Challenges and perspectives in vaccination against leishmaniasis

Parasitology International

Volumn 58, Issue 4, 2009, Pages 319-324

  de Oliveira, Camila I ^a   Nascimento, Ivan P ^a   Barral, Aldina ^a,b   Soto, Manuel ^c   Barral Netto, Manoel ^a,b  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b Institute de Investigação em Imunologia iii   (Brazil)

^c CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

Author keywords

BCG; Leishmania; Saliva; Sand fly

Indexed keywords

B7 ANTIGEN; BCG VACCINE; CPG OLIGODEOXYNUCLEOTIDE; DNA VACCINE; GAMMA INTERFERON; HISTONE H3; HLA DR ANTIGEN; IMMUNOGLOBULIN ANTIBODY; IMMUNOGLOBULIN E ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G4 ANTIBODY; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; LEISHMANIA VACCINE; MAXADILAN; MEGLUMINE ANTIMONATE; PARASITE ANTIGEN; RECOMBINANT VACCINE; SALIVA PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; CELL PROLIFERATION; CELLULAR IMMUNITY; CLINICAL TRIAL; CYTOKINE RELEASE; DELAYED HYPERSENSITIVITY; DISEASE MODEL; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG SAFETY; ERYTHEMA; EXPERIMENTAL INFECTION; HUMAN; IMMUNOGENICITY; IMMUNOMODULATION; IMMUNOPATHOGENESIS; IMMUNOPROPHYLAXIS; IMMUNOSTIMULATION; IMMUNOTHERAPY; LEISHMANIA BRAZILIENSIS; LEISHMANIA DONOVANI; LEISHMANIA MAJOR; LEISHMANIA MEXICANA; LEISHMANIASIS; NONHUMAN; PARASITE TRANSMISSION; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN SYNTHESIS INHIBITION; PSYCHODIDAE; REVIEW; SALIVA; SINGLE DRUG DOSE; STRAIN DIFFERENCE; TH1 CELL; TREATMENT OUTCOME; VISCERAL LEISHMANIASIS;

ANIMALS; ANTIGENS, PROTOZOAN; HUMANS; LEISHMANIA BRAZILIENSIS; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; MICE; MYCOBACTERIUM BOVIS; PROTOZOAN VACCINES; PSYCHODIDAE; SALIVA; VACCINATION;

LEISHMANIA BRAZILIENSIS; LEISHMANIA MAJOR; PHLEBOTOMINAE; PROTOZOA; VERTEBRATA;

EID: 70349820129     PISSN: 13835769     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.parint.2009.07.013     Document Type: Review

References (94)

