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Host–Parasite Interactions: Regulation of Leishmania Infection in Sand Fly

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Abstract

Purpose

Sand flies are the only proven vectors of leishmaniases, a tropical neglected disease endemic in at least 92 countries. Vector–parasite interactions play a significant role in vector-borne disease transmission. There are various bottlenecks to Leishmania colonization of the sand fly midgut. Such bottlenecks include the production of innate immune-related molecules, digestive proteases, parasite impermeable peritrophic membrane, and resident gut microbiota. These barriers determine the parasite load transmitted and, consequently, the disease outcome in mammalian host. Therefore, it is important to understand the molecular responses of both sand fly and Leishmania during infection.

Method

Here, we reviewed the published literature on sand fly–Leishmania interactions bringing together earlier and current findings to highlight new developments and research gaps in the field.

Conclusion

Recent research studies on sand fly–Leishmania interaction have revealed contrasting observations to past studies. However, how Leishmania parasites evade the sand fly immune response still needs further research. Sand fly response to Leishmania infection can be best understood by analyzing its tissue transcriptome. Better characterization of the role of midgut components could be a game changer in development of transmission-blocking strategies for leishmaniasis.

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References

  1. Maurício I (2018) Leishmania taxonomy. In: Bruschi F, Gradoni L (eds) The leishmaniases: old neglected tropical disease, 1st edn. Springer, pp 17–20 (Retrieved 13 Mar 2021)

    Google Scholar 

  2. Gossage S, Rogers M, Bates P (2003) Two separate growth phases during the development of Leishmania in sand flies: implications for understanding the life cycle. Int J Parasitol 33(10):1027–1034. https://doi.org/10.1016/s0020-7519(03)00142-5

    Article  PubMed  PubMed Central  Google Scholar 

  3. Rogers M, Bates P (2007) Leishmania manipulation of sand fly feeding behavior results in enhanced transmission. PLoS Pathog 3(6):e91. https://doi.org/10.1371/journal.ppat.0030091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Dvorak V, Shaw J, Volf P (2018) Parasite biology: the vectors. In: Bruschi F, Gradoni L (eds) The leishmaniases: old neglected tropical diseases, 1st edn. Springer, Cham, pp 31–40 (Retrieved 13 March 2021)

    Chapter  Google Scholar 

  5. WHO (2021) Leishmaniasis. Who.int. Retrieved 14 March 2021, from https://www.who.int/westernpacific/health-topics/leishmaniasis.

  6. Bates P, Depaquit J, Galati E, Kamhawi S, Maroli M, McDowell M et al (2015) Recent advances in phlebotomine sand fly research related to leishmaniasis control. Parasites Vectors 8(1):131. https://doi.org/10.1186/s13071-015-0712-x

    Article  PubMed  PubMed Central  Google Scholar 

  7. Killick-Kendrick R (1990) Phlebotomine vectors of the leishmaniases: a review. Med Vet Entomol 4(1):1–24. https://doi.org/10.1111/j.1365-2915.1990.tb00255.x

    Article  CAS  PubMed  Google Scholar 

  8. Oliveira F, Jochim R, Valenzuela J, Kamhawi S (2009) Sand flies, Leishmania, and transcriptome-borne solutions. Parasitol Int 58(1):1–5. https://doi.org/10.1016/j.parint.2008.07.004

    Article  PubMed  Google Scholar 

  9. Bates P (2007) Transmission of Leishmania metacyclic promastigotes by phlebotomine sand flies. Int J Parasitol 37(10):1097–1106

    Article  CAS  Google Scholar 

  10. Wilson R, Bates M, Dostalova A, Jecna L, Dillon R, Volf P, Bates P (2010) Stage-specific adhesion of Leishmania promastigotes to sand fly midguts assessed using an improved comparative binding assay. PLoS Negl Trop Dis 4(9):e816. https://doi.org/10.1371/journal.pntd.0000816

    Article  PubMed  PubMed Central  Google Scholar 

  11. Louradour I, Monteiro C, Inbar E, Ghosh K, Merkhofer R, Lawyer P et al (2017) The midgut microbiota plays an essential role in sand fly vector competence for Leishmania major. Cell Microbiol 19(10):e12755. https://doi.org/10.1111/cmi.12755

