Advertisement

Biology of the Leishmania−Sand Fly Interaction

  • Paulo F. P. Pimenta
  • Vanessa C. de Freitas
  • Carolina C. Monteiro
  • Ana Clara M. A. Pires
  • Nágila Francinete C. Secundino
Chapter

Abstract

Leishmaniasis is a spectrum of diseases transmitted by sand-fly vector caused by a protozoa parasite from the genus Leishmania (Trypanosomatida: Trypanosomatidae) This vector-borne disease is transmitted to humans exclusively through sand-fly bites. The Leishmania genus was given to honor Sir William Boog Leishman, an assistant professor of pathology in the British Army Medical School, who discovered the parasite for the first time on a slide spleen smear in 1903.

Notes

Acknowledgements

The authors Paulo F. P. Pimenta and Nágila F. C. Secundino received financial support from Fiocruz, CNPq e Fapemig.

References

  1. Adler S (1938) Factors determining the Behaviour of Leishmania sp. in Sandflies. Harefuah 14Google Scholar
  2. Adler S (1964) Leishmania. Adv Parasitol 2:35–96Google Scholar
  3. Ahmed SB, Kaabi B, Chelbi I, Derbali M, Cherni S, Laouini D, Zhioua E (2010) Lack of protection of pre-immunization with saliva of long-term colonized Phlebotomus papatasi against experimental challenge with Leishmania major and saliva of wild-caught P. papatasi. Am J Trop Med Hyg 83:512–514. PM:20810812CrossRefPubMedPubMedCentralGoogle Scholar
  4. Anderson JM, Oliveira F, Kamhawi S, Mans BJ, Reynoso D, Seitz AE, Lawyer P, Garfield M, Pham M, Valenzuela JG (2006) Comparative salivary gland transcriptomics of sandfly vectors of visceral leishmaniasis. BMC Genomics 15:7–52Google Scholar
  5. Barral A, Honda E, Caldas A, Costa J, Vinhas V, Rowton ED, Valenzuela JG, Charlab R, Barral-Netto M, Ribeiro JM (2000) Human immune response to sand fly salivary gland antigens: a useful epidemiological marker? Am J Trop Med Hyg 62:740–745. PM:11304066CrossRefPubMedGoogle Scholar
  6. Bates PA (2008) Leishmania sand fly interaction: progress and challenges. Curr Opin Microbiol 11:340–344. PM:18625337CrossRefPubMedPubMedCentralGoogle Scholar
  7. Beach R, Kiilu G, Leeuwenburg J (1985) Modifications of sand fly biting behavior by Leishmania leads to increased parasite transmission. Am J Trop Med Hyg 34:278–282CrossRefPubMedGoogle Scholar
  8. Belkaid Y, Kamhawi S, Modi G, Valenzuela J, Noben-Trauth N, Rowton E, Ribeiro J, Sacks DL (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. PM:9815271CrossRefPubMedPubMedCentralGoogle Scholar
  9. Belkaid Y, Mendez S, Lira R, Kadambi N, Milon G, Sacks D (2000) A natural model of Leishmania major infection reveals a prolonged “silent” phase of parasite amplification in the skin before the onset of lesion formation and immunity. J Immunol 165:969–977. PM:10878373CrossRefPubMedGoogle Scholar
  10. Berner R, Rudin W, Hecker H (1983) Peritrophic membranes and protease activity in the midgut of the malaria mosquito, Anopheles stephensi (Liston) (Insecta: Diptera) under normal and experimental conditions. J Ultrastruct Res 83:195–204CrossRefPubMedGoogle Scholar
  11. Bezerra HS, Teixeira MJ (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. PM:11313642CrossRefPubMedGoogle Scholar
  12. Billingsley PF, Rudin W (1992) The role of the mosquito peritrophic membrane in blood meal digestion and infectivity of Plasmodium species. J Parasitol 78:430–440. PM:1597785CrossRefPubMedGoogle Scholar
  13. Borovsky D, Schlein Y (1987) Trypsin and chymotrypsin-like enzymes of the sand fly Phlebotomus papatasi infected with Leishmania and their possible role in vector competence. Med Vet Entomol 1:235–242. PM:2979536CrossRefPubMedGoogle Scholar