1. Herwaldt B.L. Leishmaniasis. Lancet 2 354 (1999) 1191-1199
2. Andrade B.B., de Oliveira C.I., Brodskyn C.I., Barral A., and Barral-Netto M. Role of sand fly saliva in human and experimental leishmaniasis: current insights. Scand J Immunol 66 (2007) 122-127
3. Rogers K.A., and Titus R.G. Immunomodulatory effects of Maxadilan and Phlebotomus papatasi sand fly salivary gland lysates on human primary in vitro immune responses. Parasite Immunol 25 (2003) 127-134
4. Costa D.J., Favali C., Clarencio J., Afonso L., Conceicao V., Miranda J.C., et al. Lutzomyia longipalpis salivary gland homogenate impairs cytokine production and costimulatory molecule expression on human monocytes and dendritic cells. Infect Immun 72 (2004) 1298-1305
5. Titus R.G., and Ribeiro J.M. Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 11 239 (1988) 1306-1308
6. Samuelson J., Lerner E., Tesh R., and Titus R. A mouse model of Leishmania braziliensis braziliensis infection produced by coinjection with sand fly saliva. J Exp Med 1 173 (1991) 49-54
7. Bezerra H.S., and Teixeira M.J. Effect of Lutzomyia whitmani (Diptera: Psychodidae) salivary gland lysates on Leishmania (Viannia) braziliensis infection in BALB/c mice. Mem Inst Oswaldo Cruz 96 (2001) 349-351
8. Norsworthy N.B., Sun J., Elnaiem D., Lanzaro G., and Soong L. Sand fly saliva enhances Leishmania amazonensis infection by modulating interleukin-10 production. Infect Immun 72 (2004) 1240-1247
9. Kamhawi S., Belkaid Y., Modi G., Rowton E., and Sacks D. Protection against cutaneous leishmaniasis resulting from bites of uninfected sand flies. Science 17 290 (2000) 1351-1354
10. Valenzuela J.G., Belkaid Y., Garfield M.K., Mendez S., Kamhawi S., Rowton E.D., et al. Toward a defined anti-Leishmania vaccine targeting vector antigens: characterization of a protective salivary protein. J Exp Med 6 194 (2001) 331-342
11. de Moura T.R., Oliveira F., Novais F.O., Miranda J.C., Clarencio J., Follador I., et al. Enhanced Leishmania braziliensis infection following pre-exposure to sandfly saliva. PLoS Negl Trop Dis 1 (2007) e84
12. Gomes R., Teixeira C., Teixeira M.J., Oliveira F., Menezes M.J., Silva C., et al. Immunity to a salivary protein of a sand fly vector protects against the fatal outcome of visceral leishmaniasis in a hamster model. Proc Natl Acad Sci U S A 3 105 (2008) 7845-7850
13. Collin N., Gomes R., Teixeira C., Cheng L., Laughinghouse A., Ward J.M., et al. Sand fly salivary proteins induce strong cellular immunity in a natural reservoir of visceral leishmaniasis with adverse consequences for Leishmania. PLoS Pathogens 5 (2009) e1000441
14. Peters N.C., Kimblin N., Secundino N., Kamhawi S., Lawyer P., and Sacks D.L. Vector transmission of Leishmania abrogates vaccine-induced protective immunity. PLoS Pathogens 5 (2009) e1000484
15. Barral A., Honda E., Caldas A., Costa J., Vinhas V., Rowton E.D., et al. Human immune response to sand fly salivary gland antigens: a useful epidemiological marker?. Am J Trop Med Hyg 62 (Jun 2000) 740-745
16. Gomes R.B., Brodskyn C., de Oliveira C.I., Costa J., Miranda J.C., Caldas A., et al. Seroconversion against Lutzomyia longipalpis saliva concurrent with the development of anti-Leishmania chagasi delayed-type hypersensitivity. J Infect Dis 186 (Nov 15 2002) 1530-1534
17. Vinhas V., Andrade B.B., Paes F., Bomura A., Clarencio J., Miranda J.C., et al. Human anti-saliva immune response following experimental exposure to the visceral leishmaniasis vector, Lutzomyia longipalpis. Eur J Immunol 37 (2007) 3111-3121
18. Requena J.M., Iborra S., Carrion J., Alonso C., and Soto M. Recent advances in vaccines for leishmaniasis. Expert Opin Biol Ther 4 (2004) 1505-1517
19. Charest H., and Matlashewski G. Developmental gene expression in Leishmania donovani: differential cloning and analysis of an amastigote-stage-specific gene. Mol Cell Biol 14 (1994) 2975-2984
20. Goto Y., Bogatzki L.Y., Bertholet S., Coler R.N., and Reed S.G. Protective immunization against visceral leishmaniasis using Leishmania sterol 24-c-methyltransferase formulated in adjuvant. Vaccine 16 25 (2007) 7450-7458
