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Intranasal vaccination with killed Leishmania amazonensis promastigotes antigen (LaAg) associated with CAF01 adjuvant induces partial protection in BALB/c mice challenged with Leishmania (infantum) chagasi.

Published online by Cambridge University Press:  23 September 2015

JANINE MIRANDA LEAL ,
MARCELLE MOSQUINI ,
LUCIANA POLACO COVRE ,
NATALY PESCINALLI STAGMILLER ,
RODRIGO RIBEIRO RODRIGUES ,
DENNIS CHRISTENSEN ,
HERBERT LEONEL DE MATOS GUEDES ,
BARTIRA ROSSI-BERGMANN  and
DANIEL CLÁUDIO DE OLIVIERA GOMES
JANINE MIRANDA LEAL
Affiliation:
Núcleo de Doenças Infecciosas/Núcleo de Biotecnologia, Universidade Federal do Espírito Santo – UFES, Vitória, Brazil
MARCELLE MOSQUINI
Affiliation:
Núcleo de Doenças Infecciosas/Núcleo de Biotecnologia, Universidade Federal do Espírito Santo – UFES, Vitória, Brazil
LUCIANA POLACO COVRE
Affiliation:
Núcleo de Doenças Infecciosas/Núcleo de Biotecnologia, Universidade Federal do Espírito Santo – UFES, Vitória, Brazil
NATALY PESCINALLI STAGMILLER
Affiliation:
Núcleo de Núcleo de Biotecnologia, Universidade Federal do Espírito Santo – UFES, Vitória, Brazil
RODRIGO RIBEIRO RODRIGUES
Affiliation:
Núcleo de Doenças Infecciosas/Núcleo de Biotecnologia, Universidade Federal do Espírito Santo – UFES, Vitória, Brazil
DENNIS CHRISTENSEN
Affiliation:
Department of Infectious Disease and Immunology, Statens Serum Institut, Copenhagen, Denmark
HERBERT LEONEL DE MATOS GUEDES
Affiliation:
Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
BARTIRA ROSSI-BERGMANN
Affiliation:
Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
DANIEL CLÁUDIO DE OLIVIERA GOMES*
Affiliation:
Núcleo de Doenças Infecciosas/Núcleo de Biotecnologia, Universidade Federal do Espírito Santo – UFES, Vitória, Brazil Núcleo de Núcleo de Biotecnologia, Universidade Federal do Espírito Santo – UFES, Vitória, Brazil
*
*Corresponding author. Laboratório de Imunobiologia, Núcleo de Doenças Infecciosas/Núcleo de Biotecnologia, Universidade Federal do Espirito Santo – UFES, Av. Marechal Campos, 1468 – Maruípe, Vitória – ES, Cep 29040-091, Brazil. E-mail: dgomes@ndi.ufes.br
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Summary

The CAF01 adjuvant has previously been shown to be safe for human use and to be a potent adjuvant for several vaccine antigens. In the present work, we sought to optimize the Leishmania amazonensis antigens (LaAg) intranasal vaccine in an attempt to enhance the protective immune responses against Leishmania (infantum) chagasi by using the CAF01 association. LaAg/CAF01 vaccinated mice that were challenged 15 days after booster dose with L. (infantum) chagasi showed a significant reduction in their parasite burden in both the spleen and liver, which is associated with an increase in specific production of IFN-γ and nitrite, and a decrease in IL-4 production. In addition, LaAg/CAF01 intranasal delivery was able to increase lymphoproliferative immune responses after parasite antigen recall. These results suggest the feasibility of using the intranasal route for the delivery of crude antigens and of a human-compatible adjuvant against visceral leishmaniasis.

