Interleukin 10-dominant immune response and increased risk of cutaneous leishmaniasis after natural exposure to Lutzomyia intermedia sand flies

Journal of Infectious Diseases

Volumn 212, Issue 1, 2015, Pages 157-165

  Carvalho, Augusto M ^a   Cristal, Juqueline R ^a   Muniz, Aline C ^b   Carvalho, Lucas P ^b,c   Gomes, Regis ^a   Miranda, Jose C ^a   Barral, Aldina ^a,d   Carvalho, Edgar M ^b,c   De Oliveira, Camila I ^a,d  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b FEDERAL UNIVERSITY OF BAHIA   (Brazil)

^c Inst Nacional de Ciência e Tecnologia em Doenças Tropicais   (Brazil)

^d Instituto de Investigac o em Imunologia   (Brazil)

Author keywords

chemokines; cutaneous leishmaniasis; cytokines; ELISA; killing assay.; L. braziliensis; lutzomyia intermedia; Sand fly saliva

Indexed keywords

CXCL9 CHEMOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G4 ANTIBODY; INTERLEUKIN 10; INTERLEUKIN 13; MONOCYTE CHEMOTACTIC PROTEIN 1; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; ANTIBODY; CYTOKINE; IMMUNOGLOBULIN G;

ADOLESCENT; ADULT; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CELLULAR IMMUNITY; CHILD; COCULTURE; COHORT ANALYSIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDEMIC DISEASE; ENVIRONMENTAL EXPOSURE; FEMALE; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMAGO; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOPATHOGENESIS; IN VITRO STUDY; INFECTION RISK; INFECTION SENSITIVITY; LEISHMANIA BRAZILIENSIS; LUTZOMYIA; LUTZOMYIA INTERMEDIA; LYMPHOCYTE; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; NONHUMAN; PARASITE DEVELOPMENT; PARASITE SURVIVAL; PRIORITY JOURNAL; PROSPECTIVE STUDY; SALIVA; SALIVARY GLAND; SKIN LEISHMANIASIS; ANIMAL; BLOOD; CD4+ T LYMPHOCYTE; DISEASE PREDISPOSITION; IMMUNOLOGY; ISOLATION AND PURIFICATION; LEISHMANIASIS, CUTANEOUS; MIDDLE AGED; PRESCHOOL CHILD; PSYCHODIDAE; RISK ASSESSMENT; SECRETION (PROCESS); YOUNG ADULT;

ADOLESCENT; ADULT; ANIMALS; ANTIBODIES; CD4-POSITIVE T-LYMPHOCYTES; CHILD; CHILD, PRESCHOOL; COHORT STUDIES; CYTOKINES; DISEASE SUSCEPTIBILITY; FEMALE; HUMANS; IMMUNOGLOBULIN G; INTERLEUKIN-10; LEISHMANIA BRAZILIENSIS; LEISHMANIASIS, CUTANEOUS; MALE; MIDDLE AGED; PROSPECTIVE STUDIES; PSYCHODIDAE; RISK ASSESSMENT; SALIVA; YOUNG ADULT;

EID: 84936773726     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiv020     Document Type: Article

References (40)

