Folia Parasitologica 53[3] 161-171 (2006) | DOI: 10.14411/fp.2006.022

Sand fly saliva: effects on host immune response and Leishmania transmission

Iva Rohou¹ová, Petr Volf
Department of Parasitology, Faculty of Science, Charles University, Vinièná 7, 128 44 Prague 2, Czech Republic

The feeding success of sand flies (Diptera: Phlebotominae) is linked to the vast array of pharmacological substances in their saliva, which interferes with the host haemostasis and immune response. Modification of feeding site plays also an important role in Leishmania transmission. In naive hosts, co-inoculation of saliva and Leishmania parasites increases the chance of successful transmission. Disease exacerbation seems to be associated with enhanced production of type 2 cytokines and selective inhibition of some macrophage functions including the production of NO and H2O2. On the other hand, hosts repeatedly exposed to sand fly bites develop anti-saliva immune response that results in a protection against Leishmania infection. This led to a new interesting approach to anti-Leishmania vaccine - using salivary components to block parasite transmission. The review is therefore focused on the interactions that run between immunomodulatory molecules in sand fly saliva and host immune response, with the impact on Leishmania infection development. Recent studies revealed that saliva-based vaccine for leishmaniasis might be effective and feasible, however, several questions still require to be solved. The knowledge based on experimental mouse model cannot be fully extrapolated to dogs or humans and due to differences in salivary antigens between sand fly species the protective effect is species-specific. On the other hand, the specificity of salivary antigens enables the use of anti-saliva antibodies for monitoring the exposure of hosts to sand fly bites and might be used as a marker of risks for Leishmania transmission in endemic areas.

Keywords: Phlebotomus, Lutzomyia, sand fly saliva, leishmaniasis, host immune response

Received: May 5, 2006; Accepted: June 1, 2006; Published: September 1, 2006  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Rohou¹ová, I., & Volf, P. (2006). Sand fly saliva: effects on host immune response and Leishmania transmission. Folia Parasitologica, 53(3), 161-171. doi: 10.14411/fp.2006.022
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. ADLER S., THEODOR O. 1926: The mouthparts, alimentary tract and salivary apparatus of the female in Phlebotomus papatasi. Ann. Trop. Med. Parasitol. 20: 109-128 Go to original source...
    2. AMARAL V.F., RANSATTO V.A.O., CONCEICAO-SILVA F., MOLINARO E., FERREIRA V., COUTINHO S.G., MCMAHON-PRATT D., GRIMALDI G. 1996: Leishmania amazonensis: the Asian rhesus macaques (Macaca mulatta) as an experimental model for study of cutaneous leishmaniasis. Exp. Parasitol. 82: 34-44 Go to original source... Go to PubMed...
    3. ANDERSON J.M., OLIVEIRA F., KAMHAWI S., MANS B.J., REYNOSO D., SEITZ A.E., LAWYER P., GARFIELD M., PHAM M.V., VALENZUELA J.G. 2006: Comparative salivary gland transcriptomics of sandfly vectors of visceral leishmaniasis. BMC Genomics 7: 52-75 Go to original source... Go to PubMed...
    4. ANJILI C.O., MBATI P.A., MWANGI R.W., GITHURE J.I., OLOBO J.O., ROBERT L.L., KOECH D.K. 1995: The chemotactic effect of Phlebotomus duboscqi (Diptera: Psychodidae) salivary gland lysates to murine monocytes. Acta Trop. 60: 97-100 Go to original source... Go to PubMed...
    5. ASHFORD R.W. 2000: The leishmaniasis as emerging and reemerging zoonoses. Int. J. Parasitol. 30: 1269-1281 Go to original source... Go to PubMed...
    6. BARRAL A., HONDA E., CALDAS A., COSTA J., VINHAS V., ROWTON E.D., VALENZUELA J.G., CHARLAB R., BARRAL-NETTO M., RIBEIRO J.M.C. 2000: Human immune response to sand fly salivary gland antigens: a useful epidemiological marker? Am. J. Trop. Med. Hyg. 62: 740-745 Go to original source... Go to PubMed...
    7. BELKAID Y., KAMHAWI S., MODI G., VALENZUELA J., NOBEN-TRAUTH N., ROWTON E., RIBEIRO J., SACKS D.L. 1998: 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. 188: 1941-1953 Go to original source... Go to PubMed...