  14. Boulanger N, Lowenberger C, Volf P, Ursic R, Sigutova L, Sabatier L, Svobodova M, Beverley SM, Spath G, Brun R (2004) Characterization of a defensin from the sand fly Phlebotomus duboscqi induced by challenge with bacteria or the protozoan parasite Leishmania major. Infect Immun 72:7140–7146. PM:15557638CrossRefPubMedPubMedCentralGoogle Scholar
  15. Butcher BA, Turco SJ, Hilty BA, Pimenta PF, Panunzio M, Sacks DL (1996) Deficiency in beta1,3-galactosyltransferase of a Leishmania major lipophosphoglycan mutant adversely influences the Leishmania-sand fly interaction. J Biol Chem 271:20573–20579. PM:8702802CrossRefPubMedGoogle Scholar
  16. da Silva RP, Hall BF, Joiner KA, Sacks DL (1989) CR1, the C3b receptor, mediates binding of infective Leishmania major metacyclic promastigotes to human macrophages. J Immunol 143:617–622. PM:2525590PubMedGoogle Scholar
  17. Elnaiem DA, Hassan HK, Ward RD (1997) Phlebotomine sandflies in a focus of visceral leishmaniasis in a border area of eastern Sudan. Ann Trop Med Parasitol 91:307–318. PM:9229023CrossRefPubMedGoogle Scholar
  18. Elnaiem DE, Meneses C, Slotman M, Lanzaro GC (2005) Genetic variation in the sand fly salivary protein, SP-15, a potential vaccine candidate against Leishmania major. Insect Mol Biol 14:145–150. PM:15796747CrossRefPubMedGoogle Scholar
  19. Feng LC (1951) The role of the peritrophic membrane in leishmania and Trypanosome infections of sandflies. Pek Nat Hist Bull 19:327–334Google Scholar
  20. Ferreira VP, Fazito VV, Pangburn MK, Abdeladhim M, Mendes-Sousa AF, Coutinho-Abreu IV, Rasouli M, Brandt EA, Meneses C, Lima KF (2016) SALO, a novel classical pathway complement inhibitor from saliva of the sand fly Lutzomyia longipalpis. Sci Rep 6:19300. PM:26758086CrossRefPubMedPubMedCentralGoogle Scholar
  21. Gemetchu T (1974) The morphology and fine structure of the midgut and peritrophic membrane fo the adult female, Phlebotomus longipes Parrot and Martin (Diptera: Psychodidae). Ann Trop Med Parasitol 68:111–124CrossRefPubMedGoogle Scholar
  22. Hosseini-Vasoukolaei N, Idali F, Khamesipour A, Yaghoobi-Ershadi MR, Kamhawi S, Valenzuela JG, Edalatkhah H, Arandian MH, Mirhendi H, Emami S (2016) Differential expression profiles of the salivary proteins SP15 and SP44 from Phlebotomus papatasi. Parasit Vectors 9:357. PM:27342811CrossRefPubMedPubMedCentralGoogle Scholar
  23. Howard RF, Ardeshir F, Reese RT (1986) Conservation and antigenicity of N-terminal sequences of GP185 from different Plasmodium falciparum isolates. Gene 46:197–205CrossRefPubMedGoogle Scholar
  24. Kamhawi S (2000) The biological and immunomodulatory properties of sand fly saliva and its role in the establishment of Leishmania infections. Microbes Infect 2:1765–1773. PM:11137049CrossRefPubMedGoogle Scholar
  25. Kamhawi S, Belkaid Y, Modi G, Rowton E, Sacks D (2000a) Protection against cutaneous leishmaniasis resulting from bites of uninfected sand flies. Science 290:1351–1354. PM:11082061CrossRefPubMedGoogle Scholar
  26. Kamhawi S, Modi GB, Pimenta PF, Rowton E, Sacks DL (2000b) The vectorial competence of Phlebotomus sergenti is specific for Leishmania tropica and is controlled by species-specific, lipophosphoglycan-mediated midgut attachment. Parasitology 121(Pt 1):25–33. PM:11085222CrossRefPubMedGoogle Scholar
  27. Kamhawi S, Ramalho-Ortigao M, Pham VM, Kumar S, Lawyer PG, Turco SJ, Barillas-Mury C, Sacks DL, Valenzuela JG (2003) A role for insect galectins in parasite survival. Cell 119:329–341CrossRefGoogle Scholar
