Immunomodulating effects of Phlebotomine saliva in Leishmania infection: Review

Authors

  • Ivan Brito Feitosa Institute of Biophysics Carlos Chagas Filho - UFRJ Oswaldo Cruz Foundation, Fiocruz - RO.
  • Wesley Roberto de Aguida Fundação Oswaldo Cruz, Fiocruz Noroeste
  • Carolina Bioni Garcia Teles Fundação Oswaldo Cruz, Fiocruz Noroeste

DOI:

https://doi.org/10.12741/ebrasilis.v11i3.776

Keywords:

Leishmania, Lutzomyia, Phlebotomus, sandflies, saliva, protection, flebótomos, proteção

Abstract

Abstract. The recognized action of some proteins present in the saliva of the phlebotomine dipteran vectors of Leishmaniasis, as modulators of the hemostatic, inflammatory and immune responses during the colonization of the protozoan in the host organism, created the expectation of formulating a vaccine against this disease. The present study aimed to provide an overview about researchs that deals with the role of phlebotomine saliva in Leishmania infections. A bibliographic search was carried out in PubMed, SciELO and LILACS databases. The articles listed address the following aspects of the vector’s saliva: intensification of infection; suppression and modulation of the host immune system; chemotaxis on phagocytic cells; induction of innate and adaptive immunity; isolation and characterization of immunoactive molecules and their possible protective function against Leishmaniasis.

Efeitos imunomoduladores da saliva de flebotomínio na infecção por Leishmania: Revisão

Resumo. A reconhecida ação de algumas proteínas presentes na saliva dos vetores flebotomíneos da Leishmaniose, como moduladores das respostas hemostáticas, inflamatórias e imunes durante a colonização do protozoário no organismo hospedeiro, criou a expectativa de formular uma vacina contra essa doença. O presente estudo teve como objetivo fornecer uma visão geral sobre pesquisas que abordam o papel da saliva de flebotomíneos em infecções por Leishmania. Foi realizada uma pesquisa bibliográfica nas bases de dados PubMed, SciELO e LILACS. Os artigos listados abordam os seguintes aspectos da saliva do vetor: intensificação da infecção; supressão e modulação do sistema imune do hospedeiro; quimiotaxia em células fagociticas; indução da imunidade inata e adaptativa; isolamento e caracterização de moléculas imunoativas e sua possível função protetora contra a leishmaniose.

References

Abdeladhim, M., A.M. Ben, S. Marzouki, H.N. Belhadj, T. Boussoffara, A.N. Belhaj, S.A. Ben & H. Louzir H. 2011. Human cellular immune response to the saliva of Phlebotomus papatasi is mediated by IL-10-producing CD8+ T cells and Th1- polarized CD4+ lymphocytes. PLoS Neglected Tropical Diseases, 5: e1345. DOI: https://doi.org/10.1371/journal.pntd.0001345.

Abdeladhim, M., Kamhawi S., & J.G. Valenzuela, 2014. What

Andrade, B.B., C.R. Teixeira, A. Barral & M. Barral-Netto, 2005. Haematophagous arthropod saliva and host defense system: a tale of tear and blood. Anais da Academia Brasileira de Ci

Ara

Asojo, O.A., A. Kelleher, Z. Liu, J. Pollet, E.M. Hudspeth, W.C. Rezende, M.J. Groen, C.A. Seid, M. Abdladhim, S. Townsend, W. De Castro, A. Mendes-Sousa, D.C. Bartholomeu, R.T. Fujiwara, M.E. Bottazzi, P.J. Hotez, B. Zhan, F. Oliveira, S. Kamhawi & J.G. Valenzuela, 2017. Structure of SALO, a leishmaniasis vaccine candidate from the sand fly Lutzomya longipalpis. PLoS Neglected Tropical Diseases, 11: e0005374. DOI: https://doi.org/10.1371/journal.pntd.0005374.