21. Requena JM, Alonso C, Soto M. Evolutionarily conserved proteins as prominent immunogens during Leishmania infections. Parasitol Today 2000; 16: 246-50.
22. Maalej I.A., Chenik M., Louzir H., Ben Salah A., Bahloul C., Amri F., et al. Comparative evaluation of ELISAs based on ten recombinant or purified Leishmania antigens for the serodiagnosis of Mediterranean visceral leishmaniasis. Am J Trop Med Hyg 68 (2003) 312-320
23. Ghedin E., Zhang W.W., Charest H., Sundar S., Kenney R.T., and Matlashewski G. Antibody response against a Leishmania donovani amastigote-stage-specific protein in patients with visceral leishmaniasis. Clin Diagn Lab Immunol 4 (1997) 530-535
24. Montoya Y., Leon C., Talledo M., Nolasco O., Padilla C., Munoz-Najar U., et al. Recombinant antigens for specific and sensitive serodiagnosis of Latin American tegumentary leishmaniasis. Trans R Soc Trop Med Hyg 91 (1997) 674-676
25. Webb J.R., Campos-Neto A., Ovendale P.J., Martin T.I., Stromberg E.J., Badaro R., et al. Human and murine immune responses to a novel Leishmania major recombinant protein encoded by members of a multicopy gene family. Infect Immun 66 (1998) 3279-3289
26. Goto Y., Howard R.F., Bhatia A., Trigo J., Nakatani M., Netto E.M., et al. Distinct antigen recognition pattern during zoonotic visceral leishmaniasis in humans and dogs. Veterinary Parasitology 160 (2009) 215-220
27. Carvalho F.A., Charest H., Tavares C.A., Matlashewski G., Valente E.P., Rabello A., et al. Diagnosis of American visceral leishmaniasis in humans and dogs using the recombinant Leishmania donovani A2 antigen. Diagn Microbiol Infect Dis 43 (2002) 289-295
28. Soto M., Requena J.M., Quijada L., Perez M.J., Nieto C.G., Guzman F., et al. Antigenicity of the Leishmania infantum histones H2B and H4 during canine viscerocutaneous leishmaniasis. Clin Exp Immunol 115 (1999) 342-349
29. Probst P., Stromberg E., Ghalib H.W., Mozel M., Badaro R., Reed S.G., et al. Identification and characterization of T cell-stimulating antigens from Leishmania by CD4 T cell expression cloning. J Immunol 166 (2001) 498-505
30. de Carvalho L.P., Soto M., Jeronimo S., Dondji B., Bacellar O., Luz V., et al. Characterization of the immune response to Leishmania infantum recombinant antigens. Microbes Infect 5 (2003) 7-12
31. Martins D.R., Jeronimo S.M., Donelson J.E., and Wilson M.E. Leishmania chagasi T-cell antigens identified through a double library screen. Infect Immun 74 (2006) 6940-6948
32. Dominguez M., Moreno I., Aizpurua C., and Torano A. Early mechanisms of Leishmania infection in human blood. Microbes Infect 5 (2003) 507-513
33. Guimaraes-Costa A.B., Nascimento M.T., Froment G.S., Soares R.P., Morgado F.N., Conceicao-Silva F., et al. Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc Natl Acad Sci U S A 21 106 (2009) 6748-6753
34. Chang K.P., Reed S.G., McGwire B.S., and Soong L. Leishmania model for microbial virulence: the relevance of parasite multiplication and pathoantigenicity. Acta Tropica 85 (2003) 375-390
35. Ghosh A., Labrecque S., and Matlashewski G. Protection against Leishmania donovani infection by DNA vaccination: increased DNA vaccination efficiency through inhibiting the cellular p53 response. Vaccine 30 19 (2001) 3169-3178
36. Ghosh A., Zhang W.W., and Matlashewski G. Immunization with A2 protein results in a mixed Th1/Th2 and a humoral response which protects mice against Leishmania donovani infections. Vaccine 12 20 (2001) 59-66
37. Melby P.C., Yang J., Zhao W., Perez L.E., and Cheng J. Leishmania donovani p36(LACK) DNA vaccine is highly immunogenic but not protective against experimental visceral leishmaniasis. Infect Immun 69 (2001) 4719-4725
38. Wilson M.E., Jeronimo S.M., and Pearson R.D. Immunopathogenesis of infection with the visceralizing Leishmania species. Microb Pathog 38 (2005) 147-160