  28. Kamhawi S, Ramalho-Ortigao M, Pham VM, Kumar S, Lawyer PG, Turco SJ, Barillas-Mury C, Sacks DL, Valenzuela JG (2004) A role for insect galectins in parasite survival. Cell 119:329–341. PM:15543683CrossRefPubMedGoogle Scholar
  29. Killick-Kendrick RR, Leaney AJ, Ready PD, Molyneux DH (1977) Leishmania in Phlebotominae sandflies. IV. The transmission of Leishmania mexicana amazonensis to hamster by bite of experimentally infected Lutzomyia longipalpis. Proc R Soc Lond 196:105–115CrossRefPubMedGoogle Scholar
  30. Killick-Kendrick R, Molyneux DH (1981) Transmission of leishmaniasis by the bite of phlebotomine sandflies: possible mechanisms. Trans R Soc Trop Med Hyg 75:152–154. PM:7268854CrossRefPubMedGoogle Scholar
  31. Kimblin N, Peters N, Debrabant A, Secundino N, Egen J, Lawyer P, Fay MP, Kamhawi S, Sacks D (2008) Quantification of the infectious dose of Leishmania major transmitted to the skin by single sand flies. Proc Natl Acad Sci U S A 105:10125–10130. PM:18626016CrossRefPubMedPubMedCentralGoogle Scholar
  32. Lainson R, Shaw JJ (1979) The role of animals in the epidemiology of South American leishmaniasis. pp 1–116 In: Lumsden WHR, Evans DA (eds) The Biology of the Kinetoplastida. Academic Press London, 738pGoogle Scholar
  33. Laurenti MD, da Matta VL, Pernichelli T, Secundino NF, Pinto LC, Corbett CE, Pimenta PP (2009a) Effects of salivary gland homogenate from wild-caught and laboratory-reared Lutzomyia longipalpis on the evolution and immunomodulation of Leishmania (Leishmania) amazonensis infection. Scand J Immunol 70:389–395. PM:19751274CrossRefPubMedGoogle Scholar
  34. Laurenti MD, Silveira VM, Secundino NF, Corbett CE, Pimenta PP (2009b) Saliva of laboratory-reared Lutzomyia longipalpis exacerbates Leishmania (Leishmania) amazonensis infection more potently than saliva of wild-caught Lutzomyia longipalpis. Parasitol Int 58:220–226. PM:19454323CrossRefPubMedGoogle Scholar
  35. Lawyer PG, Young DG, Butler JF, Akin DE (1987) Development of Leishmania mexicana in Lutzomyia diabolica and Lutzomyia shannoni (Diptera: Psychodidae). J Med Entomol 24:347–355CrossRefPubMedGoogle Scholar
  36. Lawyer PG, Ngumbi PM, Anjili CO, Odongo SO, Mebrahtu YB, Githure JI, Koech DK, Roberts CR (1990) Development of Leishmania major in Phlebotomus duboscqi and Sergentomyia schwetzi (Diptera: Psychodidae). Am J Trop Med Hyg 43:31–43CrossRefPubMedGoogle Scholar
  37. Malta J, Martins GF, Weng JL, Fernandes KM, Munford ML, Ramalho-Ortigao M (2016) Effects of specific antisera targeting peritrophic matrix-associated proteins in the sand fly vector Phlebotomus papatasi. Acta Trop 159:161–169. PM:27012717CrossRefPubMedGoogle Scholar
  38. Mbow ML, Bleyenberg JA, Hall LR, Titus RG (1998) Phlebotomus papatasi sand fly salivary gland lysate downregulates a Th1, but up-regulates a Th2, response in mice infected with Leishmania major. J Immunol 161(10):5571–5577PubMedGoogle Scholar
  39. McConville MJ, Blackwell JM (1991) Developmental changes in the glycosylated phosphatidylinositols of Leishmania donovani. Characterization of the promastigote and amastigote glycolipids. J Biol Chem 266:15170–15179. PM:1831200PubMedGoogle Scholar
  40. Miller N, Lehane MJ (1993) Peritrophic membranes, cell surface molecules and parasite tropisms within arthropod vectors. Parasitol Today 9:45–50. PM:15463702CrossRefPubMedGoogle Scholar