    Article  CAS  Google Scholar 

  12. Campolina T, Villegas L, Monteiro C, Pimenta P, Secundino N (2020) Tripartite interactions: Leishmania, microbiota and Lutzomyia longipalpis. PLoS Negl Trop Dis 14(10):e0008666. https://doi.org/10.1371/journal.pntd.0008666

    Article  PubMed  PubMed Central  Google Scholar 

  13. Kimblin N, Peters N, Debrabant A, Secundino N, Egen J, Lawyer P et al (2008) Quantification of the infectious dose of Leishmania major transmitted to the skin by single sand flies. Proc Natl Acad Sci 105(29):10125–10130. https://doi.org/10.1073/pnas.0802331105

    Article  PubMed  PubMed Central  Google Scholar 

  14. Stamper L, Patrick R, Fay M, Lawyer P, Elnaiem D, Secundino N et al (2011) Infection parameters in the sand fly vector that predict transmission of Leishmania major. PLoS Negl Trop Dis 5(8):e1288. https://doi.org/10.1371/journal.pntd.0001288

    Article  PubMed  PubMed Central  Google Scholar 

  15. Maia C, Seblova V, Sadlova J, Votypka J, Volf P (2011) Experimental transmission of Leishmania infantum by two major vectors: a comparison between a viscerotropic and a dermotropic strain. PLoS Negl Trop Dis 5(6):e1181. https://doi.org/10.1371/journal.pntd.0001181

    Article  PubMed  PubMed Central  Google Scholar 

  16. Secundino N, de Freitas V, Monteiro C, Pires A, David B, Pimenta P (2012) The transmission of Leishmania infantum chagasi by the bite of the Lutzomyia longipalpis to two different vertebrates. Parasites Vectors. https://doi.org/10.1186/1756-3305-5-20

    Article  PubMed  PubMed Central  Google Scholar 

  17. Yu X, Zhu Y, Ma C, Fabrick J, Kanost M (2002) Pattern recognition proteins in Manduca sexta plasma. Insect Biochem Mol Biol 32(10):1287–1293. https://doi.org/10.1016/s0965-1748(02)00091-7

    Article  CAS  PubMed  Google Scholar 

  18. Pal S, Wu LP (2009) Lessons from the fly: pattern recognition in Drosophila melanogaster. In: Kishore U (ed) Target pattern recognition in innate immunity. Advances in experimental medicine and biology, vol 653. Springer, New York NY, pp 45–46

    Google Scholar 

  19. Ramalho-Ortigão M, Jochim R, Anderson J, Lawyer P, Pham V, Kamhawi S, Valenzuela J (2007) Exploring the midgut transcriptome of Phlebotomus papatasi: comparative analysis of expression profiles of sugar-fed, blood-fed and Leishmania major-infected sand flies. BMC Genomics 8(1):300. https://doi.org/10.1186/1471-2164-8-300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Jochim R, Teixeira C, Laughinghouse A, Mu J, Oliveira F, Gomes R et al (2008) The midgut transcriptome of Lutzomyia longipalpis: comparative analysis of cDNA libraries from sugar-fed, blood-fed, post-digested and Leishmania infantum chagasi-infected sand flies. BMC Genomics 9(1):15. https://doi.org/10.1186/1471-2164-9-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Abrudan J, Ramalho-Ortigão M, O’Neil S, Stayback G, Wadsworth M, Bernard M et al (2013) The characterization of the Phlebotomus papatasi transcriptome. Insect Mol Biol 22(2):211–232. https://doi.org/10.1111/imb.12015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Sloan M, Sadlova J, Lestinova T, Sanders M, Cotton J, Volf P, Ligoxygakis P (2021) The Phlebotomus papatasi systemic transcriptional response to trypanosomatid-contaminated blood does not differ from the non-infected blood meal. Parasites Vectors. https://doi.org/10.1186/s13071-020-04498-0