    8. BELKAID Y., VALENZUELA J.G., KAMHAWI S., ROWTON E., SACKS D.L., RIBEIRO J.M.C. 2000: Delayed-type hypersensitivity to Phlebotomus papatasi sand fly bite: An adaptive response induced by the fly? Proc. Natl. Acad. Sci. USA 97: 6704-6709 Go to original source... Go to PubMed...
    9. BEZERRA H.S.D., TEIXEIRA M.J. 2001: Effect of Lutzomyia whitmani (Diptera: Psychodidae) salivary gland lysates on Leishmania (Viannia) braziliensis infection in BALB/c mice. Mem. Inst. Oswaldo Cruz 96: 349-351 Go to original source... Go to PubMed...
    10. BOZZA M., SOARES M.B.P., BOZZA P.T., SATOSKAR A.R., DIACOVO T.G., BROMBACHER F., TITUS R.G., SHOEMAKER C.B., DAVID J.R. 1998: The PACAPtype I receptor agonist maxadilan from sand fly saliva protects mice against lethal endotoxemia by a mechanism partially dependent on IL-10. Eur. J. Immunol. 28: 3120- 3127 Go to original source... Go to PubMed...
    11. BRODSKYN C.I., GOMES R., TEIXEIRA C., SILVA C., TEIXEIRA M.J., BARRAL-NETTO M., BARRAL A., VALENZUELA J. 2005: Immunization with cDNA from Lutzomyia longipalpis salivary protein glands protects hamsters from infection by Leishmania chagasi. Third World Congress on Leishmaniosis Worldleish3, April 10- 15, 2005, Palermo-Terrasini, Sicily, Italy. Abstract book p. 121
    12. BROWN S.J., ROSALSKY J.H. 1984: Blood leukocyte response in hosts parasitized by the hematophagous arthropods Triatoma protracta and Lutzomyia longipalpis. Am. J. Trop. Med. Hyg. 33: 499-505 Go to original source... Go to PubMed...
    13. CASTRO-SOUSA F., PARANHOS-SILVA M., SHERLOCK I., PAIXAO M.S., PONTES-DE-CARVALHO L.C., DOS-SANTOS W.L.C. 2001: Dissociation between vasodilation and Leishmania infection-enhancing effects of sand fly saliva and maxadilan. Mem. Inst. Oswaldo Cruz 96: 997-999 Go to original source... Go to PubMed...
    14. CAVALCANTE R.R., PEREIRA M.H., GONTIJO N.F. 2003: Anti-complement activity in the saliva of phlebotomine sand flies and other haematophagous insects. Parasitology 127: 87-93 Go to original source... Go to PubMed...
    15. CERNA P., MIKES L., VOLF P. 2002: Salivary gland hyaluronidase in various species of phlebotomine sand flies (Diptera : Psychodidae). Insect Biochem. Mol. Biol. 32: 1691-1697 Go to original source... Go to PubMed...
    16. CHARLAB R., VALENZUELA J.G., ROWTON E.D., RIBEIRO J.M.C. 1999: Toward an understanding of the biochemical and pharmacological complexity of the saliva of a hematophagous sand fly Lutzomyia longipalpis. Proc. Natl. Acad. Sci. USA 96: 15155-15160 Go to original source... Go to PubMed...
    17. COSTA D.J., FAVALI C., CLARENCIO J., AFONSO L., CONCEICAO V., MIRANDA J.C., TITUS R.G., VALENZUELA J., BARRAL-NETTO M., BARRAL A., BRODSKYN C.I. 2004: Lutzomyia longipalpis salivary gland homogenate impairs cytokine production and costimulatory molecule expression on human monocytes and dendritic cells. Infect. Immun. 72: 1298-1305 Go to original source... Go to PubMed...
    18. DONNELLY K.B., LIMA H.C., TITUS R.G. 1998: Histologic characterization of experimental cutaneous leishmaniasis in mice infected with Leishmania braziliensis in the presence or absence of sand fly vector salivary gland lysate. J. Parasitol. 84: 97-103 Go to original source... Go to PubMed...
    19. ELNAIEM D.E.A., MENESES C., SLOTMAN M., LANZARO G.C. 2005: Genetic variation in the sand fly salivary protein, SP-15, a potential vaccine candidate against Leishmania major. Insect Mol. Biol. 14: 145-150 Go to original source... Go to PubMed...
