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Parasite-Vector Interactions

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Abstract

In the most important protozoan tropical diseases – malaria, leishmaniosis, sleeping sickness and Chagas disease – the parasites are transmitted to humans by specific vectors: the sporozoan Plasmodium spp. by female Anopheles mosquitoes, Leishmania spp. by female sandflies, Trypanosoma brucei ssp. by both gender of tsetse flies and Trypanosoma cruzi by all stages of triatomines. In the lumen of the vector´s gut, all parasites are confronted with the digestive enzymes of the insect and its intestinal immune reactions but also to the microbial fauna. If the parasites are transmitted via the saliva, they must also evade the immune reactions during their way to and in the salivary glands. On the molecular base, specific surface components of the parasites and respective receptors of the insect induce an attachment to or an invasion of the respective tissue, the development of infectious stages and/or immune reactions. In refractory vectors, the latter kill the parasites, but in susceptible vectors at least some parasites survive and can be transmitted. Since full genome sequences are available for many vector species and parasites, modern genomic and proteomic analyses will perhaps identify targets for control of parasite development in the vector.

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References

  • Abraham EG, Jacobs-Lorena M (2004) Mosquito midgut barriers to malaria parasite development. Insect Biochem Mol Biol 34:667–671

    Article  CAS  PubMed  Google Scholar 

  • Acosta-Serrano A, Vassella E, Liniger M, Kunz Renggli C, Brun R (2001) The surface coat of procyclic Trypanosoma brucei: programmed expression and proteolytic cleavage of procyclin in the tsetse fly. Proc Natl Acad Sci USA 98:1513–1518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adini A, Warburg A (1999) Interaction of Plasmodium gallinaceum ookinetes and oocysts with extracellular matrix proteins. Parasitology 119:331–336

    Article  CAS  PubMed  Google Scholar 

  • Aksoy S, Gibson WC, Lehane MJ (2003) Interactions between tsetse and trypanosomes with implications for the control of trypanosomiasis. Adv Parasitol 53:1–83

    Article  PubMed  Google Scholar 

  • Aksoy S, Weiss BL, Attardo GM (2014) Trypanosome transmission dynamics in tsetse. Curr Opin Insect Sci 3:43–49

    Article  PubMed  PubMed Central  Google Scholar 

  • Alam U, Medlock J, Brelsfoard C, Pais R, Lohs C et al. (2011) Wolbachia symbiont infections induces strong cytoplasmic incompatibility in the tsetse fly Glossina morsitans. PLoS Pathog 7, e1002415. doi:10.1371/journal.ppat.1002415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alves CR, Albuquerque-Cunha JM, Mello CB, Garcia ES, Nogueira NF et al. (2007) Trypanosoma cruzi attachment to perimicrovillar membrane glycoproteins of Rhodnius prolixus. Exp Parasitol 116:44–52

    Article  CAS  PubMed  Google Scholar 

  • Aly ASI, Vaughan AM, Kappe SHI (2009) Malaria parasite development in the mosquito and infection of the mammalian host. Annu Rev Microbiol 63:195–221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Araújo Soares RM, Souza dos Santos AL, Bonaldo MC, Andrade AFB, Alviano CS et al. (2003) Leishmania (Leishmania) amazonensis: differential expression of proteinases and cell-surface polypeptides in avirulent and virulent promastigotes. Exp Parasitol 104:104–112

    Article  PubMed  CAS  Google Scholar 

  • Armengaud J, Christie-Oleza JA, Clair G, Malard V, Duport C (2012) Exoproteomics: exploring the world around biological systems. Expert Rev Proteomic 9:561–575

    Article  CAS  Google Scholar 

  • Arrighi RBG, Lycett G, Mahairaki V, Siden-Kiamos I, Louis C (2005) Laminin and the malaria parasite's journey through the mosquito midgut. J Exp Biol 208:2497–2502

    Article  PubMed  Google Scholar 

  • Ashford RW (1997) The leishmaniases as model zoonoses. Ann Trop Med Parasitol 9:693–702

    Article  Google Scholar 

  • Ashford RW (2000) The leishmaniases as emerging and reemerging zoonoses. Int J Parasitol 30:1269–1281

    Article  CAS  PubMed  Google Scholar 

  • Atayde VD, Aslan H, Townsend S, Hassani K, Kamhawi S, Olivier M (2015) Exosome secretion by the parasitic protozoan Leishmania within the sandfly midgut. Cell Rep 13:957–967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Atwood JA, Weatherly DB, Minning TA, Bundy B, Cavola C et al. (2005) The Trypanosoma cruzi proteome. Science 309:473–476

    Article  CAS  PubMed  Google Scholar 

  • Atyame Nten CM, Sommerer N, Rofidal V, Hirtz C, Rossignol M et al. (2010) Excreted/secreted proteins from trypanosome procyclic strains. J Biomed Biotechnol 2010:212817. doi:10.1155/2010/212817

    Article  PubMed  CAS  Google Scholar 

  • Ávila AR, Dallagiovanna B, Yamada-Ogatta SF, Monteiro-Góes V, Fragoso SP et al. (2003) Stage-specific gene expression during Trypanosoma cruzi metacyclogenesis. Genet Mol Res 2:159–168

    PubMed  Google Scholar 

  • Azambuja P, Garcia ES, Ratcliffe NA (2005) Gut microbiota and parasite transmission by insect vectors. Trends Parasitol 21:568–572

    Article  PubMed  Google Scholar 

  • Bahia AC, Kubota MS, Tempone AJ, Araújo HRC, Guedes BAM et al. (2011) The JAK-STAT pathway controls Plasmodium vivax load in early stages of Anopheles aquasalis infection. PLoS Negl Trop Dis 5, e1317. doi:10.1371/journal.pntd.0001317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baida RCP, Santos MRM, Carmo MS, Yoshida N, Ferreira D et al. (2006) Molecular characterization of serine-, alanine-, and proline-rich proteins of Trypanosoma cruzi and their possible role in host cell infection. Infect Immun 74:1537–1546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balczun C, Siemanowski J, Pausch JK, Helling S, Marcus K et al. (2012) Intestinal aspartate proteases TiCatD and TiCatD2 of the haematophagous bug Triatoma infestans (Reduviidae): sequence characterisation, expression pattern and characterisation of proteolytic activity. Insect Biochem Mol Biol 42:240–250