    Article  PubMed  PubMed Central  Google Scholar 

  23. Boulanger N, Lowenberger C, Volf P, Ursic R, Sigutova L, Sabatier L et al (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(12):7140–7146. https://doi.org/10.1128/iai.72.12.7140-7146.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Hajmová M, Chang K, Kolli B, Volf P (2004) Down-regulation of gp63 in Leishmania amazonensis reduces its early development in Lutzomyia longipalpis. Microbes Infect 6(7):646–649. https://doi.org/10.1016/j.micinf.2004.03.003

    Article  CAS  PubMed  Google Scholar 

  25. Secundino N, Kimblin N, Peters N, Lawyer P, Capul A, Beverley S et al (2010) Proteophosphoglycan confers resistance of Leishmania major to midgut digestive enzymes induced by blood feeding in vector sand flies. Cell Microbiol 12(7):906–918. https://doi.org/10.1111/j.1462-5822.2010.01439.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Evans J, Aronstein K, Chen Y, Hetru C, Imler J, Jiang H et al (2006) Immune pathways and defense mechanisms in honey bees Apis mellifera. Insect Mol Biol 15(5):645–656. https://doi.org/10.1111/j.1365-2583.2006.00682.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Tanaka H, Ishibashi J, Fujita K, Nakajima Y, Sagisaka A, Tomimoto K et al (2008) A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochem Mol Biol 38(12):1087–1110. https://doi.org/10.1016/j.ibmb.2008.09.001

    Article  CAS  PubMed  Google Scholar 

  28. Clayton A, Dong Y, Dimopoulos G (2014) The Anopheles innate immune system in the defense against malaria infection. J Innate Immun 6(2):169–181. https://doi.org/10.1159/000353602

    Article  CAS  PubMed  Google Scholar 

  29. Klowden M (2007) Physiological systems in insects, 2nd edn. Elsevier/Academic Press, pp 378–382

    Google Scholar 

  30. Chapman R, Simpson S, Douglas A (2013) The insects, 5th edn. Cambridge University Press, pp 48–55 (64–65, 121–125)

    Google Scholar 

  31. Nation J (2015) Insect physiology and biochemistry, 3rd edn. Chapman and Hall/CRC, pp 45–50 (437-444)

    Google Scholar 

  32. Rosales C (2017) Cellular and molecular mechanisms of insect immunity. Insect Physiol Ecol. https://doi.org/10.5772/67107

    Article  Google Scholar 

  33. Di-Blasi T, Telleria E, Marques C, Couto R, Silva-Neves M, Jancarova M et al (2019) Lutzomyia longipalpis TGF-β has a role in Leishmania infantum chagasi survival in the vector. Front Cell Infect Microbiol. https://doi.org/10.3389/fcimb.2019.00071

    Article  PubMed  PubMed Central  Google Scholar 

  34. Telleria E, Azevedo-Brito D, Kykalová B, Tinoco-Nunes B, Pitaluga A, Volf P, Traub-Csekö Y (2021) Leishmania infantum infection modulates the Jak-STAT pathway in Lutzomyia longipalpis LL5 embryonic cells and adult females, and affects parasite growth in the sand fly. Front Trop Dis. https://doi.org/10.3389/fitd.2021.747820

    Article  Google Scholar 

  35. Louradour I, Ghosh K, Inbar E, Sacks D (2019) CRISPR/Cas9 mutagenesis in Phlebotomus papatasi: the immune deficiency pathway impacts vector competence for Leishmania major. MBio. https://doi.org/10.1128/mbio.01941-19

    Article  PubMed  PubMed Central  Google Scholar 

  36. Volf P, Kiewegova A, Nemec A (2002) Bacterial colonization in the gut of Phlebotomus duboscqi (Diptera: Psychodidae): transstadial passage and the role of female diet. Folia Parasitol 49(1):73–77. https://doi.org/10.14411/fp.2002.014

    Article  Google Scholar 

  37. Telleria E, Sant’Anna M, Alkurbi M, Pitaluga A, Dillon R, Traub-Csekö Y (2013) Bacterial feeding, Leishmania infection and distinct infection routes induce differential defensin expression in Lutzomyia longipalpis. Parasites Vectors 6(1):12. https://doi.org/10.1186/1756-3305-6-12