    20. GHOSH K.N., MUKHOPADHYAY A. 1998: The effect of anti-sandfly saliva antibodies on Phlebotomus argentipes and Leishmania donovani. Int. J. Parasitol. 28: 275-281 Go to original source... Go to PubMed...
    21. GOMES R.B., BRODSKYN U., DE OLIVEIRA C.I., COSTA J., MIRANDA J.C., CALDAS A., VALENZUELA J.G., BARRAL-NETTO M., BARRAL A. 2002: Seroconversion against Lutzomyia longipalpis saliva concurrent with the development of anti-Leishmania chagasi delayedtype hypersensitivity. J. Infect. Dis. 186: 1530-1534 Go to original source... Go to PubMed...
    22. GUILPIN V.O., SWARDSON-OLVER C., NOSBISCH L., TITUS R.G. 2002: Maxadilan, the vasodilator/immunomodulator from Lutzomyia longipalpis sand fly saliva, stimulates haematopoiesis in mice. Parasite Immunol. 24: 437-446 Go to original source... Go to PubMed...
    23. HALL L.R., TITUS R.G. 1995: Sand fly vector saliva selectively modulates macrophage functions that inhibit killing of Leishmania major and nitric oxide production. J. Immunol. 155: 3501-3506 Go to original source... Go to PubMed...
    24. KAMHAWI S., BELKAID Y., MODI G., ROWTON E., SACKS D. 2000: Protection against cutaneous leishmaniasis resulting from bites of uninfected sand flies. Science 290: 1351-1354 Go to original source... Go to PubMed...
    25. KATZ O., WAITUMBI J.N., ZER R., WARBURG A. 2000: Adenosine, AMP, and protein phosphatase activity in sandfly saliva. Am. J. Trop. Med. Hyg. 62: 145-150 Go to original source... Go to PubMed...
    26. KILLICK-KENDRICK R. 1990: Phlebotomine vectors of the leishmaniases: a review. Med. Vet. Entomol. 4: 1-24 Go to original source... Go to PubMed...
    27. KILLICK-KENDRICK R., KILLICK-KENDRICK M., PINELLI E., DELREAL G., MOLINA R., VITUTIA M.M., CANAVATE M.C., NIETO J. 1994: A laboratory model of canine leishmaniasis: the inoculation of dogs with Leishmania infantum promastigotes from midguts of experimentally infected phlebotomine sandflies. Parasite 1: 311-318 Go to original source... Go to PubMed...
    28. KLEIN J., HOREJSI V. 1997: Immunology. Blackwell Science, Oxford, 722 pp
    29. LANZARO G.C., LOPES A.H.C.S., RIBEIRO J.M.C., SHOEMAKER C.B., WARBURG A., SOARES M., TITUS R.G. 1999: Variation in the salivary peptide, maxadilan, from species in the Lutzomyia longipalpis complex. Insect Mol. Biol. 8: 267-275 Go to original source... Go to PubMed...
    30. LEHN M., WEISER W.Y., ENGELHORN S., GILLIS S., REMOLD H.G. 1989: IL-4 inhibits H2O2 production and antileishmanial capacity of human cultured monocytes mediated by IFN-γ. J. Immunol. 143: 3020-3024 Go to original source... Go to PubMed...
    31. LIMA H.C., TITUS R.G. 1996: Effects of sand fly vector saliva on development of cutaneous lesions and the immune response to Leishmania braziliensis in BALB/c mice. Infect. Immun. 64: 5442-5445 Go to original source... Go to PubMed...
    32. LOUZIR H., KILLICK-KENDRICK R., KILLICKKENDRICK M., BEN SALAH A., ZHIOUA E., CHELBI I., CHEMKI J., MOKNI M., DELLAGI K. 2005: Antibody to sand fly saliva in a Tunisian population at risk for zoonotic cutaneous leishmaniasis. Fifth International Symposium on Phlebotomine Sandflies ISOPS V, Gammarth-Tunis, Tunisia, April 17-21, 2005. Abstract OP-62. Arch. Inst. Pasteur Tunis 82: 80
    33. MBOW M.L., BLEYENBERG J.A., HALL L.R., TITUS R.G. 1998: Phlebotomus papatasi sand fly salivary gland lysate down-regulates a Th1, but up-regulates a Th2, response in mice infected with Leishmania major. J. Immunol. 161: 5571-5577 Go to original source... Go to PubMed...