39. Bhardwaj S., Vasishta R.K., and Arora S.K. Vaccination with a novel recombinant Leishmania antigen plus MPL provides partial protection against L. donovani challenge in experimental model of visceral leishmaniasis. Exp Parasitol 121 (2009) 29-37
40. Carrion J., Nieto A., Soto M., and Alonso C. Adoptive transfer of dendritic cells pulsed with Leishmania infantum nucleosomal histones confers protection against cutaneous leishmaniosis in BALB/c mice. Microbes Infect 9 (2007) 735-743
41. + regulatory T cells control Leishmania major persistence and immunity. Nature 5 420 (2002) 502-507
42. Mendez S., Reckling S.K., Piccirillo C.A., Sacks D., and Belkaid Y. Role for CD4(+) CD25(+) regulatory T cells in reactivation of persistent leishmaniasis and control of concomitant immunity. J Exp Med 19 200 (2004) 201-210
43. + (Foxp3) regulatory T cells in human visceral leishmaniasis. J Exp Med 26 (2007) 204
44. Borges M.M., Campos-Neto A., Sleath P., Grabstein K.H., Morrissey P.J., Skeiky Y.A., et al. Potent stimulation of the innate immune system by a Leishmania brasiliensis recombinant protein. Infect Immun 69 (2001) 5270-5277
45. Mougneau E., Altare F., Wakil A.E., Zheng S., Coppola T., Wang Z.E., et al. Expression cloning of a protective Leishmania antigen. Science 28 268 (1995) 563-566
46. Campos-Neto A., Webb J.R., Greeson K., Coler R.N., Skeiky Y.A., and Reed S.G. Vaccination with plasmid DNA encoding TSA/LmSTI1 leishmanial fusion proteins confers protection against Leishmania major infection in susceptible BALB/c mice. Infect Immun 70 (2002) 2828-2836
47. Gurunathan S., Sacks D.L., Brown D.R., Reiner S.L., Charest H., Glaichenhaus N., et al. Vaccination with DNA encoding the immunodominant LACK parasite antigen confers protective immunity to mice infected with Leishmania major. J Exp Med 6 186 (1997) 1137-1147
48. Iborra S., Soto M., Carrion J., Alonso C., and Requena J.M. Vaccination with a plasmid DNA cocktail encoding the nucleosomal histones of Leishmania confers protection against murine cutaneous leishmaniosis. Vaccine 28 22 (2004) 3865-3876
49. Iborra S., Carrion J., Anderson C., Alonso C., Sacks D., and Soto M. Vaccination with the Leishmania infantum acidic ribosomal P0 protein plus CpG oligodeoxynucleotides induces protection against cutaneous leishmaniasis in C57BL/6 mice but does not prevent progressive disease in BALB/c mice. Infect Immun 73 (2005) 5842-5852
50. Iborra S., Soto M., Carrion J., Nieto A., Fernandez E., Alonso C., et al. The Leishmania infantum acidic ribosomal protein P0 administered as a DNA vaccine confers protective immunity to Leishmania major infection in BALB/c mice. Infect Immun 71 (2003) 6562-6572
51. Iborra S., Abanades D.R., Parody N., Carrion J., Risueno R.M., Pineda M.A., et al. The immunodominant T helper 2 (Th2) response elicited in BALB/c mice by the Leishmania LiP2a and LiP2b acidic ribosomal proteins cannot be reverted by strong Th1 inducers. Clin Exp Immunol 150 (2007) 375-385
52. Rafati S., Gholami E., Hassani N., Ghaemimanesh F., Taslimi Y., Taheri T., et al. Leishmania major heat shock protein 70 (HSP70) is not protective in murine models of cutaneous leishmaniasis and stimulates strong humoral responses in cutaneous and visceral leishmaniasis patients. Vaccine 22 25 (2007) 4159-4169
53. Belkaid Y., Hoffmann K.F., Mendez S., Kamhawi S., Udey M.C., Wynn T.A., et al. The role of interleukin (IL)-10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti-IL-10 receptor antibody for sterile cure. J Exp Med 19 194 (2001) 1497-1506
54. Levick M.P., Tetaud E., Fairlamb A.H., and Blackwell J.M. Identification and characterisation of a functional peroxidoxin from Leishmania major. Mol Biochem Parasitol 30 96 (1998) 125-137
55. Gicquel B. BCG as a vector for the construction of multivalent recombinant vaccines. Biologicals 23 (1995) 113-118
56. Handman E. Leishmaniasis: current status of vaccine development. Clin Microbiol Rev 14 (2001) 229-243