    Article  CAS  PubMed  Google Scholar 

  • Barillas-Mury C (2007) CLIP proteases and Plasmodium melanization in Anopheles gambiae. Trends Parasitol 23:297–299

    Article  CAS  PubMed  Google Scholar 

  • Bates PA (2008) Leishmania sandfly interaction: progress and challenges. Curr Opin Microbiol 11:340–344

    Article  PubMed  PubMed Central  Google Scholar 

  • Bates PA, Rogers ME (2004) New insights into the developmental biology and transmission mechanisms of Leishmania. Curr Mol Med 4:601–609

    Article  CAS  PubMed  Google Scholar 

  • Bates PA, Depaquit J, Galati EAB, Kamhawi S, Maroli M et al. (2015) Recent advances in phlebotomine sandfly research related to leishmaniasis control. Parasit Vectors 8:131. doi:10.1186/s13071-015-0712-x

    Article  PubMed  PubMed Central  Google Scholar 

  • Baton LA, Robertson A, Warr E, Strand MR, Dimopoulos G (2009) Genome-wide transcriptomic profiling of Anopheles gambiae hemocytes reveals pathogen-specific signatures upon bacterial challenge and Plasmodium berghei infection. BMC Genomics 10:257. doi:10.1186/1471-2164-10-257

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bayer-Santos E, Aguilar-Bonavides C, Rodrigues SP, Cordero EM, Marques AF et al. (2013) Proteomic analysis of Trypanosoma cruzi secretome: characterization of two populations of extracellular vesicles and soluble proteins. J Proteome Res 12:883–897

    Article  CAS  PubMed  Google Scholar 

  • Beier JC, Koros JK (1991) Anatomical dissemination of circumsporozoite protein in wild Afrotropical Anopheles affects malaria sporozoite rate determination by ELISA. Med Vet Entomol 5:81–85

    Article  CAS  PubMed  Google Scholar 

  • Besansky NJ (2015) Genome analysis of vectorial capacity in major Anopheles vectors of malaria parasites. https://www.vectorbase.org/projects/genome-analysis-vectorial-capacity-major-anopheles-vectors-malaria-parasites. Accessed 7 Dec 2015

  • Billingsley PF (1990) The midgut ultrastructure of hematophagous insects. Annu Rev Entomol 35:219–248

    Article  Google Scholar 

  • Billingsley PF, Rudin W (1992) The role of the mosquito peritrophic membrane in bloodmeal digestion and infectivity of Plasmodium species. J Parasitol 78:430–440

    Article  CAS  PubMed  Google Scholar 

  • Blandin S, Shiao SH, Moita LF, Janse CJ, Waters AP et al. (2004) Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116:661–670

    Article  CAS  PubMed  Google Scholar 

  • Boissière A, Tchioffo MT, Bachar D, Abate L, Marie A et al. (2012) Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with Plasmodium falciparum infection. PLoS Pathog 8, e1002742. doi:10.1371/journal.ppat.1002742

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bonay P, Molina R, Fresno M (2001) Binding specificity of mannose-specific carbohydrate-binding protein from the cell surface of Trypanosoma cruzi. Glycobiology 11:719–729

    Article  CAS  PubMed  Google Scholar 

  • Bongio NJ, Lampe DJ (2015) Inhibition of Plasmodium berghei development in mosquitoes by effector proteins secreted from Asaia sp. bacteria using a novel native secretion signal. PLoS ONE 10:e0143541. doi:10.1371/journal.pone.0143541

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Boulanger N, Brun R, Ehret-Sabatier L, Kunz C, Bulet P (2002) Immunopeptides in the defense reactions of Glossina morsitans to bacterial and Trypanosoma brucei brucei infections. Insect Biochem Mol Biol 32:369–375

    Article  CAS  PubMed  Google Scholar 

  • Boulanger N, Lowenberger C, Volf P, Ursic R, Sigutova L et al. (2004) Characterization of a defensin from the sandfly Phlebotomus duboscqi induced by challenge with bacteria or the protozoan parasite Leishmania major. Infect Immun 72:7140–7146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brun R, Blum J, Chappuis F, Burri C (2010) Human African trypanosomiasis. Lancet 375:148–159

    Article  PubMed  Google Scholar 

  • Brunoro GVF, Caminha MA, da Silva Ferreira AT, da Veiga LF, Carvalho PC et al. (2015) Reevaluating the Trypanosoma cruzi proteomic map: the shotgun description of bloodstream trypomastigotes. J Proteomics 115:58–65

    Article  CAS  PubMed  Google Scholar 

  • Buarque DS, Gomes CM, Araújo RN, Pereira MH, Ferreira RC et al. (2016) A new antimicrobial protein from the anterior midgut of Triatoma infestans mediates Trypanosoma cruzi establishment by controlling the microbiota. Biochimie 123:138–143

    Article  CAS  PubMed  Google Scholar 

  • Buscaglia CA, Campo VA, Frasch AC, Di Noia JM (2006) Trypanosoma cruzi surface mucins: host-dependent coat diversity. Nat Rev Microbiol 4:229–236

    Article  CAS  PubMed  Google Scholar 

  • Butter F, Bucerius F, Michel M, Cicova Z, Mann M et al. (2013) Comparative proteomics of two life cycle stages of stable isotope-labeled Trypanosoma brucei reveals novel components of the parasite´s host adaptation machinery. Mol Cell Proteomics 12:172–179

    Article  PubMed  CAS  Google Scholar 

  • Castro DP, Moraes CS, Gonzalez MS, Ratcliffe NA, Azambuja P et al. (2012) Trypanosoma cruzi immune response modulation decreases microbiota in Rhodnius prolixus gut and is crucial for parasite survival and development. PLOS One 7(5), e36591. doi:10.1371/journal.pone.0036591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cázares-Raga FE, Chávez-Munguía B, González-Calixto C, Ochoa-Franco AP, Gawinowicz MA et al. (2014) Morphological and proteomic characterization of midgut of the malaria vector Anopheles albimanus at early time after a blood feeding. J Proteomics 111:100–112

    Article  PubMed  CAS  Google Scholar 

  • Champagne DE (2004) Antihemostatic strategies of blood-feeding arthropods. Curr Drug Targets Cardiovasc Haematol Disord 4:375–396

    Article  CAS  PubMed  Google Scholar 

  • Chandra M, Liniger M, Tetley L, Roditi I, Barry JD (2004) TsetseEP, a gut protein from the tsetse Glossina morsitans, is related to a major surface glycoprotein of trypanosomes transmitted by the fly and to the products of a Drosophila gene family. Insect Biochem Mol Biol 34:1163–1173

