Dual effect of Lutzomyia longipalpis saliva on Leishmania braziliensis infection is mediated by distinct saliva-induced cellular recruitment into BALB/c mice ear

BMC Microbiology

Volumn 13, Issue 1, 2013, Pages

  Carregaro, Vanessa ^a   Costa, Diego Luis ^a   Brodskyn, Claudia ^b,c,d   Barral, Aldina Maria ^b,c,d   Barral Netto, Manuel ^b,c,d   Cunha, Fernando Q ^a   Silva, João Santana ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

^c FEDERAL UNIVERSITY OF BAHIA   (Brazil)

^d Institute of Investigation in Immunology   (Brazil)

Author keywords

Cytokines; Immunoregulation; Inflammatory leucocytes; Leishmania braziliensis; Lutzomyia longipalpis saliva; Phlebotomines saliva

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; TRANSCRIPTION FACTOR FOXP3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; IMMUNOCOMPETENT CELL; INOCULATION; LEISHMANIA BRAZILIENSIS; LEISHMANIA BRAZILIENSIS INFECTION; LEISHMANIASIS; LEUKOCYTE; LUTZOMYIA LONGIPALPIS; MACROPHAGE; MALE; MOUSE; NEUTROPHIL; NONHUMAN; SALIVA; SALIVARY GLAND;

ANIMALS; EAR; INSECT BITES AND STINGS; LEISHMANIA BRAZILIENSIS; LEUKOCYTES; MALE; MICE; MICE, INBRED BALB C; PSYCHODIDAE; SALIVA;

EID: 84878084240     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-13-102     Document Type: Article

References (41)