1. Gomes R, Oliveira F. The immune response to sand fly salivary proteins and its influence on Leishmania immunity. Front Immunol 2012; 3:110.
2. Titus RG, Ribeiro JM. Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 1988; 239: 1306-8.
3. Belkaid Y, Kamhawi S, Modi G, et al. Development of a natural model of cutaneous leishmaniasis: powerful effects of vector saliva and saliva preexposure on the long-term outcome of Leishmania major infection in the mouse ear dermis. J Exp Med 1998; 188:1941-53.
4. Kamhawi S, Belkaid Y, Modi G, Rowton E, Sacks D. Protection against cutaneous leishmaniasis resulting from bites of uninfected sand flies. Science 2000; 290:1351-4.
5. Valenzuela JG, Belkaid Y, Garfield MK, et al. Toward a defined anti-Leishmania vaccine targeting vector antigens: characterization of a protective salivary protein. J Exp Med 2001; 194:331-42.
6. Gomes R, Teixeira C, Teixeira MJ, 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 USA 2008; 105: 7845-50.
7. Gomes RB, Brodskyn C, de Oliveira CI, et al. Seroconversion against Lutzomyia longipalpis saliva concurrent with the development of anti-Leishmania chagasi delayed-type hypersensitivity. J Infect Dis 2002; 186:1530-4.
8. Aquino DM, Caldas AJ, Miranda JC, Silva AA, Barral-Netto M, Barral A. Epidemiological study of the association between anti-Lutzomyia longipalpis saliva antibodies and development of delayed-type hypersensitivity to Leishmania antigen. Am J Trop Med Hyg 2010; 83:825-7.
9. Vinhas V, Andrade BB, Paes F, et al. Human anti-saliva immune response following experimental exposure to the visceral leishmaniasis vector, Lutzomyia longipalpis. Eur J Immunol 2007; 37:3111-21.
10. Abdeladhim M, Ben Ahmed M, Marzouki S, et al. 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 Negl Trop Dis 2011; 5:e1345.
11. Llanos Cuentas EA, Cuba CC, Barreto AC, Marsden PD. Clinical characteristics of human Leishmania braziliensis braziliensis infections. Trans R Soc Trop Med Hyg 1984; 78:845-6.
12. Turetz ML, Machado PR, Ko AI, et al. Disseminated leishmaniasis: a new and emerging form of leishmaniasis observed in northeastern Brazil. J Infect Dis 2002; 186:1829-34.
13. de Moura TR, Oliveira F, Novais FO, et al. Enhanced Leishmania braziliensis infection following pre-exposure to sandfly saliva. PLoS Negl Trop Dis 2007; 1:e84.
14. de Moura TR, Oliveira F, Rodrigues GC, et al. Immunity to Lutzomyia intermedia saliva modulates the inflammatory environment induced by Leishmania braziliensis. PLoS Negl Trop Dis 2010; 4:e712.
15. Schnorr D, Muniz AC, Passos S, et al. IFN-? production to leishmania antigen supplements the leishmania skin test in identifying exposure to L. braziliensis infection. PLoS Negl Trop Dis 2012; 6:e1947.
16. de Moura TR, Novais FO, Oliveira F, et al. Toward a novel experimental model of infection to study American cutaneous leishmaniasis caused by Leishmania braziliensis. Infect Immun 2005; 73:5827-34.
17. Rohousova I, Ozensoy S, Ozbel Y, Volf P. Detection of species-specific antibody response of humans and mice bitten by sand flies. Parasitology 2005; 130:493-9.
18. Souza NA, Andrade-Coelho CA, Peixoto AA, Rangel EF. Nocturnal activity rhythms of Lutzomyia intermedia and Lutzomyia whitmani (Diptera: Psychodidae) in a transmission area of American cutaneous leishmaniasis in Rio de Janeiro State, Brazil. J Med Entomol 2005; 42:986-92.
19. Marzouki S, Ben Ahmed M, Boussoffara T, et al. Characterization of the antibody response to the saliva of Phlebotomus papatasi in people living in endemic areas of cutaneous leishmaniasis. Am J Trop Med Hyg 2011; 84:653-61.
20. Peng Z, Beckett AN, Engler RJ, Hoffman DR, Ott NL, Simons FE. Immune responses to mosquito saliva in 14 individuals with acute systemic allergic reactions to mosquito bites. J Allergy Clin Immunol 2004; 114:1189-94.