    Article  CAS  PubMed  Google Scholar 

  • Chouaia B, Rossi P, Montagna M, Ricci I, Crotti E et al. (2010) Molecular evidence for multiple infections as revealed by typing of Asaia bacterial symbionts of four mosquito species. Appl Environ Microbiol 76:7444–7450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Contreras VT, Morel CM, Goldenberg S (1985) Stage specific gene expression precedes morphological changes during Trypanosoma cruzi metacyclogenesis. Mol Biochem Parasitol 14:83–96

    Article  CAS  PubMed  Google Scholar 

  • Cordero EM, Gentil LG, Crisante G, Ramírez JL, Yoshida N et al. (2008) Expression of GP82 and GP90 surface glycoprotein genes of Trypanosoma cruzi during in vivo metacyclogenesis in the insect vector Rhodnius prolixus. Acta Trop 105:87–91

    Article  CAS  PubMed  Google Scholar 

  • Cornelie S, Rossignol M, Seveno M, Demettre E, Mouchet F et al. (2014) Salivary gland proteome analysis reveals modulation of anopheline unique proteins in insensitive acetylcholinesterase resistant Anopheles gambiae mosquitoes. PLoS ONE 9, e103816. doi:10.1371/journal.pone.0103816

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cortez C, Sobreira TJP, Maeda FY, Yoshida N (2014) The gp82 surface molecule of Trypanosoma cruzi metacyclic forms. In: Santos ALS, Branquinha MH, d’Avila-Levy CM, Kneipp LF, Sodré CL (eds) Proteins and proteomics of Leishmania and Trypanosoma. Subcellular Biochemistry, vol 74. Springer, Dordrecht, pp 137–150

    Google Scholar 

  • Coutinho-Abreu IV, Ramalho-Ortigao M (2010) Transmission blocking vaccines to control insect-borne diseases: a review. Mem Inst Oswaldo Cruz 105:1–12

    Article  CAS  PubMed  Google Scholar 

  • Coutinho-Abreu IV, Sharma NK, Robles-Murguia M, Ramalho-Ortigao M (2010) Targeting the midgut secreted PpChit1 reduces Leishmania major development in its natural vector, the sandfly Phlebotomus papatasi. PLoS Negl Trop Dis 4, e901. doi:10.1371/journal.pntd.0000901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dale C, Maudlin I (1999) Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans. Int J Syst Bacteriol 49:267–275

    Article  CAS  PubMed  Google Scholar 

  • Dale C, Welburn SC (2001) The endosymbionts of tsetse flies: manipulating host-parasite interactions. Int J Parasitol 31:628–631

    Article  CAS  PubMed  Google Scholar 

  • DaMatta RA, Seabra SH, Deolindo P, Arnholdt ACV, Manhaes L et al. (2007) Trypanosoma cruzi exposes phosphatidylserine as an evasion mechanism. FEMS Microbiol Lett 266:29–33

    Article  CAS  PubMed  Google Scholar 

  • da Mota FF, Marinho LP, Moreira CJ, Lima MM, Mello CB et al. (2012) Cultivation-independent methods reveal differences among bacterial gut microbiota in triatomine vectors of Chagas disease. PLOS Neglect Trop D 6(5), e1631. doi:10.1371/journal.pntd.0001631

    Article  CAS  Google Scholar 

  • d’Avila-Levy CM, Altoe EC, Uehara LA, Branquinha MH, Santos AL (2014) GP63 function in the interaction of trypanosomatids with the invertebrate host: facts and prospects. In: Santos ALS, Branquinha MH, d’Avila-Levy CM, Kneipp LF, Sodré CL (eds) Proteins and proteomics of Leishmania and Trypanosoma. Subcellular Biochemistry, vol 74. Springer, Dordrecht, pp 253–270

    Google Scholar 

  • de Godoy LM, Marchini FK, Pavoni DP, Rampazzo Rde C, Probst CM et al. (2012) Quantitative proteomics of Trypanosoma cruzi during metacyclogenesis. Proteomics 12:2694–2703

    Article  PubMed  CAS  Google Scholar 

  • de Jesus JB, Mesquita-Rodrigues C, Cuervo P (2014) Proteomics advances in the study of Leishmania parasites and leishmaniasis. In: Santos ALS, Branquinha MH, d’Avila-Levy CM, Kneipp LF, Sodré CL (eds) Proteins and proteomics of Leishmania and Trypanosoma, vol 74, Subcellular Biochemistry. Springer, Dordrecht, pp 323–349

    Chapter  Google Scholar 

  • De Vooght L, Caljon G, Van Hees J, Van Den Abbeele J (2015) Paternal transmission of a secondary symbiont during mating in the viviparous tsetse fly. Mol Biol Evol 32:1977–1980

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dean S, Marchetti R, Kirk K, Matthews KR (2009) A surface transporter family conveys the trypanosome differentiation signal. Nature 459:213–217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dessens JT, Beetsma AL, Dimopoulos G, Wengelnik K, Crisanti A et al. (1999) CTRP is essential for mosquito infection by malaria ookinetes. EMBO J 18:6221–6227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dessens JT, Sidén-Kiamos I, Mendoza J, Mahairaki V, Khater E et al. (2003) SOAP, a novel malaria ookinete protein involved in mosquito midgut invasion and oocyst development. Mol Microbiol 49:319–329

    Article  CAS  PubMed  Google Scholar 

  • Dias F de A, Guerra B, Vieira LR, Perdomo HD, Gandara ACP et al. (2015) Monitoring of the parasite load in the digestive tract of Rhodnius prolixus by combined qPCR analysis and imaging techniques provides new insights into the trypanosome life cycle. PLOS Neglect Trop D 9(10), e0004186. doi:10.1371/journal.pntd.0004186

    Article  Google Scholar 

  • Diaz-Albiter H, Sant'Anna MRV, Genta FA, Dillon RJ (2012) Reactive oxygen species-mediated immunity against Leishmania mexicana and Serratia marcescens in the phlebotomine sand fly Lutzomyia longipalpis. J Biol Chem 287:23995–24003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dimopoulos G, Müller H, Levashina EA, Kafatos FC (2001) Innate immune defense against malaria infection in the mosquito. Curr Opin Immunol 13:79–88