Keywords

Leishmania infantum chagasi; intranasal vaccination; LaAgCAF01 adjuvant
Type
Research Article
Information
Parasitology , Volume 142 , Issue 13 , November 2015 , pp. 1640 - 1646
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Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Agger, E. M., Rosenkrands, I., Hansen, J., Brahimi, K., Vandahl, B. S., Aagaard, C., Werninghaus, K., Kirschning, C., Lang, R., Christensen, D., Theisen, M., Follmann, F. and Andersen, P. (2008). Cationic liposomes formulated with synthetic mycobacterial cordfactor (CAF01): a versatile adjuvant for vaccines with different immunological requirements. PLoS ONE 3, e3116.CrossRefGoogle ScholarPubMed
Carapau, D., Mitchell, R., Nacer, A., Shaw, A., Othoro, C., Frevert, U. and Nardin, E. (2013). Protective humoral immunity elicited by a needle-free malaria vaccine comprised of a chimeric Plasmodium falciparum circumsporozoite protein and a Toll-like receptor 5 agonist, flagellin. Infection and Immunity 81, 4350–4362.Google Scholar
Cardoso, S. R. A., Da Silva, J. C. F., Da Costa, R. T., Mayrink, W., Melo, M. N., Marques Michalick, M. S., Willi Liu, I. A., Fujiwara, R. T. and Nascimento, E. (2003). Identification and purification of immunogenic proteins from nonliving promastigote polyvalent Leishmania vaccine (Leishvacin®). Revista da Sociedade Brasileira de Medicina Tropical 36, 193–199.Google Scholar
Chaves, S. P., Claudio, D., Gomes, O., De-simone, S. G., Rossi-bergmann, B. and De Matos, H. L. (2015). Vaccines & vaccination serine proteases and vaccines against. Leishmaniasis: A Dual Role 6, 1–5.Google Scholar
Da Silva-Couto, L., Ribeiro-Romão, R. P., Saavedra, A. F., da Silva Costa Souza, B. L., Moreira, O. C., Gomes-Silva, A., Rossi-Bergmann, B., Da-Cruz, A. M. and Pinto, E. F. (2015). Intranasal vaccination with Leishmanial antigens protects golden hamsters (Mesocricetus auratus) against Leishmania (Viannia) braziliensis infection. PLoS Neglected Tropical Diseases 9, e3439.Google Scholar
De Oliveira Gomes, D. C., Da Silva Costa Souza, B. L., De Matos Guedes, H. L., Lopes, U. G. and Rossi-Bergmann, B. (2011). Intranasal immunization with LACK-DNA promotes protective immunity in hamsters challenged with Leishmania chagasi . Parasitology 138, 1892–1897.Google Scholar
De Oliveira Gomes, D. C., Schwedersky, R. P., De-Melo, L. D. B., Da Silva Costa Souza, B. L., De Matos Guedes, H. L., Lopes, U. G. and Rossi-Bergmann, B. (2012). Peripheral expression of LACK-mRNA induced by intranasal vaccination with PCI-NEO-LACK defines the protection duration against murine visceral leishmaniasis. Parasitology 139, 1562–1569.Google Scholar
Dietrich, J., Andreasen, L. V., Andersen, P. and Agger, E. M. (2014). Inducing dose sparing with inactivated polio virus formulated in adjuvant CAF01. PLoS ONE 9, e100879.CrossRefGoogle ScholarPubMed
Fomsgaard, A., Karlsson, I., Gram, G., Schou, C., Tang, S., Bang, P., Kromann, I., Andersen, P. and Andreasen, L. V. (2011). Development and preclinical safety evaluation of a new therapeutic HIV-1 vaccine based on 18 T-cell minimal epitope peptides applying a novel cationic adjuvant CAF01. Vaccine 29, 7067–7074.Google Scholar