Bhattacharya, P., S. Ghosh & S.A. Ejazi, 2016. Induction of IL-10 and TGF? from CD4+CD25+FoxP3+ T Cells Correlates with Parasite Load in Indian Kala-azar Patients Infected with Leishmania donovani. Bates PA, ed. PLoS Neglected Tropical Diseases, 10: e0004422. DOI: https://doi.org/10.1371/journal.pntd.0004422.

Bhattachrjee, A., S. Majumder, S. Das & S. Ghosh, 2016. Leishmania donovani induced PGE2 generation is critically dependent on host TLR2-cPLA2 signaling. Infection and Immunity. 84 : 2963-2973. DOI: https://doi.org/10.1128/iai.00528-16.

Brodie, T.M., M.C. Smith, R.V. Morris, & R.G. Titus, 2007. Immunomodulatory effects of the Lutzomyia longipalpis salivary gland protein maxadilan on mouse macrophages. Infection and Immunity, 75: 2359-2365, DOI: https://doi.org/10.1128/iai.01812-06.

Carregaro, V., J.M. Ribeiro, J.G. Valenzuela, D.L. Souza-J

Cavalcante, R.R., M.H. Pereira & N.F. Gontijo, 2003. Anti-complement activity in the saliva of phlebotomine sand flies and other haematophagous insects. Parasitology, 127: 87-93. DOI: https://doi.org/10.1017/s0031182003003329.

Collin, N., R. Gomes, C. Teixeira, L. Cheng, A. Laughinghouse, J.M. Ward, D.E. Elnaiem, L. Fischer, J.G. Valenzuela & S. Kamhawi 2009. Sand fly salivary proteins induce strong cellular immunity in a natural reservoir of visceral leishmaniasis with adverse consequences for Leishmania. PLoS Pathogens. 5: e1000441. DOI: https://doi.org/10.1371/journal.ppat.1000441.

Control of the Leishmaniasis: report of a meeting of the

Costa, D.J., C. Favali , J. Clarencio, L. Afonso, V. Conceicao, J.C. Miranda, R.G. Titus , J. Valenzuela, M. Barral-Netto , A.Barral & C.I. Brodskyn, 2004. Lutzomyia longipalpis salivary gland homogenate impairs cytokine production and costimulatory molecule expression on human monocytes and dendritic cells. Infection and Immunity, 72: 1298-1305. DOI: https://doi.org/10.1128/iai.72.3.1298-1305.2004.

De Paula, C.D.R., J.H.D. Sampaio, D.R. Cardoso & R.N.R. Sampaio, 2003. Estudo comparativo da efic

Delves, P.J. & I.M. Roitt, 2000. The immune system. First of two parts. New England Journal of Medicine, 343: 37-49. DOI: https://doi.org/10.1056/nejm200007063430107.

Descoteaux, A. & S.J. Turco, 1993. The lipophosphoglycan of Leishmania and macrophage protein kinase C. Parasitology Today, 9: 468-471. DOI: https://doi.org/10.1016/0169-4758(93)90105-o.

Elnaiem, D.-E.A., C. Meneses, M. Slotman & G. Lanzaro, C. 2005. Genetic variation in the sand fly salivary protein, SP-15, a potential vaccine candidate against Leishmania major. Insect Molecular Biology, 14: 145-150. DOI: https://doi.org/10.1111/j.1365-2583.2004.00539.x.

Enserink, M., 2001. Infecton Sand fly saliva may be key to new vaccine. Science. 293: 1028

Ferreira, V.P., V. Fazito Vale, M.K. Pangburn, M. Abdeladhim, A.F. Mendes-Sousa, I.V. Coutinho-Abreu, M. Rasouli, E.A. Brandt, C. Meneses, K.F. Lima, R. Nascimento Ara

Gazzinelli, R.T. & E.Y. Denkerst, 2006. Protozoan encounters with toll-like receptor signalling pathways: implications for host parasitism. Nature Reviews Immunology, 6: 895-906. DOI: https://doi.org/10.1038/nri1978.