    Article  PubMed  PubMed Central  Google Scholar 

  38. Kykalová B, Tichá L, Volf P, Loza Telleria E (2021) Phlebotomus papatasi antimicrobial peptides in larvae and females and a gut-specific defensin upregulated by Leishmania major Infection. Microorganisms 9(11):2307. https://doi.org/10.3390/microorganisms9112307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Nimmo D, Ham P, Ward R, Maingon R (1997) The sand fly Lutzomyia longipalpis shows specific humoral responses to bacterial challenge. Med Vet Entomol 11(4):324–328. https://doi.org/10.1111/j.1365-2915.1997.tb00417.x

    Article  CAS  PubMed  Google Scholar 

  40. Dillon R, Ivens A, Churcher C, Holroyd N, Quail M, Rogers M et al (2006) Analysis of ESTs from Lutzomyia longipalpis sand flies and their contribution toward understanding the insect–parasite relationship. Genomics 88(6):831–840. https://doi.org/10.1016/j.ygeno.2006.06.011

    Article  CAS  PubMed  Google Scholar 

  41. Pitaluga A, Beteille V, Lobo A, Ortigão-Farias J, Dávila A, Souza A et al (2009) EST sequencing of blood-fed and Leishmania-infected midgut of Lutzomyia longipalpis, the principal visceral leishmaniasis vector in the Americas. Mol Genet Genom 282(3):307–317. https://doi.org/10.1007/s00438-009-0466-2

    Article  CAS  Google Scholar 

  42. Dostálová A, Votýpka J, Favreau A, Barbian K, Volf P, Valenzuela J, Jochim R (2011) The midgut transcriptome of Phlebotomus (Larroussius) perniciosus, a vector of Leishmania infantum: comparison of sugar fed and blood fed sand flies. BMC Genom. https://doi.org/10.1186/1471-2164-12-223

    Article  Google Scholar 

  43. Coutinho-Abreu I, Serafim T, Meneses C, Kamhawi S, Oliveira F, Valenzuela J (2020) Leishmania infection induces a limited differential gene expression in the sand fly midgut. BMC Genom. https://doi.org/10.1186/s12864-020-07025-8

    Article  Google Scholar 

  44. Dong Y, Aguilar R, Xi Z, Warr E, Mongin E, Dimopoulos G (2006) Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog 2(6):e52. https://doi.org/10.1371/journal.ppat.0020052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Bahia A, Kubota M, Tempone A, Pinheiro W, Tadei W, Secundino N et al (2010) Anopheles aquasalis infected by Plasmodium vivax displays unique gene expression profiles when compared to other malaria vectors and plasmodia. PLoS ONE 5(3):e9795. https://doi.org/10.1371/journal.pone.0009795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Smagghe G, Goodman C, Stanley D (2009) Insect cell culture and applications to research and pest management. In Vitro Cell Dev Biol Anim 45(3–4):93–105. https://doi.org/10.1007/s11626-009-9181-x

    Article  PubMed  Google Scholar 

  47. Tinoco-Nunes B, Telleria E, da Silva-Neves M, Marques C, Azevedo- Brito D, Pitaluga A, Traub-Csekö Y (2016) The sand fly Lutzomyia longipalpis LL5 embryonic cell line has active Toll and Imd path- ways and shows immune responses to bacteria, yeast and Leishmania. Parasites Vectors. https://doi.org/10.1186/s13071-016-1507-4

    Article  PubMed  PubMed Central  Google Scholar 

  48. da Silva Gonçalves D, Iturbe-Ormaetxe I, Martins-da-Silva A, Telleria E, Rocha M, Traub-Csekö Y et al (2019) Wolbachia introduction into Lutzomyia longipalpis (Diptera: Psychodidae) cell lines and its effects on immune-related gene expression and interaction with Leishmania infantum. Parasites Vectors. https://doi.org/10.1186/s13071-018-3227-4