1. Modification of sand fly biting behavior by Leishmania leads to increased parasite transmission. Beach R, Kiilu G, Leeuwenburg J, AmJTrop Med Hyg 1985 34 2 278 282 (Pubitemid 15085220)
2. Role of saliva in blood-feeding by arthropods. Ribeiro JM, Annu Rev Entomol 1987 32 463 478 10.1146/annurev.en.32.010187.002335 2880553
3. The role of vector saliva in transmission of arthropod-borne disease. Titus RG, Ribeiro JM, Parasitol Today 1990 6 5 157 160 10.1016/0169-4758(90) 90338-5 15463328 (Pubitemid 20137089)
4. Blood-feeding arthropods: live syringes or invertebrate pharmacologists? Ribeiro JM, Infect Agents Dis 1995 4 3 143 152 8548192
5. Phlebotomus papatasi saliva inhibits protein phosphatase activity and nitric oxide production by murine macrophages. Waitumbi J, Warburg A, Infect Immun 1998 66 4 1534 1537 9529078 (Pubitemid 128471515)
6. The immunomodulatory factors of arthropod saliva and the potential for these factors to serve as vaccine targets to prevent pathogen transmission. Titus RG, Bishop JV, Mejia JS, Parasite Immunol 2006 28 4 131 141 16542315
7. Effects of sand fly vector saliva on development of cutaneous lesions and the immune response to Leishmania braziliensis in BALB/c mice. Lima HC, Titus RG, Infect Immun 1996 64 12 5442 5445 8945606 (Pubitemid 26404021)
8. Phlebotomus papatasi sand fly salivary gland lysate down-regulates a Th1, but up-regulates a Th2, response in mice infected with Leishmania major. Mbow ML, Bleyenberg JA, Hall LR, Titus RG, J Immunol 1998 161 10 5571 5577 9820534 (Pubitemid 28519121)
9. 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. Belkaid Y, Kamhawi S, Modi G, Valenzuela J, Noben-Trauth N, Rowton E, Ribeiro J, Sacks DL, J Exp Med 1998 188 10 1941 1953 10.1084/jem.188.10.1941 9815271 (Pubitemid 28536781)
10. The development of effector and memory T cells in cutaneous leishmaniasis: the implications for vaccine development. Scott P, Artis D, Uzonna J, Zaph C, Immunol Rev 2004 201 318 338 10.1111/j.0105-2896.2004.00198.x 15361250 (Pubitemid 39318461)
11. Re-examination of the immunosuppressive mechanisms mediating non-cure of Leishmania infection in mice. Sacks D, Anderson C, Immunol Rev 2004 201 225 238 10.1111/j.0105-2896.2004.00185.x 15361244 (Pubitemid 39318455)
12. Indomethacin treatment slows disease progression and enhances a Th1 response in susceptible BALB/c mice infected with Leishmania major. De Freitas LA, Mbow LM, Estay M, Bleyenberg JA, Titus RG, Parasite Immunol 1999 21 5 273 277 10.1046/j.1365-3024.1999.00211.x 10320625 (Pubitemid 29199816)
13. Phlebotomine salivas inhibit immune inflammation-induced neutrophil migration via an autocrine DC-derived PGE2/IL-10 sequential pathway. Carregaro V, Valenzuela JG, Cunha TM, Verri WA Jr, Grespan R, Matsumura G, Ribeiro JM, Elnaiem DE, Silva JS, Cunha FQ, J Leukoc Biol 2008 84 1 104 114 10.1189/jlb.1107797 18390928 (Pubitemid 351960285)
14. Sandfly maxadilan exacerbates infection with Leishmania major and vaccinating against it protects against L. major infection. Morris RV, Shoemaker CB, David JR, Lanzaro GC, Titus RG, J Immunol 2001 167 9 5226 5230 11673536 (Pubitemid 33009759)
15. Protection against cutaneous leishmaniasis resulting from bites of uninfected sand flies. Kamhawi S, Belkaid Y, Modi G, Rowton E, Sacks D, Science 2000 290 5495 1351 1354 10.1126/science.290.5495.1351 11082061
16. Toward a defined anti-Leishmania vaccine targeting vector antigens: characterization of a protective salivary protein. Valenzuela JG, Belkaid Y, Garfield MK, Mendez S, Kamhawi S, Rowton ED, Sacks DL, Ribeiro JM, J Exp Med 2001 194 3 331 342 10.1084/jem.194.3.331 11489952 (Pubitemid 32730807)
17. Effect of Lutzomyia longipalpis salivary gland extracts on leukocyte migration induced by Leishmania major. Monteiro MC, Lima HC, Souza AA, Titus RG, Romão PR, Cunha FQ, AmJTrop Med Hyg 2007 76 1 88 94 (Pubitemid 351627808)
18. Saliva from Lutzomyia longipalpis induces CC chemokine ligand 2/monocyte chemoattractant protein-1 expression and macrophage recruitment. Teixeira CR, Teixeira MJ, Gomes RB, Santos CS, Andrade BB, Raffaele-Netto I, Silva JS, Guglielmotti A, Miranda JC, Barral A, Brodskyn C, Barral-Netto M, J Immunol 2005 175 12 8346 8353 16339576 (Pubitemid 41798401)
19. What determines the success or failure of intracellular cutaneous parasites? Lessons learned from leishmaniasis. Maurer M, Dondji B, von Stebut E, Med Microbiol Immunol 2009 198 3 137 146 10.1007/s00430-009-0114-9 19396461
20. The chemotactic effect of Phlebotomus duboscqi (Diptera: Psychodidae) salivary gland lysates to murine monocytes. Anjili CO, Mbati PA, Mwangi RW, Githure JI, Olobo JO, Robert LL, Koech DK, Acta Trop 1995 60 2 97 100 10.1016/0001-706X(95)00112-R 8610544 (Pubitemid 126666211)
21. Effect of sand fly saliva on Leishmania uptake by murine macrophages. Zer R, Yaroslavski I, Rosen L, Warburg A, Int J Parasitol 2001 31 8 810 814 10.1016/S0020-7519(01)00190-4 11403772 (Pubitemid 32524165)
22. The impact of vector-mediated neutrophil recruitment on cutaneous leishmaniasis. Peters NC, Sacks DL, Cell Microbiol 2009 11 9 1290 1296 10.1111/j.1462-5822.2009.01348.x 19545276
23. Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Titus RG, Ribeiro JM, Science 1988 239 4845 1306 1308 10.1126/science.3344436 3344436
24. BALB/c mice infected with antimony treatment refractory isolate of Leishmania braziliensis present severe lesions due to IL-4 production. Costa DL, Carregaro V, Lima-Júnior DS, Silva NM, Milanezi CM, Cardoso CR, Giudice  de Jesus AR, Carvalho EM, Almeida RP, Silva JS, PLoS Negl Trop Dis 2011 5 3 965 10.1371/journal.pntd.0000965 21390155
25. A simple, non-chromatographic procedure to purify immunoglobulins from serum and ascites fluid. McKinney MM, Parkinson A, J Immunol Methods 1987 96 2 271 278 10.1016/0022-1759(87)90324-3 3805742 (Pubitemid 17022661)
26. Cutting edge: neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. van Zandbergen G, Klinger M, Mueller A, Dannenberg S, Gebert A, Solbach W, Laskay T, J Immunol 2004 173 11 6521 6525 15557140 (Pubitemid 39541033)
27. Macrophage interactions with neutrophils regulate Leishmania major infection. Ribeiro-Gomes FL, Otero AC, Gomes NA, Moniz-De-Souza MC, Cysne-Finkelstein L, Arnholdt AC, Calich VL, Coutinho SG, Lopes MF, DosReis GA, J Immunol 2004 172 7 4454 4462 15034061 (Pubitemid 38375261)
28. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Peters NC, Egen JG, Secundino N, Debrabant A, Kimblin N, Kamhawi S, Lawyer P, Fay MP, Germain RN, Sacks D, Science 2008 321 5891 970 974 10.1126/science.1159194 18703742
29. Natural regulatory T cells in infectious disease. Belkaid Y, Rouse BT, Nat Immunol 2005 6 4 353 360 15785761 (Pubitemid 41716772)
30. CD4 + CD25+ T cells in skin lesions of patients with cutaneous leishmaniasis exhibit phenotypic and functional characteristics of natural regulatory T cells. Campanelli AP, Roselino AM, Cavassani KA, Pereira MS, Mortara RA, Brodskyn CI, Goncalves HS, Belkaid Y, Barral-Netto M, Barral A, Silva JS, J Infect Dis 2006 193 9 1313 1322 10.1086/502980 16586370
31. IL-10 family of cytokines. Sabat R, Cytokine Growth Factor Rev 2010 21 5 315 324 10.1016/j.cytogfr.2010.11.001 21112807
32. Interleukin-10 and the interleukin-10 receptor. Moore KW, de Waal MR, Coffman RL, O'Garra A, Annu Rev Immunol 2001 19 683 765 10.1146/annurev.immunol. 19.1.683 11244051 (Pubitemid 32368050)
33. Suppressor of cytokine signaling 1 inhibits IL-10-mediated immune responses. Ding Y, Chen D, Tarcsafalvi A, Su R, Qin L, Bromberg JS, J Immunol 2003 170 3 1383 1391 12538698 (Pubitemid 36139505)
34. Sand fly saliva enhances Leishmania amazonensis infection by modulating interleukin-10 production. Norsworthy NB, Sun J, Elnaiem D, Lanzaro G, Soong L, Infect Immun 2004 72 3 1240 1247 10.1128/IAI.72.3.1240-1247.2004 14977924 (Pubitemid 38263741)
35. Immunity to a salivary protein of a sand fly vector protects against the fatal outcome of visceral leishmaniasis in a hamster model. Gomes R, Teixeira C, Teixeira MJ, Oliveira F, Menezes MJ, Silva C, de Oliveira CI, Miranda JC, Elnaiem DE, Kamhawi S, Valenzuela JG, Brodskyn CI, Proc Natl Acad Sci U S A 2008 105 22 7845 7850 10.1073/pnas.0712153105 18509051 (Pubitemid 351872726)
36. Structure and function of a "yellow" protein from saliva of the sand fly Lutzomyia longipalpis that confers protective immunity against Leishmania major infection. Xu X, Oliveira F, Chang BW, Collin N, Gomes R, Teixeira C, Reynoso D, My Pham V, Elnaiem DE, Kamhawi S, Ribeiro JM, Valenzuela JG, Andersen JF, J Biol Chem 2011 286 37 32383 32393 10.1074/jbc.M111.268904 21795673
37. DNA vaccination with KMP11 and Lutzomyia longipalpis salivary protein protects hamsters against visceral leishmaniasis. da Silva RA, Tavares NM, Costa D, Pitombo M, Barbosa L, Fukutani K, Miranda JC, de Oliveira CI, Valenzuela JG, Barral A, Soto M, Barral-Netto M, Brodskyn C, Acta Trop 2011 120 3 185 190 10.1016/j.actatropica.2011.08.007 21875567
38. Lutzomyia longipalpis saliva or salivary protein LJM19 protects against Leishmania braziliensis and the saliva of its vector, Lutzomyia intermedia. Tavares NM, Silva RA, Costa DJ, Pitombo MA, Fukutani KF, Miranda JC, Valenzuela JG, Barral A, de Oliveira CI, Barral-Netto M, Brodskyn C, PLoS Negl Trop Dis 2011 5 5 1169 10.1371/journal.pntd.0001169 21655303
39. The immune response to sand fly salivary proteins and its influence on leishmania immunity. Gomes R, Oliveira F, Front Immunol 2012 3 110 22593758
40. Nucleosides from Phlebotomus papatasi salivary gland ameliorate murine collagen-induced arthritis by impairing dendritic cell functions. Carregaro V, Sá-Nunes A, Cunha TM, Grespan R, Oliveira CJ, Lima-Junior DS, Costa DL, Verri WA Jr, Milanezi CM, Pham VM, Brand DD, Valenzuela JG, Silva JS, Ribeiro JM, Cunha FQ, J Immunol 2011 187 8 4347 4359 10.4049/jimmunol.1003404 21930966
41. Discovery of markers of exposure specific to bites of Lutzomyia longipalpis: the vector of Leishmania infantum chagasi in Latin America. Teixeira C, Gomes R, Collin N, Reynoso D, Jochim R, Oliveira F, Seitz A, Elnaiem DE, Caldas A, de Souza AP, Brodskyn CI, de Oliveira CI, Mendonca I, Costa CH, Volf P, Barral A, Kamhawi S, Valenzuela JG, PLoS Negl Trop Dis 2010 4 3 638 10.1371/journal.pntd.0000638 20351786