21. Souza AP, Andrade BB, Aquino D, et al. Using recombinant proteins from Lutzomyia longipalpis saliva to estimate human vector exposure in visceral leishmaniasis endemic areas. PLoS Negl Trop Dis 2010; 4: e649.
22. Teixeira C, Gomes R, Collin N, et al. Discovery of markers of exposure specific to bites of Lutzomyia longipalpis, the vector of Leishmania infantum chagasi in Latin America. PLoS Negl Trop Dis 2010; 4:e638.
23. Ribeiro JM, Katz O, Pannell LK, Waitumbi J, Warburg A. Salivary glands of the sand fly Phlebotomus papatasi contain pharmacologically active amounts of adenosine and 5?-AMP. J Exp Biol 1999; 202:1551-9.
24. Katz O, Waitumbi JN, Zer R, Warburg A. Adenosine, AMP, and protein phosphatase activity in sandfly saliva. Am J Trop Med Hyg 2000; 62:145-50.
25. Hasko G, Szabo C, Nemeth ZH, Kvetan V, Pastores SM, Vizi ES. Adenosine receptor agonists differentially regulate IL-10, TNF-?, and nitric oxide production in RAW 264.7 macrophages and in endotoxemic mice. J Immunol 1996; 157:4634-40.
26. Hasko G, Kuhel DG, Chen JF, et al. Adenosine inhibits IL-12 and TNF-? production via adenosine A2a receptor-dependent and independent mechanisms. FASEB J 2000; 14:2065-74.
27. Oliveira F, Traore B, Gomes R, et al. Delayed-type hypersensitivity to sand fly saliva in humans from a leishmaniasis-endemic area of Mali is Th1-mediated and persists to midlife. J Invest Dermatol 2013; 133: 452-9.
28. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003; 299:1057-61.
29. Asseman C, Mauze S, Leach MW, Coffman RL, Powrie F. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J Exp Med 1999; 190:995-1004.
30. Campanelli AP, Roselino AM, Cavassani KA, et al. CD4+CD25+ T cells in skin lesions of patients with cutaneous leishmaniasis exhibit phenotypic and functional characteristics of natural regulatory T cells. J Infect Dis 2006; 193:1313-22.
31. Costa DL, Guimaraes LH, Cardoso TM, et al. Characterization of regulatory T cell (Treg) function in patients infected with Leishmania braziliensis. Hum Immunol 2013; 74:1491-500.
32. Battaglia M, Gregori S, Bacchetta R, Roncarolo MG. Tr1 cells: from discovery to their clinical application. Semin Immunol 2006; 18:120-7.
33. Pot C, Jin H, Awasthi A, et al. Cutting edge: IL-27 induces the transcription factor c-Maf, cytokine IL-21, and the costimulatory receptor ICOS that coordinately act together to promote differentiation of IL-10-producing Tr1 cells. J Immunol 2009; 183:797-801.
34. Satoguina JS, Weyand E, Larbi J, Hoerauf A. T regulatory-1 cells induce IgG4 production by B cells: role of IL-10. J Immunol 2005; 174: 4718-26.
35. van der Zee JS, van Swieten P, Aalberse RC. Inhibition of complement activation by IgG4 antibodies. Clin Exp Immunol 1986; 64:415-22.
36. Weinkopff T, de Oliveira CI, de Carvalho AM, et al. Repeated exposure to Lutzomyia intermedia sand fly saliva induces local expression of interferon-inducible genes both at the site of injection in mice and in human blood. PLoS Negl Trop Dis 2014; 8:e2627.
37. Ritter U, Korner H. Divergent expression of inflammatory dermal chemokines in cutaneous leishmaniasis. Parasite Immunol 2002; 24: 295-301.
38. Teixeira CR, Teixeira MJ, Gomes RB, et al. Saliva from Lutzomyia longipalpis induces CC chemokine ligand 2/monocyte chemoattractant protein-1 expression and macrophage recruitment. J Immunol 2005; 175:8346-53.
39. Barral A, Honda E, Caldas A, et al. Human immune response to sand fly salivary gland antigens: a useful epidemiological marker? Am J Trop Med Hyg 2000; 62:740-5.
40. Collin N, Gomes R, Teixeira C, et al. Sand fly salivary proteins induce strong cellular immunity in a natural reservoir of visceral leishmaniasis with adverse consequences for Leishmania. PLoS Pathog 2009; 5: e1000441.