Fouda, G. G. a., Amos, J. D., Wilks, A. B., Pollara, J., Ray, C. a., Chand, A., Kunz, E. L., Liebl, B. E., Whitaker, K., Carville, A., Smith, S., Colvin, L., Pickup, D. J., Staats, H. F., Overman, G., Eutsey-Lloyd, K., Parks, R., Chen, H., Labranche, C., Barnett, S., Tomaras, G. D., Ferrari, G., Montefiori, D. C., Liao, H.-X., Letvin, N. L., Haynes, B. F. and Permar, S. R. (2013). Mucosal immunization of lactating female rhesus monkeys with a transmitted/founder HIV-1 envelope induces strong Env-specific IgA antibody responses in breast milk. Journal of Virology 87, 6986–6999.Google Scholar
Garg, R. and Dube, A. (2006). Animal models for vaccine studies for visceral leishmaniasis. Indian Journal of Medical Research 123, 439–454.Google Scholar
Ghosh, A., Zhang, W. W. and Matlashewski, G. (2001). Immunization with A2 protein results in a mixed Th1/Th2 and a humoral response which protects mice against Leishmania donovani infections. Vaccine 20, 59–66.Google Scholar
Gomes, D. C. D. O., Pinto, E. F., Melo, L. D. B. D., Lima, W. P., Larraga, V., Lopes, U. G. and Rossi-Bergmann, B. (2007). Intranasal delivery of naked DNA encoding the LACK antigen leads to protective immunity against visceral leishmaniasis in mice. Vaccine 25, 2168–2172.Google Scholar
Green, L. C., Wagner, D. A., Glogowski, J., Skipper, P. L., Wishnok, J. S. and Tannenbaum, S. R. (1982). Analysis of nitrate, nitrite and [15N]nitrate in biological fluids. Analytical Biochemistry 126, 131–138.Google Scholar
Iniesta, V., Gómez-Nieto, L. C., Molano, I., Mohedano, A., Carcelén, J., Mirón, C., Alonso, C. and Corraliza, I. (2002). Arginase I induction in macrophages, triggered by Th2-type cytokines, supports the growth of intracellular Leishmania parasites. Parasite Immunology 24, 113–118.Google Scholar
Kamath, A. T., Mastelic, B., Christensen, D., Rochat, A.-F., Agger, E. M., Pinschewer, D. D., Andersen, P., Lambert, P.-H. and Siegrist, C.-A. (2012). Synchronization of dendritic cell activation and antigen exposure is required for the induction of Th1/Th17 responses. Journal of Immunology (Baltimore, MD: 1950) 188, 4828–4837.Google Scholar
Khalil, E. A. G., Musa, A. M., Modabber, F. and El-Hassan, A. M. (2006). Safety and immunogenicity of a candidate vaccine for visceral leishmaniasis (Alum-precipitated autoclaved Leishmania major + BCG) in children: an extended phase II study. Annals of Tropical Paediatrics 26, 357–361.Google Scholar
Leonel, H., Guedes, D. M., Lilian, B., Chaves, S. P., Cláudio, D., Gomes, D. O., Nosanchuk, J. D. and De Simone, S. G. (2014). Intranasal vaccination with extracellular serine proteases of Leishmania amazonensis confers protective immunity to BALB/c mice against infection. Parasites and Vectors 7, 1–7.Google Scholar
Lindenstrøm, T., Agger, E. M., Korsholm, K. S., Darrah, P. A, Aagaard, C., Seder, R. A, Rosenkrands, I. and Andersen, P. (2009). Tuberculosis subunit vaccination provides long-term protective immunity characterized by multifunctional CD4 memory T cells. Journal of Immunology (Baltimore, MD: 1950) 182, 8047–8055.Google Scholar
Majumder, S., Bhattacharjee, A., Chowdhury, B. P., Majumdar, S. B. and Majumdar, S. (2014). Antigen-pulsed CpG-ODN-activated dendritic cells induce host-protective immune response by regulating the T regulatory cell functioning in Leishmania donovani-infected mice: critical role of CXCL10. Frontiers in Immunology 5, 1–9.Google Scholar