    Article  CAS  PubMed  Google Scholar 

  • Dinglasan RR, Alaganan A, Ghosh AK, Saito A, van Kuppevelt TH et al. (2007) Plasmodium falciparum ookinetes require mosquito midgut chondroitin sulfate proteoglycans for cell invasion. Proc Natl Acad Sci USA 104:15882–15887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dostálová A, Volf P (2012) Leishmania development in sandflies: parasite-vector interactions overview. Parasit Vectors 5:276. doi:10.1186/1756-3305-5-276

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dyer NA, Rose C, Ejeh NO, Acosta-Serrano A (2013) Flying tryps: survival and maturation of trypanosomes in tsetse flies. Trends Parasitol 29:188–196

    Article  PubMed  Google Scholar 

  • Eappen AG, Smith RC, Jacobs-Lorena M (2013) Enterobacter-activated mosquito immune responses to Plasmodium involve activation of SRPN6 in Anopheles stephensi. PLoS ONE 8, e62937. doi:10.1371/journal.pone.0062937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eichler S, Schaub GA (2002) Development of symbionts in triatomine bugs and the effects of infections with trypanosomatids. Exp Parasitol 100:17–27

    Article  CAS  PubMed  Google Scholar 

  • Eichler S, Reintjes N, Jung M, Yassin AF, Schaal KP et al. (1996) Identification of bacterial isolates and symbionts from wild populations of Triatoma infestans and T. sordida. Mem Inst Oswaldo Cruz 91 Suppl:125

    Google Scholar 

  • El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G et al. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of chagas disease. Science 309:409–415

    Article  CAS  PubMed  Google Scholar 

  • Engstler M, Boshart M (2004) Cold shock and regulation of surface protein trafficking convey sensitization to inducers of stage differentiation in Trypanosoma brucei. Genes Dev 18:2798–2811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ennes-Vidal V, Menna-Barreto RFS, Santos ALS, Branquinha MH, d’Avila-Levy CM (2011) MDL28170, a calpain inhibitor, affects Trypanosoma cruzi metacyclogenesis, ultrastructure and attachment to Rhodnius prolixus midgut. PLOS One 6(4), e18371. doi:10.1371/journal.pone.0018371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fenn K, Matthews KR (2007) The cell biology of Trypanosoma brucei differentiation. Curr Opin Microbiol 10:539–546. doi:10.1016/j.mib.2007.09.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fiuza JA, Dey R, Davenport D, Abdeladhim M, Meneses C et al. (2016) Intradermal immunization of Leishmania donovani centrin knock-out parasites in combination with salivary protein LJM19 from sandfly vector induces a durable protective immune response in hamsters. PLoS Negl Trop Dis 10, e0004322. doi:10.1371/journal.pntd.0004322

    Article  PubMed  PubMed Central  Google Scholar 

  • Fragoso CM, Schumann Burkard G, Oberle M, Kunz Renggli C, Hilzinger K et al. (2009) PSSA-2, a membrane-spanning phosphoprotein of Trypanosoma brucei, is required for efficient maturation of infection. PLoS ONE 4, e7074. doi:10.1371/journal.pone.0007074

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Franco JR, Simarro PP, Diarra A, Jannin JG (2014) Epidemiology of human African trypanosomiasis. Clin Epidemiol 6:257–275

    PubMed  PubMed Central  Google Scholar 

  • Freitas-Mesquita AL, Meyer-Fernandes JR (2014) Ecto-nucleotidases and ecto-phosphatases from Leishmania and Trypanosoma parasites. In: Santos ALS, Branquinha MH, d’Avila-Levy CM, Kneipp LF, Sodré CL (eds) Proteins and proteomics of Leishmania and Trypanosoma, vol 74, Subcellular Biochemistry. Springer, Dordrecht, pp 217–252

    Chapter  Google Scholar 

  • Frolet C, Thoma M, Blandin S, Hoffmann JA, Levashina EA (2006) Boosting NF-kappaB-dependent basal immunity of Anopheles gambiae aborts development of Plasmodium berghei. Immunity 25:677–685

    Article  CAS  PubMed  Google Scholar 

  • Garcia ES, Genta FA, de Azambuja P, Schaub GA (2010) Interactions of intestinal compounds of triatomines and Trypanosoma cruzi. Trends Parasitol 26:499–505

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Silva MR, das Neves RF, Cabrera-Cabrera F, Sanguinetti J, Medeiros LC et al. (2013) Extracellular vesicles shed by Trypanosoma cruzi are linked to small RNA pathways, life cycle regulation, and susceptibility to infection of mammalian cells. Parasitol Res 113:285–304

    Article  PubMed  Google Scholar 

  • Garver LS, Dong Y, Dimopoulos G (2009) Caspar controls resistance to Plasmodium falciparum in diverse anopheline species. PLoS Pathog 5, e1000335. doi:10.1371/journal.ppat.1000335

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Garver LS, Bahia AC, Das S, Souza-Neto JA, Shiao J et al. (2012) Anopheles Imd pathway factors and effectors in infection intensity-dependent anti-Plasmodium action. PLoS Pathog 8, e1002737. doi:10.1371/journal.ppat.1002737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geiger A, Ravel S, Mateille T, Janelle J, Patrel D et al. (2007) Vector competence of Glossina palpalis gambiensis for Trypanosoma brucei s.l. and genetic diversity of the symbiont Sodalis glossinidius. Mol Biol Evol 24:102–109

    Article  CAS  PubMed  Google Scholar 

  • Geiger A, Fardeau ML, Njiokou F, Ollivier B (2013) Glossina spp. gut bacterial flora and their putative role fly-hosted trypanosome development. Cell Infect Microbiol 3:34. doi:10.3389/fcimb.2013.00034

    Google Scholar 

  • Geiger A, Hamidou Soumana I, Tchicaya B, Rofidal V, Decourcelle M et al. (2015) Differential expression of midgut proteins in Trypanosoma brucei gambiense-stimulated vs. non-stimulated Glossina palpalis gambiensis flies. Front Microbiol 6:444. doi:10.3389/fmicb.2015.00444

    Article  PubMed  PubMed Central  Google Scholar 

  • Ghosh AK, Ribolla PE, Jacobs-Lorena M (2001) Targeting Plasmodium ligands on mosquito salivary glands and midgut with a phage display peptide library. Proc Natl Acad Sci USA 98:13278–13281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghosh AK, Devenport M, Jethwaney D, Kalume DE, Pandey A et al. (2009) Malaria parasite invasion of the mosquito salivary gland requires interaction between the Plasmodium TRAP and the Anopheles saglin proteins. PLoS Pathog 5, e1000265. doi:10.1371/journal.ppat.1000265

