and IL-4 generation: evidence for mixed Th1- and Th2-like responses in visceral leishmaniasis. J Immunol 174: 7160-7171.
43. Rollenhagen C, Sorensen M, Rizos K, Hurvitz R, Bumann D, (2004) Antigen selection based on expression levels during infection facilitates vaccine development for an intracellular pathogen. Proc Natl Acad Sci U S A 101: 8739-8744.
44. Hess J, Gentschev I, Miko D, Welzel M, Ladel C, et al. (1996) Superior efficacy of secreted over somatic antigen display in recombinant Salmonella vaccine induced protection against listeriosis. Proc Natl Acad Sci U S A 93: 1458-1463.
45. Kanaly ST, Nashleanas M, Hondowicz B, Scott P, (1999) TNF receptor p55 is required for elimination of inflammatory cells following control of intracellular pathogens. J Immunol 163: 3883-3889.
46. Sakthianandeswaren A, Elso CM, Simpson K, Curtis JM, Kumar B, et al. (2005) The wound repair response controls outcome to cutaneous leishmaniasis. Proc Natl Acad Sci U S A 102: 15551-15556.
47. Handman E, Elso C, Foote S, (2005) Genes and susceptibility to leishmaniasis. Adv Parasitol 59: 1-75.:1-75.
48. Snapper CM, Paul WE, (1987) Interferon-gamma and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science 236: 944-947.
49. Trujillo C, Ramirez R, Velez ID, Berberich C, (1999) The humoral immune response to the kinetoplastid membrane protein-11 in patients with American leishmaniasis and Chagas disease: prevalence of IgG subclasses and mapping of epitopes. Immunol Lett 70: 203-209.
50. Rosenzweig D, Smith D, Opperdoes F, Stern S, Olafson RW, et al. (2008) Retooling Leishmania metabolism: from sand fly gut to human macrophage. FASEB J 22: 590-602.
51. Stober CB, (2004) From genomes to vaccines for leishmaniasis. Methods Mol Biol 270: 423-38.:423-438.
52. Almeida R, Norrish A, Levick M, Vetrie D, Freeman T, et al. (2002) From genomes to vaccines: Leishmania as a model. Philos Trans R Soc Lond B Biol Sci 357: 5-11.
53. Aebischer T, Wolfram M, Patzer SI, Ilg T, Wiese M, et al. (2000) Subunit vaccination of mice against new world cutaneous leishmaniasis: comparison of three proteins expressed in amastigotes and six adjuvants. Infect Immun 68: 1328-1336.
54. Overath P, Aebischer T, (1999) Antigen presentation by macrophages harboring intravesicular pathogens. Parasitol Today 15: 325-332.
55. Forgber M, Basu R, Roychoudhury K, Theinert S, Roy S, et al. (2006) Mapping the antigenicity of the parasites in Leishmania donovani infection by proteome serology. PLoS One 1: e40.
56. Forgber M, Gellrich S, Sharav T, Sterry W, Walden P, (2009) Proteome-based analysis of serologically defined tumor-associated antigens in cutaneous lymphoma. PLoS One 4: e8376.
57. Skeiky YA, Guderian JA, Benson DR, Bacelar O, Carvalho EM, et al. (1995) A recombinant Leishmania antigen that stimulates human peripheral blood mononuclear cells to express a Th1-type cytokine profile and to produce interleukin 12. J Exp Med 181: 1527-1537.
58. Goto Y, Coler RN, Guderian J, Mohamath R, Reed SG, (2006) Cloning, characterization, and serodiagnostic evaluation of Leishmania infantum tandem repeat proteins. Infect Immun 74: 3939-3945.
59. Peters C, Aebischer T, Stierhof YD, Fuchs M, Overath P, (1995) The role of macrophage receptors in adhesion and uptake of Leishmania mexicana amastigotes. J Cell Sci 108: 3715-3724.
60. Deak E, Jayakumar A, Cho KW, Goldsmith-Pestana K, Dondji B, et al. (2010) Murine visceral leishmaniasis: IgM and polyclonal B-cell activation lead to disease exacerbation. Eur J Immunol 40: 1355-1368.
61. Bhaumik S, Basu R, Sen S, Naskar K, Roy S, (2009) KMP-11 DNA immunization significantly protects against L. donovani infection but requires exogenous IL-12 as an adjuvant for comparable protection against L. major. Vaccine 27: 1306-1316.
62. Nascimento E, Fernandes DF, Vieira EP, Campos-Neto A, Ashman JA, et al. (2010) A clinical trial to evaluate the safety and immunogenicity of the LEISH-F1+MPL-SE vaccine when used in combination with meglumine antimoniate for the treatment of cutaneous leishmaniasis. Vaccine 28: 6581-6587.
63. Moreno J, Nieto J, Masina S, Canavate C, Cruz I, et al. (2007) Immunization with H1, HASPB1 and MML Leishmania proteins in a vaccine trial against experimental canine leishmaniasis. Vaccine 25: 5290-5300.
64. Miret J, Nascimento E, Sampaio W, Franca JC, Fujiwara RT, et al. (2008) Evaluation of an immunochemotherapeutic protocol constituted of N-methyl meglumine antimoniate (Glucantime) and the recombinant Leish-110f+MPL-SE vaccine to treat canine visceral leishmaniasis. Vaccine 26: 1585-1594.
65. Palatnik-de-Sousa CB, Silva-Antunes I, Morgado AA, Menz I, Palatnik M, et al. (2009) Decrease of the incidence of human and canine visceral leishmaniasis after dog vaccination with Leishmune in Brazilian endemic areas. Vaccine 27: 3505-3512.
66. Galen JE, Pasetti MF, Tennant S, Ruiz-Olvera P, Sztein MB, et al. (2009) Salmonella enterica serovar Typhi live vector vaccines finally come of age. Immunol Cell Biol 87: 400-412.
67. Aebischer T, Walduck A, Schroeder J, Wehrens A, Chijioke O, et al. (2008) A vaccine against Helicobacter pylori: towards understanding the mechanism of protection. Int J Med Microbiol 298: 161-168.
68. Salerno-Goncalves R, Sztein MB, (2009) Priming of Salmonella enterica serovar Typhi-specific CD8+ T cells by suicide dendritic cell cross-presentation in humans. PLoS One 4: e5879.
69. Schroeder J, Aebischer T, (2011) Vaccines for Leishmaniasis: From proteome to vaccine candidates. Hum Vaccin 7: 10-15.
70. Angelakopoulos H, Hohmann EL, (2000) Pilot study of phoP/phoQ-deleted Salmonella enterica serovar Typhimurium expressing Helicobacter pylori urease in adult volunteers. Infect Immun 68: 2135-2141.
71. Petavy AF, Hormaeche C, Lahmar S, Ouhelli H, Chabalgoity A, et al. (2008) An oral recombinant vaccine in dogs against Echinococcus granulosus, the causative agent of human hydatid disease: a pilot study. PLoS Negl Trop Dis 2: e125.
72. McVey DS, Chengappa MM, Mosier DE, Stone GG, Oberst RD, et al. (2002) Immunogenicity of chi4127 phoP- Salmonella enterica serovar Typhimurium in dogs. Vaccine 20: 1618-1623.
73. Chabalgoity JA, Moreno M, Carol H, Dougan G, Hormaeche CE, (2000) Salmonella typhimurium as a basis for a live oral Echinococcus granulosus vaccine. Vaccine 19: 460-469.