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

Folia Parasitologica

Volumn 53, Issue 3, 2006, Pages 161-171

  Rohoušová, Iva ^a   Volf, Petr ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Host immune response; Leishmaniasis; Lutzomyia; Phlebotomus; Sand fly saliva

Indexed keywords

CANIS FAMILIARIS; DIPTERA; PHLEBOTOMINAE; PSYCHODIDAE;

EID: 33750056121     PISSN: 00155683     EISSN: None     Source Type: Journal    
DOI: 10.14411/fp.2006.022     Document Type: Review

References (75)

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.
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.
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.
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.
5. ASHFORD R.W. 2000: The leishmaniasis as emerging and reemerging zoonoses. Int. J. Parasitol. 30: 1269-1281.
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.
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.
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.
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.
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 PACAP-type 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.
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.
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.
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.
15. ČERNÁ P., MIKEŠ L., VOLF P. 2002: Salivary gland hyaluronidase in various species of phlebotomine sand flies (Diptera : Psychodidae). Insect Biochem. Mol. Biol. 32: 1691-1697.
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.
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.
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.
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.
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.
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 delayed-type hypersensitivity. J. Infect. Dis. 186: 1530-1534.
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.
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.
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.
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.
26. KILLICK-KENDRICK R. 1990: Phlebotomine vectors of the leishmaniases: a review. Med. Vet. Entomol. 4: 1-24.
27. KILLICK-KENDRICK R., KILLICK-KENDRICK M., PINELLI E., DEL REAL 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.
28. KLEIN J., HOŘEJŠÍ V. 1997: Immunology. Blackwell Science, Oxford, 722 pp.
29. LANZARO G.G., 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.
30. 2 production and antileishmanial capacity of human cultured monocytes mediated by IFN-γ. J. Immunol. 143: 3020-3024.
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.
32. LOUZIR H., KILLICK-KENDRICK R., KILLICK-KENDRICK M., BEN SALAH A., ZHIOUA E., CHELBI L, 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.
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.
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.
36. MILLERON R.S., MUTEBI J.P., VALLE S., MONTOYA A., YIN H.Z., SOONG L., LANZARO G.G. 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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
49. ROHOUŠOVÁ 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.
50. ROHOUŠOVÁ I., VOLF P., LIPOLDOVÁ 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.
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.
52. SACKS D., KAMHAWI S. 2001: Molecular aspects of parasite-vector and vector-host interactions in leishmaniasis. Annu. Rev. Microbiol. 55: 453-483.
53. SÁDLOVÁ 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.
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.
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.
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.
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.
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.
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.
61. THIAKAKI M., ROHOUŠOVÁ I., VOLFOVÁ V., VOLF P., CHANG K.P., SOTERIADOU K. 2005: Sand fly species-specificity of saliva-mediated protective immunity in Leishmania amazonensis-BALB/c mouse model. Microbes Infect. 7: 760-766.
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.
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.
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.
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.
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 anti-Leishmania vaccine targeting vector antigens: characterization of a protective salivary protein. J. Exp. Med. 194: 331-342.
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.
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.
69. VOLF P., ROHOUŠOVÁ I. 2001: Species-specific antigens in salivary glands of phlebotomine sandflies. Parasitology 122: 37-41.
70. VOLF P., TESAŘOVÁ P., NOHÝNKOVÁ E. 2000: Salivary proteins and glycoproteins in phlebotomine sandflies of various species, sex and age. Med. Vet. Entomol. 14: 251-256.
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.
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.
73. WARBURG A., SCHLEIN Y. 1986: The effect of postblood-meal nutrition of Phlebotomus papatasi on the transmission of Leishmania major. Am. J. Trop. Med. Hyg. 35: 926-930.
74. WHO July 2005: http://www.who.int/tdr/diseases/leish/
75. 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.