  41. Miranda JC, Secundino NF, Nieves E, Souza AP, Bahia AC, Prates DB, Pimenta RN, Pinto LC, Barral A, Pimenta PFP (2008) Studies of the influence of the presence of domestic animals on increasing the transmission probabilities of leishmaniasis. Ann Med Entomol 17:9–15Google Scholar
  42. Myskova J, Svobodova M, Beverley SM, Volf P (2007) A lipophosphoglycan-independent development of Leishmania in permissive sand flies. Microbes Infect 9:317–324. PM:17307009CrossRefPubMedPubMedCentralGoogle Scholar
  43. Nieves E, Pimenta PF (2000) Development of Leishmania (Viannia) braziliensis and Leishmania (Leishmania) amazonensis in the sand fly Lutzomyia migonei (Diptera: Psychodidae). J Med Entomol 37:134–140. PM:15218917CrossRefPubMedGoogle Scholar
  44. Nieves E, Pimenta PF (2002) Influence of vertebrate blood meals on the development of Leishmania (Viannia) braziliensis and Leishmania (Leishmania) amazonensis in the sand fly Lutzomyia migonei (Diptera: Psychodidae). Am J Trop Med Hyg 67:640–647. PM:12518856CrossRefPubMedGoogle Scholar
  45. Oliveira F, Lawyer PG, Kamhawi S, Valenzuela JG (2008) Immunity to distinct sand fly salivary proteins primes the anti-Leishmania immune response towards protection or exacerbation of disease. PLoS Negl Trop Dis 2:e226. PM:18414648CrossRefPubMedPubMedCentralGoogle Scholar
  46. Pascoa V, Oliveira PL, Dansa-Petretski M, Silva JR, Alvarenga PH, Jacobs-Lorena M, Lemos FJ (2002) Aedes aegypti peritrophic matrix and its interaction with heme during blood digestion. Insect Biochem Mol Biol 32:517–523. PM:11891128CrossRefPubMedGoogle Scholar
  47. Peters W (1992) Peritrophic membranes. Springer, New YorkCrossRefGoogle Scholar
  48. Peters NC, Egen JG, Secundino N, Debrabant A, Kimblin N, Kamhawi S, Lawyer P, Fay MP, Germain RN, Sacks D (2008) In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321:970–974. PM:18703742CrossRefPubMedPubMedCentralGoogle Scholar
  49. Pimenta PF, da Silva RP, Sacks DL, da Silva PP (1989) Cell surface nanoanatomy of Leishmania major as revealed by fracture-flip. A surface meshwork of 44 nm fusiform filaments identifies infective developmental stage promastigotes. Eur J Cell Biol 48(2):180–190PubMedGoogle Scholar
  50. Pimenta PF, Saraiva EM, Sacks DL (1991) The comparative fine structure and surface glycoconjugate expression of three life stages of Leishmania major. Exp Parasitol 72(2):191–204CrossRefPubMedGoogle Scholar
  51. Pimenta PF, Turco SJ, McConville MJ, Lawyer PG, Perkins PV, Sacks DL (1992) Stage-specific adhesion of Leishmania promastigotes to the sand fly midgut. Science 256:1812–1815. PM:1615326CrossRefPubMedGoogle Scholar
  52. Pimenta PF, Saraiva EM, Rowton E, Modi GB, Garraway LA, Beverley SM, Turco SJ, Sacks DL (1994) Evidence that the vectorial competence of phlebotomine sand flies for different species of Leishmania is controlled by structural polymorphisms in the surface lipophosphoglycan. Proc Natl Acad Sci U S A 91:9155–9159. PM:8090785CrossRefPubMedPubMedCentralGoogle Scholar
  53. Pimenta PF, McConville MJ, Schneider P, Turco SJ (1995) Stage-specific binding of Leishmania donovani to the sand fly vector midgut is regulated by conformational changes in the abundant surface lipophosphoglycan. J Exp Med 181(2):685–697CrossRefPubMedGoogle Scholar
  54. Pimenta PF, Modi GB, Pereira ST, Shahabuddin M, Sacks DL (1997) A novel role for the peritrophic matrix in protecting Leishmania from the hydrolytic activities of the sand fly midgut. Parasitology 115(Pt 4):359–369. PM:9364562CrossRefPubMedGoogle Scholar