    34. MELO M.N., WILLIAMS P., TAFURI W.L. 2001: Influence of lysates of the salivary glands of Lutzomyia longipalpis on the development of a Leishmania-major-like parasite in the skin of the golden hamsters. Ann. Trop. Med. Parasitol. 95: 59-68 Go to original source... Go to PubMed...
    35. MENON J.N., BRETSCHER P.A. 1996: Characterization of the immunological memory state generated in mice susceptible to Leishmania major following exposure to low doses of L. major and resulting in resistance to a normally pathogenic challenge. Eur. J. Immunol. 26: 243- 249 Go to original source... Go to PubMed...
    36. MILLERON R.S., MUTEBI J.P., VALLE S., MONTOYA A., YIN H.Z., SOONG L., LANZARO G.C. 2004a: Antigenic diversity in maxadilan, a salivary protein from the sand fly vector of American visceral leishmaniasis. Am. J. Trop. Med. Hyg. 70: 286-293 Go to original source... Go to PubMed...
    37. MILLERON R.S., RIBEIRO J.M.C., ELNAIME D., SOONG L., LANZARO G.C. 2004b: Negative effect of antibodies against maxadilan on the fitness of the sand fly vector of American visceral leishmaniasis. Am. J. Trop. Med. Hyg. 70: 278-285 Go to original source... Go to PubMed...
    38. MONTEIRO M.C., NOGUEIRA L.G., SOUZA A.A.A., RIBEIRO J.M.C., SILVA J.S., CUNHA F.Q. 2005: Effect of salivary gland extract of Leishmania vector, Lutzomyia longipalpis, on leukocyte migration in OVA-induced immune peritonitis. Eur. J. Immunol. 35: 2424-2433 Go to original source... Go to PubMed...
    39. MORRIS R.V., SHOEMAKER C.B., DAVID J.R., LANZARO G.C., TITUS R.G. 2001: Sandfly maxadilan exacerbates infection with Leishmania major and vaccinating against it protects against L. major infection. J. Immunol. 167: 5226-5230 Go to original source... Go to PubMed...
    40. NORSWORTHY N.B., SUN J.R., ELNAIEM D., LANZARO G., SOONG L. 2004: Sand fly saliva enhances Leishmania amazonensis infection by modulation interleukin-10 production. Infect. Immun. 72: 1240-1247 Go to original source... Go to PubMed...
    41. OLIVEIRA F., KAMHAWI S., SEITZ A.E., PHAM V.M., GUIGAL P.M., FISCHER L., WARD J., VALENZUELA J.G. 2006: From transcriptome to proteome: Identification of DTH inducing proteins from a Phlebotomus ariasi salivary gland cDNA library. Vaccine 24: 374-390 Go to original source... Go to PubMed...
    42. PARANHOS M., DOS SANTOS W.C., SHERLOCK I., OLIVEIRA G.G.S., PONTES DE CARVALHO L.C. 1993: Development of eosinophilia in dogs intradermically inoculated with sand fly saliva and Leishmania (Leishmania) chagasi stationary phase. Mem. Inst. Oswaldo Cruz 88: 249-251 Go to original source... Go to PubMed...
    43. PARANHOS-SILVA M., OLIVEIRA G.G.S., REIS E.A., DE MENEZES R.M.C., FERNANDES O., SHERLOCK I., GOMES R.B.B., PONTES DE CARVALHO L.C., DOS SANTOS W.L.C. 2003: A follow-up of Beagle dogs intradermally infected with Leishmania chagasi in the presence or absence of sand fly saliva. Vet. Parasitol. 114: 97-111 Go to original source... Go to PubMed...
    44. QURESHI A.A., ASAHINA A., OHNUMA M., TAJIMA M., GRANSTEIN R.D., LERNER E.A. 1996: Immunomodulatory properties of maxadilan, the vasodilator peptide from sand fly salivary gland extracts. Am. J. Trop. Med. Hyg. 54: 665-671 Go to original source... Go to PubMed...
    45. ROGERS K.A., DEKREY G.K., MBOW M.L., GILLESPIE R.D., BRODSKYN C.I., TITUS R.G. 2002a: Type 1 and type 2 responses to Leishmania major. FEMS Microbiol. Lett. 209: 1-7 Go to original source... Go to PubMed...