Gomes, R., F. Oliveira, C. Teixeira, C. Meneses, D.C. Gilmore, D.E. Elnaiem, S. Kamhawi & J.G. Valenzuela. 2012. Immunity to sand fly salivary protein LJM11 modulates host response to vector-transmitted Leishmania conferring ulcer-free protection. Journal of Investigative Dermatology, 132: 2735-2743. DOI: https://doi.org/10.1038/jid.2012.205.

Green, S.J. & C.A. Nacy, 1993. Antimicrobial and immunopathologic effects of cytokine-induced nitric oxide synthesis. Current Opinion in Infectious Diseases, 6: 384-396.

Harris, S.G., J. Padilla, L. Koumas, D. Ray & R.P. Phipps, 2002. Prostaglandins as modulators of immunity. Trends in Immunology 23: 144-150. DOI: https://doi.org/10.1016/s1471-4906(01)02154-8.

Health Organization, 2010.

Hermoso, T., Z. Fishelson, S.L. Becker, K. Hirscheberg & C.L. Jaffe, 1991. Leishmanial protein kinases phosphorylate components of the complement cascade. EMBO Journal, 10: 4061-4067. DOI: https://doi.org/10.1002/j.1460-2075.1991.tb04982.x.

Hostomsk

Hostomska J., I. Rohousova, V. Volfova, D. Stanneck, N. Mencke & P. Volf. 2008. Kinetics of canine antibody response to saliva of the sand fly Lutzomyia longipalpis. Vector-Borne and Zoonotic Diseases. 8: 443-450. DOI: https://doi.org/10.1089/vbz.2007.0214.

Kamhawi, S., Y. Belkaid, G. Modi, E. Rowton & D. Sacks, 2000. Protection against cutaneous leishmaniasis resulting from bites of uninfected sand flies. Science. 290: 1351-1354. DOI: https://doi.org/10.1126/science.290.5495.1351.

Kariminia, A., E. Bourreau, H. Pascalis, P. Couppie, D. Sainte-Marie, F. Tacchini-Cottier & P. Launois 2005. Transforming growth factor beta 1 production by CD4(+) CD25(+) regulatory T cells in peripheral blood mononuclear cells from healthy subjects stimulated with Leishmania guyanensis. Infection and Immunity, 73: 5908-5914. DOI: https://doi.org/10.1128/iai.73.9.5908-5914.2005.

Laurenti, M.D., V.L.R. Matta, T. Pernichelli, N.F.C. Secundino, L.C. Pinto, C.E.P. Corbett & P.P.F. Pimenta, 2009. Effects of salivary gland homogenate from wild-caught and laboratory-reared Lutzomyia longipalpis on the evolution and immunomodulation of Leishmania (Leishmania) amazonensis infection. Scandinavian Journal of Immunology. 70: 389-95. DOI: https://doi.org/10.1111/j.1365-3083.2009.02310.x.

Lerner, E.A., Ribeiro, J.M., Nelson, R.J. & M.R. Lerner, 1991. Isolation of maxadilan, a potent vasodilatory peptide from the salivary glands of the sand fly Lutzomyia longipalpis. Journal of Biological Chemistry. 266: 11234-11236.

Lestinova, T., M. Vlkova, J. Votypka, P. Volf & I. Rohousova, 2015. Phlebotomus papatasi exposure cross-protects mice against Leishmania major co-inoculated with Phlebotomus duboscqi salivary gland homogenate. Acta Tropica, 144: 9-18. DOI: https://doi.org/10.1016/j.actatropica.2015.01.005.

Menezes, M., D.J. Costa, J. Clar

Monteiro, M. C., H.C. Lima, A.A.A. Souza, R.G. Titus, P.R.T. Rom

Moura, T.R., F. Oliveira, F.O. Novais, J.C. Miranda, J. Clar

Mukbel, R.M., R.H. Khasharmeh, N.S. Hijjawi, M.S. Khalifeh, M.M. Hatmal & M.A. McDowell. 2016. Human immune response to salivary proteins of wild-caught Phlebotomus papatasi. Parasitology Research, 115: 3345-3355. DOI https://doi.org/10.1007/s00436-016-5094-2.