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gibson W, Bailey M (2003) The development of Trypanosoma brucei within the tsetse fly midgut observed using green fluorescent trypanosomes. Kinetoplastid Biol Dis 2:1. doi:10.1186/1475-9292-2-1

    Article  PubMed  PubMed Central  Google Scholar 

  • Gibson W, Peacock L, Ferris V, Williams K, Bailey M (2008) The use of yellow fluorescent hybrids to indicate mating in Trypanosoma brucei. Parasite Vector 1:4. doi:10.1186/1756-3305-1-4

    Article  CAS  Google Scholar 

  • Gibson W, Peacock L, Ferris V, Fischer K, Livingstone J et al. (2015) Genetic recombination between human and animal parasites creates novel strains of human pathogen. PLoS Negl Trop Dis 9, e0003665. doi:10.1371/journal.pntd.0003665

    Article  PubMed  PubMed Central  Google Scholar 

  • Giorgi ME, de Lederkremer RM (2011) Trans-sialidase and mucins of Trypanosoma cruzi: an important interplay for the parasite. Carbohyd Res 346:1389–1393

    Article  CAS  Google Scholar 

  • Goldenberg S, Ávila AR (2011) Aspects of Trypanosoma cruzi stage differentiation. Adv Parasitol 75:285–305

    Article  PubMed  Google Scholar 

  • Gonzalez MS, Nogueira NFS, Mello CB, de Souza W, Schaub GA et al. (1999) Influence of brain and azadirachtin on Trypanosoma cruzi development in the vector, Rhodnius prolixus. Exp Parasitol 92:100–108

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez MS, Hamedi A, Albuquerque-Cunha JM, Nogueira NFS, de Souza W et al. (2006) Antiserum against perimicrovillar membranes and midgut tissue reduces the development of Trypanosoma cruzi in the insect vector, Rhodnius prolixus. Exp Parasitol 114:297–304

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez MS, Souza MS, Garcia ES, Nogueira NFS, Mello CB et al. (2013) Trypanosoma cruzi TcSMUG L-surface mucins promote development and infectivity in the triatomine vector Rhodnius prolixus. PLOS Neglect Trop D 7(11), e2552. doi:10.1371/journal.pntd.0002552

    Article  CAS  Google Scholar 

  • Gossage SM, Rogers ME, Bates PA (2003) Two separate growth phases during the development of Leishmania in sandflies: implications for understanding the life cycle. Int J Parasitol 33:1027–1034

    Article  PubMed  PubMed Central  Google Scholar 

  • Gouagna LC, Mulder B, Noubissi E, Tchuinkam T, Boudin C (1998) The early sporogonic cycle of Plasmodium falciparum in laboratory-infected Anopheles gambiae: an estimation of parasite efficacy. Trop Med Int Health 3:21–28

    Article  CAS  PubMed  Google Scholar 

  • Gumiel M, da Mota FF, de Sousa RV, Sarquis O, Castro DP et al. (2015) Characterization of the microbiota in the guts of Triatoma brasiliensis and Triatoma pseudomaculata infected by Trypanosoma cruzi in natural conditions using culture independent methods. Parasite Vector 8:245. doi:10.1186/s13071-015-0836-z

    Article  Google Scholar 

  • Gunasekera K, Wuthrich D, Braga-Lagache S, Heller M, Ochsenreiter T (2012) Proteome remodeling during development from blood to insect-form Trypanosoma brucei quantified by SILAC and mass spectrometry. BMC Genomics 13:556. doi:10.1186/1471-2164-13-556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta L, Kumar S, Han YS, Pimenta PFP, Barillas-Mury C (2005) Midgut epithelial responses of different mosquito-Plasmodium combinations: the actin cone zipper repair mechanism in Aedes aegypti. Proc Natl Acad Sci USA 102:4010–4015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta L, Molina-Cruz A, Kumar S, Rodrigues J, Dixit R et al. (2009) The STAT pathway mediates late-phase immunity against Plasmodium in the mosquito Anopheles gambiae. Cell Host Microbe 5:498–507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gutiérrez-Cabrera AE, Alejandre-Aguilar R, Hernández-Martínez S, Espinoza-Gutiérrez B (2014) Development and glycoprotein composition of the perimicrovillar membrane in Triatoma (Meccus) pallidipennis (Hemiptera: Reduviidae). Arthropod Struct Dev 43:571–578

    Article  PubMed  Google Scholar 

  • Guzmán H, Tesh RB (2000) Effects of temperature and diet on the growth and longevity of phlebotomine sandflies (Diptera: Psychodidae). Biomédica 20:190–199

    Article  Google Scholar 

  • Haddow JD, Haines LR, Gooding RH, Olafson RW, Pearson TW (2005) Identification of midgut proteins that are differentially expressed in trypanosome-susceptible and normal tsetse flies (Glossina morsitans morsitans). Insect Biochem Mol Biol 35:425–433

    Article  CAS  PubMed  Google Scholar 

  • Haines LR (2013) Examining the tsetse teneral phenomenon and permisssiveness to trypanosome infection. Front Cell Infect Microbiol 3:84. doi:10.3389/fcimb.2013.00084

    Article  PubMed  PubMed Central  Google Scholar 

  • Haines LR, Jackson AM, Lehane MJ, Thomas JM, Yamaguchi AY (2005) Increased expression of unusual EP repeat-containing proteins in the midgut of the tsetse fly (Glossina) after bacterial challenge. Insect Biochem Mol Biol 35:413–423

    Article  CAS  PubMed  Google Scholar 

  • Haines LR, Lehane SM, Pearson TW, Lehane MJ (2010) Tsetse EP protein protects the fly midgut from trypanosome establishment. PLoS Pathog 6, e1000793. doi:10.1371/journal.ppat.1000793

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hamidou Soumana I, Klopp C, Ravel S, Nabihoudine I, Tchicaya B et al. (2015) RNA seq de novo assembly reveals differential gene expression in Glossina palpalis gambiensis infected with Trypanosoma brucei gambiense vs. non-infected and self-cured flies. Front Microbiol 6:1259. doi:10.3389/fmicb.2015.01259