    46. ROGERS K.A., TITUS R.G. 2003: Immunomodulatory effects of Maxadilan and Phlebotomus papatasi sand fly salivary gland lysates on human primary in vitro immune responses. Parasite Immunol. 25: 127-134 Go to original source... Go to PubMed...
    47. ROGERS M.E., CHANCE M.L., BATES P.A. 2002b: The role of promastigote secretory gel in the origin and transmission of the infective stage of Leishmania mexicana by the sandfly Lutzomyia longipalpis. Parasitology 124: 495-507 Go to original source... Go to PubMed...
    48. ROGERS M.E., ILG T., NIKOLAEV A.V., FERGUSON M.A.J., BATES P.A. 2004: Transmission of cutaneous leishmaniasis by sand flies is enhanced by regurgitation of fPPG. Nature 430: 463-467. Go to original source... Go to PubMed...
    49. ROHOUSOVA I., OZENSOY S., OZBEL Y., VOLF P. 2005b: Detection of species-specific antibody response of humans and mice bitten by sand flies. Parasitology 130: 443-449 Go to original source... Go to PubMed...
    50. ROHOUSOVA I., VOLF P., LIPOLDOVA M. 2005a: Modulation of murine cellular immune response and cytokine production by salivary gland lysate of three sand fly species. Parasite Immunol. 27: 469-473 Go to original source... Go to PubMed...
    51. ROJAS E., SCORZA J.V. 1995: Leishmania braziliensis: isolation of lesions by inoculation of hamsters with and without the addition of salivary gland lysates of Lutzomyia youngi. Rev. Saude Publica 29: 1-5 Go to original source... Go to PubMed...
    52. SACKS D., KAMHAWI S. 2001: Molecular aspects of parasite-vector and vector-host interactions in leishmaniasis. Annu. Rev. Microbiol. 55: 453-483 Go to original source... Go to PubMed...
    53. SADLOVA J. 1999: The life history of Leishmania (Kinetoplastida: Trypanosomatidae). Acta Soc. Zool. Bohem. 63: 331-366
    54. SAMUELSON J., LERNER E., TESH R., TITUS R. 1991: A mouse model of Leishmania braziliensis braziliensis infection produced by coinjection with sand fly saliva. J. Exp. Med. 173: 49-54 Go to original source... Go to PubMed...
    55. SILVA F., GOMES R., PRATES D., MIRANDA J.C., ANDRADE B., BARRAL-NETTO M., BARRAL A. 2005: Inflammatory cell infiltration and high antibody production in BALB/c mice caused by natural exposure to Lutzomyia longipalpis bites. Am. J. Trop. Med. Hyg. 72: 94-98 Go to original source... Go to PubMed...
    56. SOARES M.B.P., TITUS R.G., SHOEMAKER C.B., DAVID J.R., BOZZA M. 1998: The vasoactive peptide maxadilan from sand fly saliva inhibits TNF-alpha and induces IL-6 by mouse macrophages through interaction with the pituitary adenylate cyclase-activating polypeptide (PACAP) receptor. J. Immunol. 160: 1811-1816 Go to original source... Go to PubMed...
    57. STIERHOF Y.D., BATES P.A., JACOBSON R.L., ROGERS M.E., SCHLEIN Y., HANDMAN E., ILG T. 1999: Filamentous proteophosphoglycan secreted by Leishmania promastigotes forms gel-like three-dimensional networks that obstruct the digestive tract of infected sandfly vectors. Eur. J. Cell Biol. 78: 675-689 Go to original source... Go to PubMed...
    58. THEODOR O. 1935: A study of the reaction to Phlebotomus bites with some remarks of "harara". Trans. R. Soc. Trop. Med. Hyg. 29: 273-284 Go to original source...
    59. THEODOS C.M., RIBEIRO J.M.C., TITUS R.G. 1991: Analysis of enhancing effect of sand fly saliva on Leishmania infection in mice. Infect. Immun. 59: 1592- 1598 Go to original source... Go to PubMed...
    60. THEODOS C.M., TITUS R.G. 1993: Salivary gland material from the sand fly Lutzomyia longipalpis has an inhibitory effect on macrophage function in vitro. Parasite Immunol. 15: 481-487 Go to original source... Go to PubMed...