Marques-Da-Silva, E. A., Coelho, E. A. F., Gomes, D. C. O., Vilela, M. C., Masioli, C. Z., Tavares, C. A. P., Fernandes, A. P., Afonso, L. C. C. and Rezende, S. A. (2005). Intramuscular immunization with p36(LACK) DNA vaccine induces IFN-γ production but does not protect BALB/c mice against Leishmania chagasi intravenous challenge. Parasitology Research 98, 67–74.Google Scholar
Martel, C. J. M., Agger, E. M., Poulsen, J. J., Jensen, T. H., Andresen, L., Christensen, D., Nielsen, L. P., Blixenkrone-Møller, M., Andersen, P. and Aasted, B. (2011). CAF01 potentiates immune responses and efficacy of an inactivated influenza vaccine in ferrets. PLoS ONE 6, e22891.Google Scholar
Mayrink, W., Dos Santos, G. C., Peixoto De Toledo, V. D. P. C., Dabés Guimarães, T. M. P., Lins Machado-Coelho, G. L., Genaro, O. and Da Costa, C. A. (2002). Vaccination of C57BL/10 mice against cutaneous leishmaniasis using killed promastigotes of different strains and species of Leishmania . Revista da Sociedade Brasileira de Medicina Tropical 35, 125–132.Google Scholar
Melby, P. C., Yang, J., Zhao, W., Perez, L. E. and Cheng, J. (2001). Leishmania donovani p36(LACK) DNA vaccine is highly immunogenic but not protective against experimental visceral leishmaniasis. Infection and Immunity 69, 4719–4725.CrossRefGoogle Scholar
Mestecky, J., Moldoveanu, Z. and Elson, C. O. (2005). Immune response versus mucosal tolerance to mucosally administered antigens. Vaccine 23, 1800–1803.Google Scholar
Nico, D., Gomes, D. C., Alves-Silva, M. V., Freitas, E. O., Morrot, A., Bahia, D., Palatnik, M., Rodrigues, M. M. and Palatnik-de-Sousa, C. B. (2014). Cross-protective immunity to Leishmania amazonensis is mediated by CD4+ and CD8+ epitopes of Leishmania donovani nucleoside hydrolase terminal domains. Frontiers in Immunology 5, 1–5.Google Scholar
Oliveira, D. M., Costa, M. A. F., Chavez-Fumagalli, M. A., Valadares, D. G., Duarte, M. C., Costa, L. E., Martins, V. T., Gomes, R. F., Melo, M. N., Soto, M., Tavares, C. A. P. and Coelho, E. A. F. (2012). Evaluation of parasitological and immunological parameters of Leishmania chagasi infection in BALB/c mice using different doses and routes of inoculation of parasites. Parasitology Research 110, 1277–1285.Google Scholar
Olsen, A. W., Theisen, M., Christensen, D., Follmann, F. and Andersen, P. (2010). Protection against chlamydia promoted by a subunit vaccine (CTH1) compared with a primary intranasal infection in a mouse genital challenge model. PLoS ONE 5, e10768.Google Scholar
Pereira, B. A. and Alves, C. R. (2008). Immunological characteristics of experimental murine infection with Leishmania (Leishmania) amazonensis . Veterinary Parasitology 158, 239–255.Google Scholar
Pinheiro, R. O., Pinto, E. F., Lopes, J. R. C., Guedes, H. L. M., Fentanes, R. F. and Rossi-Bergmann, B. (2005). TGF-β-associated enhanced susceptibility to leishmaniasis following intramuscular vaccination of mice with Leishmania amazonensis antigens. Microbes and Infection 7, 1317–1323.Google Scholar
Pinheiro, R. O., Pinto, E. F., de Matos Guedes, H. L., Filho, O. A. A., de Mattos, K. A., Saraiva, E. M., de Mendonça, S. C. F. and Rossi-Bergmann, B. (2007). Protection against cutaneous leishmaniasis by intranasal vaccination with lipophosphoglycan. Vaccine 25, 2716–2722.Google Scholar
Pinto, E. F., De Mello Cortezia, M. and Rossi-Bergmann, B. (2003). Interferon-gamma-inducing oral vaccination with Leishmania amazonensis antigens protects BALB/c and C57BL/6 mice against cutaneous leishmaniasis. Vaccine 21, 3534–3541.Google Scholar