    Article  PubMed  PubMed Central  Google Scholar 

  49. Telleria E, Tinoco-Nunes B, Leštinová T, de Avellar L, Tempone A, Pitaluga A et al (2021) Lutzomyia longipalpis antimicrobial peptides: differential expression during development and potential involvement in vector interaction with microbiota and Leishmania. Microorganisms 9(6):1271. https://doi.org/10.3390/microorganisms9061271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Jing T, Qi F, Wang Z (2020) Most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision. Microbiome. https://doi.org/10.1186/s40168-020-00823-y

    Article  PubMed  PubMed Central  Google Scholar 

  51. Omondi ZN, Demir S (2020) Bacteria composition and diversity in the gut of sand fly: impact on Leishmania and sand fly development. Int J Trop Insect Sci 41(1):25–32. https://doi.org/10.1007/s42690-020-00184-x

    Article  Google Scholar 

  52. Telleria E, Sant’Anna M, Ortigão-Farias J, Pitaluga A, Dillon V, Bates P et al (2012) Caspar-like gene depletion reduces Leishmania infection in sand fly host Lutzomyia longipalpis. J Biol Chem 287(16):12985–12993. https://doi.org/10.1074/jbc.m111.331561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Bang I (2019) JAK/STAT signaling in insect innate immunity. Entomol Res 49(8):339–353. https://doi.org/10.1111/1748-5967.12384

    Article  CAS  Google Scholar 

  54. Gupta L, Molina-Cruz A, Kumar S, Rodrigues J, Dixit R, Zamora R, Barillas-Mury C (2009) The STAT pathway mediates late-phase immunity against Plasmodium in the mosquito Anopheles gambiae. Cell Host Microbe 5(5):498–507. https://doi.org/10.1016/j.chom.2009.04.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Bahia A, Kubota M, Tempone A, Araújo H, Guedes B, Orfanó A et al (2011) The JAK-STAT pathway controls Plasmodium vivax load in early stages of Anopheles aquasalis infection. PLoS Negl Trop Dis 5(11):e1317. https://doi.org/10.1371/journal.pntd.0001317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Lehane M (1997) Peritrophic matrix structure and function. Annu Rev Entomol 42(1):525–550. https://doi.org/10.1146/annurev.ento.42.1.525

    Article  CAS  PubMed  Google Scholar 

  57. Hegedus D, Erlandson M, Gillott C, Toprak U (2009) New insights into peritrophic matrix synthesis, architecture, and function. Annu Rev Entomol 54(1):285–302. https://doi.org/10.1146/annurev.ento.54.110807.090559

    Article  CAS  PubMed  Google Scholar 

  58. Blackburn K, Wallbanks K, Molyneux D, Lavin D, Winstanley S (1988) The peritrophic membrane of the female sand fly Phlebotomus papatasi. Ann Trop Med Parasitol 82(6):613–619. https://doi.org/10.1080/00034983.1988.11812297

    Article  CAS  PubMed  Google Scholar 

  59. Devenport M, Alvarenga P, Shao L, Fujioka H, Bianconi M, Oliveira P, Jacobs-Lorena M (2006) Identification of the Aedes aegypti peritrophic matrix protein AeIMUCI as a heme-binding protein. Biochemistry 45(31):9540–9549. https://doi.org/10.1021/bi0605991

    Article  CAS  PubMed  Google Scholar 

  60. Pimenta P, Modi G, Pereira S, Shahabuddin M, Sacks D (1997) A novel role for the peritrophic matrix in protecting Leishmania from the hydrolytic activities of the sand fly midgut. Parasitology 115(4):359–369. https://doi.org/10.1017/s0031182097001510

    Article  PubMed  Google Scholar 

  61. Schlein Y, Schnur L, Jacobson R (1990) Released glycoconjugate of indigenous Leishmania major enhances survival of a foreign L. major in Phlebotomus papatasi. Trans R Soc Trop Med Hyg 84(3):353–355. https://doi.org/10.1016/0035-9203(90)90315-6