Norsworthy, N. B., J. Sun, D. Elnaiem, G. Lanzaro & L. Soong, 2004. Sand Fly Saliva Enhances Leishmania amazonensis Infection by Modulating Interleukin-10 Production. Infection and Immunity, 72: 1240-1247. DOI: https://doi.org/10.1128/iai.72.3.1240-1247.2004.

Oliveira, F., Rowton, E., H. Aslan, R. Gomes, P.A. Castrovinci, P.H. Alvarenga, M. Abdeladhim, C. Teixeira, C. Meneses, L.T. Kleeman, A.B. Guimaraes-Costa, T.E. Rowland, D. Gilmore, S. Doumbia, S.G. Reed, P.G. Lawyer, J.F. Andersen, S. Kamhawi & J.G. Valenzuela, 2015. A sand fly salivary protein vaccine shows efficacy against vector-transmitted cutaneous leishmaniasis in nonhuman primates. Science Translational Medicine, 7: 290ra90. DOI: https://doi.org/10.1126/scitranslmed.aaa3043.

Oliveira, F., B. Traor

Peters-Golden, M., C. Canetti, P. Mancuso, M.J. Coffey, 2005. Leukotrienes: underappreciated mediators of innate immune responses. Journal of Immunology,174: 589-594. DOI: https://doi.org/10.4049/jimmunol.174.2.589.

Pushpanjali, A.K.T., B. Purkait, F. Jamal, M.K. Singh, G. Ahmed, S. Bimal, V. Kumar, S.K. Singh, S. Keshri, P. Das & S. Narayan, 2016. Direct evidence for role of anti-saliva antibodies against salivary gland homogenate of P. argentipes in modulation of protective Th1-immune response against Leishmania donavani. Cytokine. 86: 79-85. DOI: https://doi.org/10.1016/j.cyto.2016.07.017.

Ribeiro, J., R. Charlab, E. Rowton & E. Cupp, 2000. Simulium vittatum (Diptera: Simuliidae) and Lutzomyia longipalpis (Diptera: Psychodidae) salivary gland hyaluronidase activity. Journal Medical Entomology, 37: 743-747. DOI: https://doi.org/10.1603/0022-2585-37.5.743.

Rittig, M.G. & R.G. Bogdan, 2000. Leishmania

Rogerio, A.P. & F.F. Anibal, 2012. Role of leukotrienes on protozoan and helminth infections. Mediators of inflammation, 2012: 595694. DOI: https://doi.org/10.1155/2012/595694.

Rogers, K.A. & R.G. Titus, 2003. Immunomodulatory effects of maxadilan and Phlebotomus papatasi sand fly salivary gland lysates on human primary in vitro immune responses. Parasite Immunology, 25: 127-134. DOI: https://doi.org/10.1046/j.1365-3024.2003.00623.x.

Rohous?ov

Semini, V., T. Aebischer, 2018 Phagosome proteomics to study Leishmania

Silva, R.A.A., N.M. Tavares, D. Costa, M. Pitombo, L. Barbosa, K. Fukutani, J.C. Miranda, C.I. Oliveira, J.G. Valenzuela, A. Barral, M. Soto, M. Barral-Netto & C. Brodskyn, 2011. DNA vaccination with KMP11 and Lutzomyia longipalpis salivary protein protects hamsters against visceral leishmaniasis. Acta Tropica, 120: 185-90. DOI: https://doi.org/10.1016/j.actatropica.2011.08.007.

Bozza, M, M.B.P. Soares, P.T. Bozza, A.R. Satoskar, T.G. Diacovo, F. Brombacher, R.G. Titus, C.B. Shoemaker & J.R. David. 1998. The PACAP-type I receptor agonist maxadilan from sand fly saliva protects mice against lethal endotoxemia by a mechanism partially dependent on IL-10. European Journal of Immunology, 28: 3120-3127. DOI: https://doi.org/10.1002/(sici)1521-4141(199810)28:10%3C3120::aid-immu3120%3E3.0.co;2-3.