    Article  PubMed  PubMed Central  Google Scholar 

  • Han YS, Thompson J, Kafatos FC, Barillas-Mury C (2000) Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: the time bomb theory of ookinete invasion of mosquitoes. EMBO J 19:6030–6040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hao Z, Kasumba I, Lehane MJ, Gibson WC, Kwon J et al. (2001) Tsetse immune responses and trypanosome transmission: implications for the development of tsetse-based strategies to reduce trypanosomiasis. Proc Natl Acad Sci USA 98:12648–12653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hao Z, Kasumba I, Aksoy S (2003) Proventriculus (cardia) plays a crucial role in immunity in tsetse fly (Diptera: Glossinidiae). Insect Biochem Mol Biol 33:1155–1164

    Article  CAS  PubMed  Google Scholar 

  • Herrera-Ortiz A, Martínez-Barnetche J, Smit N, Rodriguez MH, Lanz-Mendoza H (2011) The effect of nitric oxide and hydrogen peroxide in the activation of the systemic immune response of Anopheles albimanus infected with Plasmodium berghei. Dev Comp Immunol 35:44–50

    Article  CAS  PubMed  Google Scholar 

  • Herwaldt BL (1999) Leishmaniasis. Lancet 354:1191–1199

    Article  CAS  PubMed  Google Scholar 

  • Hillyer JF, Schmidt SL, Christensen BM (2003) Rapid phagocytosis and melanization of bacteria and Plasmodium sporozoites by hemocytes of the mosquito Aedes aegypti. J Parasitol 89:62–69

    Article  PubMed  Google Scholar 

  • Hölscher C, Mossmann H, Hartmann R, Schaub GA (2003) Effects of the isolation methodology on protein profiles of blood trypomastigotes of Trypanosoma cruzi. Parasitology 126:41–51

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann JA, Kafatos FC, Janeway CA, Ezekowitz RA (1999) Phylogenetic perspectives in innate immunity. Science 284:1313–1318

    Article  CAS  PubMed  Google Scholar 

  • Hu C, Aksoy S (2006) Innate immune responses regulate trypanosome parasite infection of the tsetse fly Glossina morsitans morsitans. Mol Microbiol 60:1194–1204

    Article  CAS  PubMed  Google Scholar 

  • Imhof S, Roditi I (2015) Social life of African trypanosomes. Trends Parasitol 31:490–498

    Article  PubMed  Google Scholar 

  • Imhof S, Vu XL, Bütikofer P, Roditi I (2015) A glycosylation mutant of Trypanosoma brucei links social motility defects in vitro to impaired colonization of tsetse flies in vivo. Eukaryot Cell 14:588–592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito J, Ghosh A, Moreira LA, Wimmer EA, Jacobs-Lorena M (2002) Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature 417:452–455

    Article  CAS  PubMed  Google Scholar 

  • Ivens AC, Peacock CS, Worthey EA, Murphy L, Aggarwal G et al. (2005) The genome of the kinetoplastid parasite, Leishmania major. Science 309:436–442

    Article  PubMed  PubMed Central  Google Scholar 

  • Jaramillo-Gutierrez G, Rodrigues J, Ndikuyeze G, Povelones M, Molina-Cruz A et al. (2009) Mosquito immune responses and compatibility between Plasmodium parasites and anopheline mosquitoes. BMC Microbiol 9:154. doi:10.1186/1471-2180-9-154

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jecna L, Dostalova A, Wilson R, Seblova V, Chang K et al. (2013) The role of surface glycoconjugates in Leishmania midgut attachment examined by competitive binding assays and experimental development in sandflies. Parasitology 140:1026–1032

    Article  CAS  PubMed  Google Scholar 

  • Jensen BC, Sivam D, Kifer CT, Myler PJ, Parsons M (2009) Widespread variation in transcript abundance within and across developmental stages of Trypanosoma brucei. BMC Genomics 10:482. doi:10.1186/1471-2164-10-482

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jochim RC, Teixeira CR, Laughinghouse A, Mu J, Oliveira F 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 sandflies. BMC Genomics 9:15. doi:10.1186/1471-2164-9-15

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kabani S, Fenn K, Ross A, Ivens A, Smith TK et al. (2009) Genome-wide expression profiling of in vivo-derived bloodstream parasite stages and dynamic analysis of mRNA alterations during synchronous differentiation in Trypanosoma brucei. BMC Genomics 10:427. doi:10.1186/1471-2164-10-427

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kariithi HM, Ince IA, Boeren S, Abd-Alla AM, Parker AG et al. (2011) The salivary secretome of the tsetse fly Glossina pallidipes (Diptera: Glossinidae) infected by salivary gland hypertrophy virus. PLoS Negl Trop Dis 5, e1371. doi:10.1371/journal.pntd.0001371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Killick-Kendrick R (1999) The biology and control of phlebotomine sandflies. Clin Dermatol 17:279–289

    Article  CAS  PubMed  Google Scholar 

  • Kleffmann T, Schmidt J, Schaub GA (1998) Attachment of Trypanosoma cruzi epimastigotes to hydrophobic substrates and use of this property to separate stages and promote metacyclogenesis. J Eukaryot Microbiol 45:548–555

    Article  CAS  PubMed  Google Scholar 

  • Kollien AH, Schaub GA (2000) The development of Trypanosoma cruzi in Triatominae. Parasitol Today 16:381–387

    Article  CAS  PubMed  Google Scholar 

  • Kollien AH, Schmidt J, Schaub GA (1998) Modes of association of Trypanosoma cruzi with the intestinal tract of the vector Triatoma infestans. Acta Trop 70:127–141

    Article  CAS  PubMed  Google Scholar 

  • Kollien AH, Grospietsch T, Kleffmann T, Zerbst-Boroffka I et al. (2001) Ionic composition of the rectal contents and excreta of the reduviid bug Triatoma infestans. J Insect Physiol 47:739–747

    Article  CAS  PubMed  Google Scholar 

  • Kollien AH, Waniek PJ, Pröls F, Habedank B, Schaub GA (2004) Cloning and characterization of a trypsin-encoding cDNA of the human body louse Pediculus humanus. Insect Mol Biol 13:9–18

    Article  CAS  PubMed  Google Scholar 

  • Krafsur ES (2009) Tsetse flies: genetics, evolution, and role as vectors. Infect Genet Evol 9:124–141