    Article  CAS  PubMed  Google Scholar 

  62. Rogers M, Hajmová M, Joshi M, Sadlova J, Dwyer D, Volf P, Bates P (2008) Leishmania chitinase facilitates colonization of sand fly vectors and enhances transmission to mice. Cell Microbiol 10(6):1363–1372. https://doi.org/10.1111/j.1462-5822.2008.01132.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Sádlová J, Volf P (2009) Peritrophic matrix of Phlebotomus duboscqi and its kinetics during Leishmania major development. Cell Tissue Res 337(2):313–325. https://doi.org/10.1007/s00441-009-0802-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Pruzinova K, Sadlova J, Seblova V, Homola M, Votypka J, Volf P (2015) Comparison of bloodmeal digestion and the peritrophic matrix in four sand fly species differing in susceptibility to Leishmania donovani. PLoS ONE 10(6):e0128203. https://doi.org/10.1371/journal.pone.0128203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Sadlova J, Dvorak V, Seblova V, Warburg A, Votypka J, Volf P (2013) Sergentomyia schwetzi is not a competent vector for Leishmania donovani and other Leishmania species pathogenic to humans. Parasit Vectors 6:186–196

    Article  Google Scholar 

  66. Sadlova J, Homola M, Myskova J, Jancarova M, Volf P (2018) Refractoriness of Sergentomyia schwetzi to Leishmania spp. is mediated by the peritrophic matrix. PLOS Negl Trop Dis 12(4):e0006382

    Article  Google Scholar 

  67. Telleria E, Araújo A, Secundino N, d’Avila-Levy C, Traub-Csekö Y (2010) Trypsin-like serine proteases in Lutzomyia longipalpis – expression, activity and possible modulation by Leishmania infantum chagasi. PLoS ONE 5(5):e10697. https://doi.org/10.1371/journal.pone.0010697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Cao X, Gulati M, Jiang H (2017) Serine protease-related proteins in the malaria mosquito, Anopheles gambiae. Insect Biochem Mol Biol 88:48–62. https://doi.org/10.1016/j.ibmb.2017.07.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Ramalho-Ortigao M, Saraiva E, Traub-Csekö Y (2010) Sand fly-Leishmania interactions: long relationships are not necessarily easy. Open Parasitol J 4(1):195–204. https://doi.org/10.2174/1874421401004010195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Schlein Y, Romano H (1986) Leishmania major and L. donovani: effects on proteolytic enzymes of Phlebotomus papatasi (Diptera, Psychodidae). Exp Parasitol 62(3):376–380. https://doi.org/10.1016/0014-4894(86)90045-7

    Article  CAS  PubMed  Google Scholar 

  71. Dillon RJ, Lane RP (1993) Influence of Leishmania infection on blood- meal digestion in the sandflies Phlebotomus papatasi and P. langeroni. Parasitol Res 79:492–496

    Article  CAS  Google Scholar 

  72. Lawyer P, Githure J, Roberts C, Anjili C, Mebrahtu Y, Ngumbi P et al (1990) Development of Leishmania major in Phlebotomus duboscqi and Sergentomyia schwetzi (Diptera: Psychodidae). Am J Trop Med Hyg 43(1):31–43. https://doi.org/10.4269/ajtmh.1990.43.31

    Article  CAS  PubMed  Google Scholar 

  73. Sant’Anna M, Diaz-Albiter H, Mubaraki M, Dillon R, Bates P (2009) Inhibition of trypsin expression in Lutzomyia longipalpis using RNAi enhances the survival of Leishmania. Parasit Vectors 2(1):62. https://doi.org/10.1186/1756-3305-2-62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Verma S, Das S, Mandal A, Ansari M, Kumari S, Mansuri R, Kumar A, Singh R, Saini S, Abhishek K, Kumar V, Sahoo G, Das P (2017) Role of inhibitors of serine peptidases in protecting Leishmania donovani against the hydrolytic peptidases of sand fly midgut. Parasites Vectors. https://doi.org/10.1186/s13071-017-2239-9

    Article  PubMed  PubMed Central  Google Scholar 

  75. Sacks DL et al (2000) The role of phosphoglycans in Leishmania- sand fly interactions. Proc Natl Acad Sci USA 97:406–411