    61. THIAKAKI M., ROHOUSOVA I., VOLFOVA V., VOLF P., CHANG K.P., SOTERIADOU K. 2005: Sand fly speciesspecificity of saliva-mediated protective immunity in Leishmania amazonensis-BALB/c mouse model. Microbes Infect. 7: 760-766 Go to original source... Go to PubMed...
    62. TITUS R.G. 1998: Salivary gland lysate from the sand fly Lutzomyia longipalpis suppresses the immune response of mice to sheep red blood cells in vivo and concanavalin A in vitro. Exp. Parasitol. 89: 133-136 Go to original source... Go to PubMed...
    63. TITUS R.G., RIBEIRO J.M.C. 1988: Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 239: 1306-1308 Go to original source... Go to PubMed...
    64. TITUS R.G., RIBEIRO J.M.C. 1990: The role of vector saliva in transmission of arthropod-borne disease. Parasitol. Today 6: 157-160 Go to original source... Go to PubMed...
    65. TRAVI B.L., OSORIO Y., GUARIN N., CADENA H. 1998: Leishmania (Leishmania) chagasi: clinical and parasitological observations in experimentally infected Didelphis marsupialis, reservoir of New World visceral leishmaniasis. Exp. Parasitol. 88: 73-75 Go to original source... Go to PubMed...
    66. VALENZUELA J.G., BELKAID Y., GARFIELD M.K., MENDEZ S., KAMHAWI S., ROWTON E.D., SACKS D.L., RIBEIRO J.M.C. 2001: Toward a defined antiLeishmania vaccine targeting vector antigens: characterization of a protective salivary protein. J. Exp. Med. 194: 331-342 Go to original source... Go to PubMed...
    67. VALENZUELA J.G., GARFIELD M., ROWTON E.D., PHAM V.M. 2004: Identification of the most abundant secreted proteins from the salivary glands of the sand fly Lutzomyia longipalpis, vector of Leishmania chagasi. J. Exp. Biol. 207: 3717-3729 Go to original source... Go to PubMed...
    68. VALENZUELA J.G., OLIVEIRA F., SEITZ A., PHAM V.M., KAMHAWI S., LAWYER P., ROWTON E., BRODSKYN C., BARRAL A., BARRAL-NETTO M., GOMEZ R., DE OLIVEIRA C.I. 2005: From massive cDNA sequencing to functional genomics of sand fly salivary glands. Fifth International Symposium on Phlebotomine Sandflies ISOPS V, Gammarth-Tunis, Tunisia, April 17-21, 2005. Abstract OP-46. Arch. Inst. Pasteur Tunis 82: 59 Go to PubMed...
    69. VOLF P., ROHOUSOVA I. 2001: Species-specific antigens in salivary glands of phlebotomine sandflies. Parasitology 122: 37-41 Go to original source... Go to PubMed...
    70. VOLF P., TESAROVA P., NOHYNKOVA E. 2000: Salivary proteins and glycoproteins in phlebotomine sandflies of various species, sex and age. Med. Vet. Entomol. 14: 251- 256 Go to original source... Go to PubMed...
    71. WAITUMBI J., WARBURG A. 1998: Phlebotomus papatasi saliva inhibits protein phosphatase activity and nitric oxide production by murine macrophages. Infect. Immun. 66: 1534-1537 Go to original source... Go to PubMed...
    72. WARBURG A., SARAIVA E., LANZARO G.C., TITUS R.G., NEVA F. 1994: Saliva of Lutzomyia longipalpis sibling species differs in its composition and capacity to enhance leishmaniasis. Philos. Trans. R. Soc. Lond. B 345: 223-230 Go to original source... Go to PubMed...
    73. WARBURG A., SCHLEIN Y. 1986: The effect of postbloodmeal nutrition of Phlebotomus papatasi on the transmission of Leishmania major. Am. J. Trop. Med. Hyg. 35: 926-930 Go to original source... Go to PubMed...
    74. WHO July 2005: http://www.who.int/tdr/diseases/leish/ ZER R., YAROSLAVSKI I., ROSEN L., WARBURG A. 2001: Effect of sand fly saliva on Leishmania uptake by murine macrophages. Int. J. Parasitol. 31: 810-814

    Return to the content