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Christophides GK, Cantera R, Charles B, Han YS et al. (2003) The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae. Proc Natl Acad Sci USA 100:14139–14144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Gupta L, Han YS, Barillas-Mury C (2004) Inducible peroxidases mediate nitration of Anopheles midgut cells undergoing apoptosis in response to Plasmodium invasion. J Biol Chem 279:53475–53482

    Article  CAS  PubMed  Google Scholar 

  • Lainson R, Ward RD, Shaw JJ (1977) Leishmania in phlebotomid sandflies: VI. Importance of hindgut development in distinguishing between parasites of the Leishmania mexicana and L. braziliensis complexes. Proc R Soc Lond, B. Biol Sci 199:309–320

    Article  CAS  Google Scholar 

  • Lavine MD, Strand MR (2002) Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32:1295–1309

    Article  CAS  PubMed  Google Scholar 

  • Lehane MJ, Msangi AR (1991) Lectin and peritrophic membrane development in the gut of Glossina m. morsitans and a discussion of their role in protecting the fly against trypanosome infection. Med Vet Entomol 5:495–501

    Article  CAS  PubMed  Google Scholar 

  • Lehane MJ, Aksoy S, Levashina E (2004) Immune response and parasite transmission in blood-feeding insects. Trends Parasitol 20:433–439

    Article  CAS  PubMed  Google Scholar 

  • Llanes A, Restrepo CM, Del Vecchio G, Anguizola FJ, Lleonart R (2015) The genome of Leishmania panamensis: insights into genomics of the L. (Viannia) subgenus. Sci Rep 5:8550. doi:10.1038/srep08550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luckhart S, Vodovotz Y, Cui L, Rosenberg R (1998) The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proc Natl Acad Sci USA 95:5700–5705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Machin A, Telleria J, Brizard J-P, Demettre E, Séveno M et al. (2014) Trypanosoma cruzi: gene expression surveyed by proteomic analysis reveals interaction between different genotypes in mixed in-vitro cultures. PLOS One 9(4), e95442. doi:10.1371/journal.pone.0095442

    Article  PubMed  PubMed Central  Google Scholar 

  • MacGregor P, Matthews KR (2010) New discoveries in the transmission biology of sleeping sickness parasites: applying the basics. J Mol Med (Berl) 88:865–871

    Article  Google Scholar 

  • MacLeod ET, Darby AC, Maudlin I, Welburn SC (2007) Factors affecting trypanosome maturation in tsetse flies. PLoS ONE 2, e239. doi:10.1371/journal.pone.0000239

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marchini FK, de Godoy LMF, Rampazzo RCP, Pavoni DP, Probst CM et al. (2011) Profiling the Trypanosoma cruzi phosphoproteome. PLOS One 6(9), e25381. doi:10.1371/journal.pone.0025381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marcilla A, Martin-Jaular L, Trelis M, de Menezes-Neto A, Osuna A et al. (2014) Extracellular vesicles in parasitic diseases. J Extracell Vesicles 3:25040. doi:10.3402/jev.v3.25040

    Article  PubMed  Google Scholar 

  • Maroli M, Feliciangeli MD, Bichaud L, Charrel RN, Gradoni L (2013) Phlebotomine sandflies and the spreading of leishmaniases and other diseases of public health concern. Med Vet Entomol 27:123–147

    Article  CAS  PubMed  Google Scholar 

  • Matthews KR (2015) 25 years of African trypanosome research: from description to molecular dissection and new drug discovery. Mol Biochem Parasitol 200:30–40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mattos EC, Tonelli RR, Colli W, Alves MJM (2014) The gp85 surface glycoproteins from Trypanosoma cruzi. In: Santos ALS, Branquinha MH, d’Avila-Levy CM, Kneipp LF, Sodré CL (eds) Proteins and proteomics of Leishmania and Trypanosoma. Subcellular Biochemistry, vol 74. Springer, Dordrecht, pp 151–180

    Google Scholar 

  • McRobert L, Taylor CJ, Deng W, Fivelmann QL, Cummings RM et al. (2008) Gametogenesis in malaria parasites is mediated by the cGMP-dependent protein kinase. PLoS Biol 6(6), e139. doi:10.1371/journal.pbio.0060139

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Meiser CK, Piechura H, Meyer HE, Warscheid B, Schaub GA et al. (2010) A salivary serine protease of the haematophagous reduviid Panstrongylus megistus: sequence characterization, expression pattern and characterization of proteolytic activity. Insect Mol Biol 19:409–421

    Article  CAS  PubMed  Google Scholar 

  • Menna-Barreto RFS, Perales J (2014) The expected outcome of the Trypanosoma cruzi proteomic map: a review of its potential biological applications for drug target discovery. In: Santos ALS, Branquinha MH, d’Avila-Levy CM, Kneipp LF, Sodré CL (eds) Proteins and proteomics of Leishmania and Trypanosoma, vol 74, Subcellular Biochemistry. Springer, Dordrecht, pp 305–322

    Chapter  Google Scholar 

  • Menna-Barreto RFS, Teixeira Belloze K, Perales J, Paes Silva F (2014) Proteomic and bioinformatic analysis of Trypanosoma cruzi chemotherapy and potential drug targets: newpieces for an old puzzle. Curr Drug Targ 15:255–271

    Article  CAS  Google Scholar 

  • Messenger LA, Miles MA (2015) Evidence and importance of genetic exchange among field populations of Trypanosoma cruzi. Acta Trop 151:150–155

    Article  PubMed  PubMed Central  Google Scholar 

  • Mesquita RD, Vionette-Amaral RJ, Lowenberger C, Rivera-Pomar R, Monteiro FA et al. (2015) Genome of Rhodnius prolixus, an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection. Proc Natl Acad Sci USA 112:14936–14941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mikolajczak SA, Silva-Rivera H, Peng X, Tarun AS, Camargo N et al. (2008) Distinct malaria parasite sporozoites reveal transcriptional changes that cause differential tissue infection competence in the mosquito vector and mammalian host. Mol Cell Biol 28:6196–6207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Molina-Cruz A, DeJong RJ, Charles B, Gupta L, Kumar S et al. (2008) Reactive oxygen species modulate Anopheles gambiae immunity against bacteria and Plasmodium. J Biol Chem 283:3217–3223

    Article  CAS  PubMed  Google Scholar 

  • Molina-Cruz A, Garver LS, Alabaster A, Bangiolo L, Haile A et al. (2013) The human malaria parasite Pfs47 gene mediates evasion of the mosquito immune system. Science 340:984–987