    Article  CAS  Google Scholar 

  76. Dostalova A, Volf P (2012) Leishmania development in sand flies: parasite-vector interactions overview. Parasites Vectors 5:276. https://doi.org/10.1186/1756-3305-5-276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Moraes C, Lucena S, Moreira B, Brazil R, Gontijo N, Genta F (2012) Relationship between digestive enzymes and food habit of Lutzomyia longipalpis (Diptera: Psychodidae) larvae: characterization of carbohydrases and digestion of microorganisms. J Insect Physiol 58(8):1136–1145. https://doi.org/10.1016/j.jinsphys.2012.05.015

    Article  CAS  PubMed  Google Scholar 

  78. Peterkova-Koci K, Robles-Murguia M, Ramalho-Ortigao M, Zurek L (2012) Significance of bacteria in oviposition and larval development of the sand fly Lutzomyia longipalpis. Parasit Vectors 5(1):145. https://doi.org/10.1186/1756-3305-5-145

    Article  PubMed  PubMed Central  Google Scholar 

  79. Diaz-Albiter H, Sant’Anna M, Genta F, Dillon R (2012) Reactive oxygen species-mediated immunity against Leishmania mexicana and Serratia marcescens in the Phlebotomine sand fly Lutzomyia longipalpis. J Biol Chem 287(28):23995–24003. https://doi.org/10.1074/jbc.m112.376095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Sant’Anna M, Diaz-Albiter H, Aguiar-Martins K, Al Salem W, Cavalcante R, Dillon V et al (2014) Colonization resistance in the sand fly gut: Leishmania protects Lutzomyia longipalpis from bacterial infection. Parasites Vectors 7(1):329. https://doi.org/10.1186/1756-3305-7-329

    Article  PubMed  PubMed Central  Google Scholar 

  81. Marayati B, Schal C, Ponnusamy L, Apperson C, Rowland T, Wasserberg G (2015) Attraction and oviposition preferences of Phlebotomus papatasi (Diptera: Psychodidae), vector of old-world cutaneous leishmaniasis, to larval rearing media. Parasites Vectors. https://doi.org/10.1186/s13071-015-1261-z

    Article  PubMed  PubMed Central  Google Scholar 

  82. Kelly P, Bahr S, Serafim T, Ajami N, Petrosino J, Meneses C et al (2017) The gut microbiome of the vector Lutzomyia longipalpis is essential for survival of Leishmania infantum. MBio 8(1):e01121-e1216. https://doi.org/10.1128/mbio.01121-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Telleria EL, Martins-da-Silva A, Tempone AJ, Traub-Csekö YM (2018) Leishmania, microbiota and sand fly immunity. Parasitology 145(10):1336–1353. https://doi.org/10.1017/s0031182018001014

    Article  PubMed  Google Scholar 

  84. Hurwitz I, Hillesland H, Fieck A, Das P, Durvasula R (2011) The paratransgenic sand fly: a platform for control of Leishmania transmission. Parasites Vectors. https://doi.org/10.1186/1756-3305-4-82

    Article  PubMed  PubMed Central  Google Scholar 

  85. Wu S, Liao C, Pan R, Juang J (2012) Infection-induced intestinal oxidative stress triggers organ-to-organ immunological communication in Drosophila. Cell Host Microbe 11(4):410–417. https://doi.org/10.1016/j.chom.2012.03.004

    Article  CAS  PubMed  Google Scholar 

  86. Kamhawi S (2006) Phlebotomine sand flies and Leishmania parasites: friends or foes? Trends Parasitol 22(9):439–445. https://doi.org/10.1016/j.pt.2006.06.012

    Article  PubMed  Google Scholar 

  87. Volf P, Myskova J (2007) Sand flies and Leishmania: specific versus permissive vectors. Trends Parasitol 23(3):91–92. https://doi.org/10.1016/j.pt.2006.12.010

    Article  PubMed  PubMed Central  Google Scholar 

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Omondi, Z.N., Arserim, S.K., Töz, S. et al. Host–Parasite Interactions: Regulation of Leishmania Infection in Sand Fly. Acta Parasit. 67, 606–618 (2022). https://doi.org/10.1007/s11686-022-00519-3

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