Svensjo, E., E.M. Saraiva, R.S. Amendola, C. Barja-Fidalgo, M.T. Bozza, E.A. Lerner, M.M. Teixeira & J. Scharfstein, 2012. Maxadilan, the Lutzomyia longipalpis vasodilator, drives plasma leakage via PAC1

Teixeira, C., R. Gomes, N. Collin, D. Reynoso, R. Jochim, F. Oliveira, A. Seitz, D.E. Elnaiem, A. Caldas, A.P. de Souza, C.I. Brodskyn, C.I. de Oliveira, I. Mendonca, C.H. Costa, P. Volf, A. Barral, S. Kamhawi & J.G. Valenzuela, 2010. Discovery of markers of exposure specific to bites of Lutzomyia longipalpis, the vector of Leishmania infantum chagasi in Latin America. PLoS Neglected Tropical Diseases, 4: e638. DOI: https://doi.org/10.1371/journal.pntd.0000638.

Titus, R.G. & J.M.C. Ribeiro, 1988. Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science, 239: 1306-1308. DOI: https://doi.org/10.1126/science.3344436.

Valenzuela, J.G., Y. Belkaid, M.K. Garfield, S. Mendez, S. Kamhawi, E.D. Rowton, D.L. Sacks & J.L Ribeiro, 2001. Toward a defined anti- Leishmania vaccine targeting vector antigens: characterization of a protective salivary protein. The Journal of Experimental Medicine, 194: 331-342. DOI: https://doi.org/10.1084/jem.194.3.331.

Van der Auwera, G. & J.C. Dujardin, 2015. Species Typing in Dermal Leishmaniasis. Clinical Microbiology Reviews, 28: 265-294. DOI: https://doi.org/10.1128/cmr.00104-14.

Verma, S. A. Mandal, Md. Y. Ansari, A. Kumar, K. Abhishek, A.K. Ghosh, A. Kumar, V. Kumar, S. Das, P. Das, 2018. P.Leishmania donovani Inhibitor of Serine Peptidases 2 Mediated Inhibition of Lectin Pathway and Upregulation of C5aR Signaling Promote Parasite Survival inside Host. Frontiers in Immunology, 9: 63. DOI: https://doi.org/10.3389/fimmu.2018.00063.

Vinhas, V., B.B. Andrade, F. Paes, A. Bomura, J. Clarencio, J.C. Miranda, A. B

Wheat, W.H., K.E. Pauken, R.V. Morris, R.G. Titus, 2008. Lutzomyia longipalpis salivary peptide maxadilan alters murine dendritic cell expression of CD80/86, CCR7, and cytokine secretion and reprograms dendritic cell-mediated cytokine release from cultures containing allogeneic T cells. Journal of Immunology, 180: 8286-8298. DOI: https://doi.org/10.4049/jimmunol.180.12.8286.

WHO Expert Committee on the Control of Leishmaniases.

WHO Technical Report Series, No. 949. Geneva: World

XU, X., F. Oliveira, B.W. Chang, N. Collin, R. Gomes, C. Teixeira, D. Reynoso, V. My Pham, D.E. Elnaiem, S. Kamhawi, J.M. Ribeiro, J.G. Valenzuela & J.F. Andersen, 2011. Structure and function of a

Young, D.G. & M.A. Duncan, 1994. Guide to the identification and geographic distribution of Lutzomyia sandflies in Mexico, the West Indies, Central and South America (Diptera: Psychodidae). Defense Technical Information Center, 881p. DOI: https://doi.org/10.21236/ada285737.

Downloads

Published

2018-12-21

How to Cite

[1]
Feitosa, I.B., Aguida, W.R. de and Teles, C.B.G. 2018. Immunomodulating effects of Phlebotomine saliva in Leishmania infection: Review. EntomoBrasilis. 11, 3 (Dec. 2018), 156–161. DOI:https://doi.org/10.12741/ebrasilis.v11i3.776.

Issue

Section

Review