Pinto, E. F., Pinheiro, R. O., Rayol, A., Larraga, V. and Rossi-Bergmann, B. (2004). Intranasal vaccination against cutaneous leishmaniasis with a particulated leishmanial antigen or DNA encoding LACK. Infection and Immunity 72, 4521–4527.Google Scholar
Pinto, V. V., Salanti, A., Joergensen, L. M., Dahlbäck, M., Resende, M., Ditlev, S. B., Agger, E. M., Arnot, D. E., Theander, T. G. and Nielsen, M. A. (2012). The effect of adjuvants on the immune response induced by a DBL4e{open}-ID4 VAR2CSA based Plasmodium falciparum vaccine against placental malaria. Vaccine 30, 572–579.Google Scholar
Rosenkrands, I., Vingsbo-Lundberg, C., Bundgaard, T. J., Lindenstrøm, T., Enouf, V., van der Werf, S., Andersen, P. and Agger, E. M. (2011). Enhanced humoral and cell-mediated immune responses after immunization with trivalent influenza vaccine adjuvanted with cationic liposomes. Vaccine 29, 6283–6291.CrossRefGoogle ScholarPubMed
Sánchez-Sampedro, L., Gómez, C. E., Mejías-Pérez, E., Sorzano, C. O. and Esteban, M. (2012). High quality long-term CD4+ and CD8+ effector memory populations stimulated by DNA-LACK/MVA-LACK regimen in Leishmania major BALB/C model of infection. PLoS ONE 7, e38859.Google Scholar
Singh, O. P. and Sundar, S. (2014). Immunotherapy and targeted therapies in treatment of visceral leishmaniasis: current status and future prospects. Frontiers in Immunology 5, 1–9.Google Scholar
Srivastava, J. K., Misra, A., Sharma, P., Srivastava, B., Naik, S. and Dube, A. (2003). Prophylactic potential of autoclaved Leishmania donovani with BCG against experimental visceral leishmaniasis. Parasitology 127, 107–114.Google Scholar
Takagi, H., Hiroi, T., Yang, L., Tada, Y., Yuki, Y., Takamura, K., Ishimitsu, R., Kawauchi, H., Kiyono, H. and Takaiwa, F. (2005). A rice-based edible vaccine expressing multiple T cell epitopes induces oral tolerance for inhibition of Th2-mediated IgE responses. Proceedings of the National Academy of Sciences of the United States of America 102, 17525–17530.Google Scholar
Van Dissel, J. T., Joosten, S. A., Hoff, S. T., Soonawala, D., Prins, C., Hokey, D. A., O'Dee, D. M., Graves, A., Thierry-Carstensen, B., Andreasen, L. V., Ruhwald, M., de Visser, A. W., Agger, E. M., Ottenhoff, T. H. M., Kromann, I. and Andersen, P. (2014). A novel liposomal adjuvant system, CAF01, promotes long-lived Mycobacterium tuberculosis-specific T-cell responses in human. Vaccine 32, 7098–7107.Google Scholar
Wahid, R., Fresnay, S., Levine, M. M. and Sztein, M. B. (2015). Immunization with Ty21a live oral typhoid vaccine elicits crossreactive multifunctional CD8+ T-cell responses against Salmonella enterica serovar Typhi, S. Paratyphi A, and S. Paratyphi B in humans. Mucosal Immunology 1–11. doi:10.1038/mi.2015.24.Google Scholar
World Health Organization (2010). Control of the leishmaniases. World Health Organization Technical Report Series 949, 1–186.Google Scholar
Yadav, A., Amit, A., Chaudhary, R., Chandel, A. S., Mahantesh, V., Suman, S. S., Singh, S. K., Dikhit, M. R., Ali, V., Rabidas, V., Pandey, K., Kumar, A., Das, P. and Bimal, S. (2015). Leishmania donovani: impairment of the cellular immune response against recombinant ornithine decarboxylase protein as a possible evasion strategy of Leishmania in visceral leishmaniasis. International Journal for Parasitology 45, 33–42.Google Scholar