57. Convit J., Ulrich M., Polegre M.A., Avila A., Rodriguez N., Mazzedo M.I., et al. Therapy of Venezuelan patients with severe mucocutaneous or early lesions of diffuse cutaneous leishmaniasis with a vaccine containing pasteurized Leishmania promastigotes and bacillus Calmette-Guerin: preliminary report. Mem Inst Oswaldo Cruz 99 (2004) 57-62
58. Khamesipour A., Rafati S., Davoudi N., Maboudi F., and Modabber F. Leishmaniasis vaccine candidates for development: a global overview. Indian J Med Res 123 (2006) 423-438
59. Noazin S., Modabber F., Khamesipour A., Smith P.G., Moulton L.H., Nasseri K., et al. First generation leishmaniasis vaccines: a review of field efficacy trials. Vaccine 9 26 (2008) 6759-6767
60. Castes M., Moros Z., Martinez A., Trujillo D., Castellanos P.L., Rondon A.J., et al. Cell-mediated immunity in localized cutaneous leishmaniasis patients before and after treatment with immunotherapy or chemotherapy. Parasite Immunol 11 (1989) 211-222
61. Sharifi I., FeKri A.R., Aflatonian M.R., Khamesipour A., Nadim A., Mousavi M.R., et al. Randomised vaccine trial of single dose of killed Leishmania major plus BCG against anthroponotic cutaneous leishmaniasis in Bam, Iran. Lancet 23 351 (1998) 1540-1543
62. Momeni A.Z., Jalayer T., Emamjomeh M., Khamesipour A., Zicker F., Ghassemi R.L., et al. A randomised, double-blind, controlled trial of a killed L. major vaccine plus BCG against zoonotic cutaneous leishmaniasis in Iran. Vaccine 5 17 (1999) 466-472
63. Khalil E.A., El Hassan A.M., Zijlstra E.E., Mukhtar M.M., Ghalib H.W., Musa B., et al. Autoclaved Leishmania major vaccine for prevention of visceral leishmaniasis: a randomised, double-blind, BCG-controlled trial in Sudan. Lancet 4 356 (2000) 1565-1569
64. Khalil E.A., Musa A.M., Modabber F., and El-Hassan A.M. Safety and immunogenicity of a candidate vaccine for visceral leishmaniasis (Alum-precipitated autoclaved Leishmania major + BCG) in children: an extended phase II study. Ann Trop Paediatr 26 (2006) 357-361
65. Barletta R.G., Snapper B., Cirillo J.D., Connell N.D., Kim D.D., Jacobs W.R., et al. Recombinant BCG as a candidate oral vaccine vector. Res Microbiol 141 (1990) 931-939
66. Lagranderie M., Murray A., Gicquel B., Leclerc C., and Gheorghiu M. Oral immunization with recombinant BCG induces cellular and humoral immune responses against the foreign antigen. Vaccine 11 (1993) 1283-1290
67. Aldovini A., and Young R.A. Humoral and cell-mediated immune responses to live recombinant BCG-HIV vaccines. Nature 6 351 (1991) 479-482
68. Matsuo K., Yamaguchi R., Yamazaki A., Tasaka H., Terasaka K., Totsuka M., et al. Establishment of a foreign antigen secretion system in mycobacteria. Infect Immun 58 (1990) 4049-4054
69. Haeseleer F., Pollet J.F., Haumont M., Bollen A., and Jacobs P. Stable integration and expression of the Plasmodium falciparum circumsporozoite protein coding sequence in mycobacteria. Mol Biochem Parasitol 57 (1993) 117-126
70. Nascimento I.P., Dias W.O., Mazzantini R.P., Miyaji E.N., Gamberini M., Quintilio W., et al. Recombinant Mycobacterium bovis BCG expressing pertussis toxin subunit S1 induces protection against an intracerebral challenge with live Bordetella pertussis in mice. Infect Immun 68 (2000) 4877-4883
71. Connell N.D., Medina-Acosta E., McMaster W.R., Bloom B.R., and Russell D.G. Effective immunization against cutaneous leishmaniasis with recombinant bacille Calmette-Guerin expressing the Leishmania surface proteinase gp63. Proc Natl Acad Sci U S A 15 90 (1993) 11473-11477
72. Abdelhak S., Louzir H., Timm J., Blel L., Benlasfar Z., Lagranderie M., et al. Recombinant BCG expressing the leishmania surface antigen Gp63 induces protective immunity against Leishmania major infection in BALB/c mice. Microbiology (Reading, England) 141 (1995) 1585-1592
73. Streit J.A., Recker T.J., Donelson J.E., and Wilson M.E. BCG expressing LCR1 of Leishmania chagasi induces protective immunity in susceptible mice. Exp Parasitol 94 (2000) 33-41
74. Liu W., O'Donnell M.A., Chen X., Han R., and Luo Y. Recombinant bacillus Calmette-Guerin (BCG) expressing interferon-alpha 2B enhances human mononuclear cell cytotoxicity against bladder cancer cell lines in vitro. Cancer Immunol Immunother 58 (2009) 1647-1655