  55. Pruzinova K, Sadlova J, Seblova V, Homola M, Votypka J, Volf P (2015) Comparison of blood meal digestion and the peritrophic matrix in four sand fly species differing in susceptibility to Leishmania donovani. PLoS One 10:e0128203. PM:26030610CrossRefPubMedPubMedCentralGoogle Scholar
  56. Puentes SM, da Silva RP, Sacks DL, Hammer CH, Joiner KA (1990) Serum resistance of metacyclic stage Leishmania major promastigotes is due to release of C5b-9. J Immunol 145:4311–4316. PM:2147941PubMedGoogle Scholar
  57. Ribeiro JM, Schneider M, Guimaraes JA (1995) Purification and characterization of prolixin S (nitrophorin 2), the salivary anticoagulant of the blood-sucking bug Rhodnius prolixus. Biochem J 308(Pt 1):243–249. PM:7755571CrossRefPubMedPubMedCentralGoogle Scholar
  58. Richards AG, Richards PA (1977) The peritrophic membranes of insects. Annu Rev Entomol 22:219–240. PM:319739CrossRefPubMedGoogle Scholar
  59. Rogers ME, Bates PA (2007) Leishmania manipulation of sand fly feeding behavior results in enhanced transmission. PLoS Pathog 3:e91. PM:17604451CrossRefPubMedPubMedCentralGoogle Scholar
  60. Rogers ME, Chance ML, Bates PA (2002) The role of promastigote secretory gel in the origin and transmission of the infective stage of Leishmania mexicana by the sand fly Lutzomyia longipalpis. Parasitology 124:495–507. PM:12049412CrossRefPubMedGoogle Scholar
  61. Rogers ME, Ilg T, Nikolaev AV, Ferguson MA, Bates PA (2004) Transmission of cutaneous leishmaniasis by sand flies is enhanced by regurgitation of fPPG. Nature 430:463–467. PM:15269771CrossRefPubMedPubMedCentralGoogle Scholar
  62. Sacks DL, Kenney RT, Kreutzer RD, Jaffe CL, Gupta AK, Sharma MC, Sinha SP, Neva FA, Saran R (1995) Indian kala-azar caused by Leishmania tropica. Lancet 345(8955):959–961CrossRefPubMedGoogle Scholar
  63. Sacks DL (2001) Leishmania-sand fly interactions controlling species-specific vector competence. Cell Microbiol 3:189–196. PM:11298643CrossRefPubMedGoogle Scholar
  64. Sacks DL, da Silva RP (1987) The generation of infective stage Leishmania major promastigotes is associated with the cell-surface expression and release of a developmentally regulated glycolipid. J Immunol 139:3099–3106. PM:3312412PubMedGoogle Scholar
  65. Sacks DL, Perkins PV (1984) Identification of an infective stage of Leishmania promastigotes. Science 223:1417–1419. PM:6701528CrossRefPubMedGoogle Scholar
  66. Sacks DL, Hieny S, Sher A (1985) Identification of cell surface carbohydrate and antigenic changes between noninfective and infective developmental stages of Leishmania major promastigotes. J Immunol 135:564–569. PM:2582050PubMedGoogle Scholar
  67. Sacks DL, Modi G, Rowton E, Spath G, Epstein L, Turco SJ, Beverley SM (2000) The role of phosphoglycans in Leishmania-sand fly interactions. Proc Natl Acad Sci U S A 97:406–411. PM:10618431CrossRefPubMedPubMedCentralGoogle Scholar
  68. Saraiva EM, Pimenta PF, Brodin TN, Rowton E, Modi GB, Sacks DL (1995) Changes in lipophosphoglycan and gene expression associated with the development of Leishmania major in Phlebotomus papatasi. Parasitology 111(Pt 3):275–287. PM:7567096CrossRefPubMedGoogle Scholar
  69. Schlein Y, Borut S, Greenblatt CL (1987) Development of sand fly forms of Leishmania major in sucrose solutions. J Parasitol 73:797–805. PM:3625431CrossRefPubMedGoogle Scholar
  70. Schlein Y, Schnur LF, Jacobson RL (1990) Released glycoconjugate of indigenous Leishmania major enhances survival of a foreign L. major in Phlebotomus papatasi. Trans R Soc Trop Med Hyg 84:353–355. PM:2260168CrossRefPubMedGoogle Scholar
  71. Schlein Y, Jacobson RL, Shlomai J (1991) Chitinase secreted by Leishmania functions in the sand fly vector. Proc Biol Sci 245:121–126. PM:1682935CrossRefPubMedGoogle Scholar