75. Chege G.K., Thomas R., Shephard E.G., Meyers A., Bourn W., Williamson C., et al. A prime-boost immunisation regimen using recombinant BCG and Pr55(gag) virus-like particle vaccines based on HIV type 1 subtype C successfully elicits Gag-specific responses in baboons. Vaccine 30 27 (2009) 4857-4866
76. Cayabyab M.J., Korioth-Schmitz B., Sun Y., Carville A., Balachandran H., Miura A., et al. Recombinant Mycobacterium bovis BCG prime-recombinant adenovirus boost vaccination in rhesus monkeys elicits robust polyfunctional simian immunodeficiency virus-specific T-cell responses. J Virol 83 (2009) 5505-5513
77. Bueno S.M., Gonzalez P.A., Cautivo K.M., Mora J.E., Leiva E.D., Tobar H.E., et al. Protective T cell immunity against respiratory syncytial virus is efficiently induced by recombinant BCG. Proc Natl Acad Sci U S A 30 105 (2008) 20822-20827
78. Bittencourt A., Silva N., Straatmann A., Nunes V.L., Follador I., and Badaro R. Post-kala-azar dermal leishmaniasis associated with AIDS. Braz J Infect Dis 7 (2003) 229-233
79. Costa J.M., Marsden P.D., Llanos-Cuentas E.A., Netto E.M., Carvalho E.M., Barral A., et al. Disseminated cutaneous leishmaniasis in a field clinic in Bahia, Brazil: a report of eight cases. J Trop Med Hyg 89 (1986) 319-323
80. Marsden P.D. Mucosal leishmaniasis ("espundia" Escomel, 1911). Trans R Soc Trop Med Hyg 80 (1986) 859-876
81. Smith D.F., Peacock C.S., and Cruz A.K. Comparative genomics: from genotype to disease phenotype in the leishmaniases. Int J Parasitol 37 (2007) 1173-1186
82. Bittencourt A., and Barral-Netto M. Leishmaniasis. In: Doerr W.S.G. (Ed). Tropical Pathology. 2nd ed (1995), Springer, Berlin 597-651
83. Grevelink S.A., and Lerner E.A. Leishmaniasis. J Am Acad Dermatol 34 (1996) 257-272
84. Belkaid Y., Mendez S., Lira R., Kadambi N., Milon G., and Sacks D. A natural model of Leishmania major infection reveals a prolonged "silent" phase of parasite amplification in the skin before the onset of lesion formation and immunity. J Immunol 15 165 (2000) 969-977
85. de Moura T.R., Novais F.O., Oliveira F., Clarencio J., Noronha A., Barral A., et al. Toward a novel experimental model of infection to study American cutaneous leishmaniasis caused by Leishmania braziliensis. Infect Immun 73 (2005) 5827-5834
86. DeKrey G.K., Lima H.C., and Titus R.G. Analysis of the immune responses of mice to infection with Leishmania braziliensis. Infect Immun 66 (1998) 827-829
87. + T cells instructs Th2 development and susceptibility to Leishmania major in BALB/c mice. Immunity 6 (1997) 541-549
88. Rocha F.J., Schleicher U., Mattner J., Alber G., and Bogdan C. Cytokines, signaling pathways, and effector molecules required for the control of Leishmania (Viannia) braziliensis in mice. Infect Immun 75 (2007) 3823-3832
89. Salay G., Dorta M.L., Santos N.M., Mortara R.A., Brodskyn C., Oliveira C.I., et al. Testing of four Leishmania vaccine candidates in a mouse model of infection with Leishmania (Viannia) braziliensis, the main causative agent of cutaneous leishmaniasis in the New World. Clin Vaccine Immunol 14 (2007) 1173-1181
90. Okwor I., and Uzonna J. Vaccines and vaccination strategies against human cutaneous leishmaniasis. Human Vaccines 12 (2009) 5
91. Menezes M.J., Costa D.J., Clarencio J., Miranda J.C., Barral A., Barral-Netto M., et al. Immunomodulation of human monocytes following exposure to Lutzomyia intermedia saliva. BMC Immunol 9 (2008) 12
92. + T cell epitopes of Leishmania major proteins in susceptible BALB/c and resistant C57BL/6 murine models of infection. Infect Genet Evol 9 (2009) 344-350
93. Herrera-Najera C., Pina-Aguilar R., Xacur-Garcia F., Ramirez-Sierra M.J., and Dumonteil E. Mining the Leishmania genome for novel antigens and vaccine candidates. Proteomics 9 (2009) 1293-1301
94. Reithinger R., Dujardin J.C., Louzir H., Pirmez C., Alexander B., and Brooker S. Cutaneous leishmaniasis. Lancet Infect Dis 7 (2007) 581-596