  72. Schlein Y, Jacobson RL, Messer G (1992) Leishmania infections damage the feeding mechanism of the sand fly vector and implement parasite transmission by bite. Proc Natl Acad Sci U S A 89:9944–9948. PM:1409724CrossRefPubMedPubMedCentralGoogle Scholar
  73. Secundino NF, Eger-Mangrich I, Braga EM, Santoro MM, Pimenta PF (2005) Lutzomyia longipalpis peritrophic matrix: formation, structure, and chemical composition. J Med Entomol 42:928–938. PM:16465730CrossRefPubMedGoogle Scholar
  74. Secundino N, Kimblin N, Peters NC, Lawyer P, Capul AA, Beverley SM, Turco SJ, Sacks D (2010) Proteophosphoglycan confers resistance of Leishmania major to midgut digestive enzymes induced by blood feeding in vector sand flies. Cell Microbiol 12:906–918. PM:20088949CrossRefPubMedPubMedCentralGoogle Scholar
  75. Secundino NF, de Freitas VC, Monteiro CC, Pires AC, David BA, Pimenta PF (2012) The transmission of Leishmania infantum chagasi by the bite of the Lutzomyia Longipalpis to two different vertebrates. Parasit Vectors 5:20. PM:22260275CrossRefPubMedPubMedCentralGoogle Scholar
  76. Shahabuddin M, Toyoshima T, Aikawa M, Kaslow DC (1993) Transmission-blocking activity of a chitinase inhibitor and activation of malarial parasite chitinase by mosquito protease. Proc Natl Acad Sci U S A 90:4266–4270. PM:8483942CrossRefPubMedPubMedCentralGoogle Scholar
  77. Shakarian AM, Dwyer DM (1998) The Ld Cht1 gene encodes the secretory chitinase of the human pathogen Leishmania donovani. Gene 208:315–322. PM:9524285CrossRefPubMedGoogle Scholar
  78. Shakarian AM, Dwyer DM (2000) Pathogenic leishmania secrete antigenically related chitinases which are encoded by a highly conserved gene locus. Exp Parasitol 94:238–242. PM:10831391CrossRefPubMedGoogle Scholar
  79. Shortt HE, Swaminath CS (1928) The method of feeding of Phlebotomus argentipes with relation to its bearing on the transmission of Kala-azar. Indian J Med Res 15:827–836. https://books.google.com.br/books?id=oK_6OwAACAAJ Google Scholar
  80. Soares RP, Macedo ME, Ropert C, Gontijo NF, Almeida IC, Gazzinelli RT, Pimenta PF, Turco SJ (2002) Leishmania chagasi: lipophosphoglycan characterization and binding to the midgut of the sand fly vector Lutzomyia longipalpis. Mol Biochem Parasitol 121:213–224. PM:12034455CrossRefPubMedGoogle Scholar
  81. Soares RP, Cardoso TL, Barron T, Araujo MS, Pimenta PF, Turco SJ (2005) Leishmania braziliensis: a novel mechanism in the lipophosphoglycan regulation during metacyclogenesis. Int J Parasitol 35:245–253. PM:15722076CrossRefPubMedGoogle Scholar
  82. Stierhof YD, Bates PA, Jacobson RL, Rogers ME, Schlein Y, Handman E (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 78:675–689CrossRefPubMedGoogle Scholar
  83. Svarovska A, Ant TH, Seblova V, Jecna L, Beverley SM, Volf P (2010) Leishmania major glycosylation mutants require phosphoglycans (lpg2-) but not lipophosphoglycan (lpg1-) for survival in permissive sand fly vectors. PLoS Negl Trop Dis 4:e580–PM:20084096CrossRefPubMedPubMedCentralGoogle Scholar
  84. 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 (2010) Discovery of markers of exposure specific to bites of Lutzomyia longipalpis, the vector of Leishmania infantum chagasi in Latin America. PLoS Negl Trop Dis 4(3):e638CrossRefPubMedPubMedCentralGoogle Scholar
  85. Tellam RL (1996) The peritrophic matrix, vol 1. Chapman & Hall, London, pp 86–114Google Scholar
  86. Terra WR (1990) Evolution of digestive systems of insects. Annu Rev Entomol 35:181–200.  https://doi.org/10.1146/annurev.en.35.010190.001145 CrossRefGoogle Scholar
  87. Terra WR, Ferreira C (1994) Insect digestive enzymes: properties, compartmentalization and function. Comp Biochem Physiol B Comp Biochem 109:1–62CrossRefGoogle Scholar
  88. Titus RG, Ribeiro JM (1988) Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 239:1306–1308. PM:3344436CrossRefPubMedGoogle Scholar
  89. Vaidyanathan R (2004) Leishmania parasites (Kinetoplastida: Trypanosomatidae) reversibly inhibit visceral muscle contractions in hemimetabolous and holometabolous insects. J Invertebr Pathol 87:123–128. PM:15579321CrossRefPubMedGoogle Scholar
  90. Vaidyanathan R (2005) Isolation of a myoinhibitory peptide from Leishmania major (Kinetoplastida: Trypanosomatidae) and its function in the vector sand fly Phlebotomus papatasi (Diptera: Psychodidae). J Med Entomol 42:142–152. PM:15799523CrossRefPubMedGoogle Scholar
  91. Valenzuela JG, Belkaid Y, Garfield MK, Mendez S, Kamhawi S, Rowton ED, Sacks DL, Ribeiro JM (2001) Toward a defined anti-Leishmania vaccine targeting vector antigens: characterization of a protective salivary protein. J Exp Med 194:331–342. PM:11489952CrossRefPubMedPubMedCentralGoogle Scholar
  92. Valenzuela JG (2002) High-throughput approaches to study salivary proteins and genes from vectors of disease. Insect Biochem Mol Biol 32(10):1199–1209CrossRefPubMedGoogle Scholar
  93. van ZG KM, Mueller A, Dannenberg S, Gebert A, Solbach W, Laskay T (2004) Cutting edge: neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. J Immunol 173:6521–6525. PM:15557140CrossRefGoogle Scholar
  94. Volf P, Tesarova P, Nohynkova EN (2000) Salivary proteins and glycoproteins in phlebotomine sandflies of various species, sex and age. Med Vet Entomol 14:251–256. PM:11016431CrossRefPubMedGoogle Scholar
  95. Volf P, Hajmova M, Sadova J, Votypka J (2004) Blocked stomodeal valve of the insect vector: similar mechanism of transmission in two trypanosomatid models. Int J Parasitol 34:1221–1227CrossRefPubMedGoogle Scholar
  96. Walters LL, Modi GB, Tesh RB, Burrage T (1987) Host-parasite relationship of Leishmania mexicana mexicana and Lutzomyia abonnenci (Diptera: Psychodidae). Am J Trop Med Hyg 36(2):294–314CrossRefPubMedGoogle Scholar
  97. Walters LL, Modi GB, Chaplin GL, Tesh RB (1989) Ultrastructural development of Leishmania chagasi in its vector Lutzomyia longipalpis (Diptera: Psychodidae). Am J Trop Med Hyg 41(3):295–317CrossRefPubMedGoogle Scholar
  98. Walters LL, Irons KP, Modi GB, Tesh RB (1992) Refractory barriers in the sand fly Phlebotomus papatasi (Diptera: Psychodidae) to infection with Leishmania panamensis. Am J Trop Med Hyg 46:211–228. PM:1539756CrossRefPubMedGoogle Scholar
  99. Warburg A, Hamada GS, Schlein Y, Shire D (1986) The effect of post-blood-meal nutrition of Phlebotomus papatasi on the transmission of Leishmania major. Am J Trop Med Hyg 35:926–930CrossRefPubMedGoogle Scholar
  100. Warburg A, Saraiva E, Lanzaro GC, Titus RG, Neva F (1994) Saliva of Lutzomyia longipalpis sibling species differs in its composition and capacity to enhance leishmaniasis. Philos Trans R Soc Lond Ser B Biol Sci 345(1312):223–230CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Paulo F. P. Pimenta
    • 1
  • Vanessa C. de Freitas
    • 1
  • Carolina C. Monteiro
    • 1
  • Ana Clara M. A. Pires
    • 1
  • Nágila Francinete C. Secundino
    • 1
  1. 1.Instituto de Pesquisas René Rachou, Fundação Oswaldo CruzBelo HorizonteBrasil

Personalised recommendations