    Article  CAS  PubMed  Google Scholar 

  • Moraes CS, Seabra SH, Castro D, Brazil RP, de Souza W et al. (2008) Leishmania (Leishmania) chagasi interactions with Serratia marcescens: ultrastructural studies, lysis and carbohydrate effects. Exp Parasitol 118:561–568

    Article  CAS  PubMed  Google Scholar 

  • Morrison LS, Goundry A, Faria MS, Tetley L, Eschenlauer SC et al. (2012) Ecotin-like serine peptidase inhibitor ISP1 of Leishmania major plays a role in flagellar pocket dynamics and promastigote differentiation. Cell Microbiol 14:1271–1286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müller U, Vogel P, Alber G, Schaub GA (2008) The innate immune system of mammals and insects. In: Egesten A, Schmidt A, Herwald H (eds) Contributions to microbiology, vol 15. Karger, Basel, pp 21–44

    Google Scholar 

  • Myung JM, Marshall P, Sinnis P (2004) The Plasmodium circumsporozoite protein is involved in mosquito salivary gland invasion by sporozoites. Mol Biochem Parasitol 133:53–59

    Article  CAS  PubMed  Google Scholar 

  • Nacer A, Walker K, Hurd H (2008) Localisation of laminin within Plasmodium berghei oocysts and the midgut epithelial cells of Anopheles stephensi. Parasite Vector 1:33. doi:10.1186/1756-3305-1-33

    Article  CAS  Google Scholar 

  • Nakayasu ES, Yashunsky DV, Nohara LL, Torrecilhas AC, Nikolaev AV et al. (2009) GPIomics: global analysis of glycosylphosphatidylinositol-anchored molecules of Trypanosoma cruzi. Mol Syst Biol 5:261. doi:10.1038/msb.2009.13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Neafsey DE, Christophides GK, Collins FH, Emrich SJ, Fontaine MC et al. (2013) The evolution of the Anopheles 16 genomes project. G3 (Bethesda) 3:1191–1194. doi:10.1534/g3.113.006247

    Article  CAS  Google Scholar 

  • Nilsson D, Gunasekera K, Mani J, Osteras M, Farinelli L et al. (2010) Spliced leader trapping reveals widespread alternative splicing patterns in the highly dynamic transcriptome of Trypanosoma brucei. PLoS Pathog 6, e1001037. doi:10.1371/journal.ppat1001037

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nogueira NFS, Gonzalez MS, Gomes JE, de Souza W, Garcia ES et al. (2007) Trypanosoma cruzi: involvement of glycoinositolphospholipids in the attachment to the luminal midgut surface of Rhodnius prolixus. Exp Parasitol 116:120–128

    Article  CAS  PubMed  Google Scholar 

  • Nogueira NP, Saraiva FMS, Sultano PE, Cunha PRBB, Laranja GAT et al. (2015) Proliferation and differentiation of Trypanosoma cruzi inside its vector have a new trigger: redox status. PLOS One 10(2), e0116712. doi:10.1371/journal.pone.0116712

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oberholzer M, Lopez MA, McLelland BT, Hill KL (2010) Social motility in African trypanosomes. PLoS Pathog 6, e1000739. doi:10.1371/journal.ppat.1000739

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oberle M, Balmer O, Brun R, Roditi I (2010) Bottlenecks and the maintenance of minor genotypes during the life cycle of Trypanosoma brucei. PlosS Pathog 6, e1001023. doi:10.1371/journal.ppat.1001023

    Article  CAS  Google Scholar 

  • Paes MC, Cosentino-Gomes D, de Souza CF, Nogueira NP, Meyer-Fernandes JR (2011) The role of heme and reactive oxygen species in proliferation and survival of Trypanosoma cruzi. J Parasitol Res 174614. doi:10.1155/2011/174614

    Google Scholar 

  • Peacock L, Ferris V, Bailey M, Gibson W (2007) Dynamics of infection and competition between two strains of Trypanosoma brucei brucei in the tsetse fly observed using fluorescent markers. Kinetoplastid Biol Dis 6:4. doi:10.1186/1475-9292-6-4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Peacock L, Cook S, Ferris V, Bailey M, Gibson W (2012a) The life cycle of Trypanosoma (Nannomonas) congolense in the tsetse fly. Parasite Vector 5:109. doi:10.1186/1756-3305-5-109

    Article  Google Scholar 

  • Peacock L, Ferris V, Bailey M, Gibson W (2012b) The influence of sex and fly species on the development of trypanosomes in tsetse flies. PLoS Negl Trop Dis 6, e1515. doi:10.1371/journal.pntd.0001515

    Article  PubMed  PubMed Central  Google Scholar 

  • Pennington PM (2015) Genetically modifying the insect gut microbiota to control Chagas disease vectors through systemic RNAi. PLOS Neglect Trop D 9(2), e0003358. doi:10.1371/journal.pntd.0003358

    Article  Google Scholar 

  • Pereira-Chioccola VL, Acosta-Serrano A, Correia de Almeida I, Ferguson MAJ, Souto-Padron T et al. (2000) Mucin-like molecules form a negatively charged coat that protects Trypanosoma cruzi trypomastigotes from killing by human anti-α-galactosyl antibodies. J Cell Sci 113:1299–1307

    CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Peterson TML, Gow AJ, Luckhart S (2007) Nitric oxide metabolites induced in Anopheles stephensi control malaria parasite infection. Free Radic Biol Med 42:132–142

    Article  CAS  PubMed  Google Scholar 

  • Pimenta P, Turco S, McConville M, Lawyer P, Perkins P et al. (1992) Stage-specific adhesion of Leishmania promastigotes to the sandfly midgut. Science 256:1812–1815

    Article  CAS  PubMed  Google Scholar 

  • Pimenta PF, Touray M, Miller L (1994) The journey of malaria sporozoites in the mosquito salivary gland. J Euk Microbiol 41:608–624

    Article  CAS  PubMed  Google Scholar 

  • 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 sandfly midgut. Parasitology 115:359–369

    Article  PubMed  Google Scholar 

  • Pimenta PFP, Orfano AS, Bahia AC, Duarte APM, Ríos-Velásquez CM et al. (2015) An overview of malaria transmission from the perspective of Amazon Anopheles vectors. Mem Inst Oswaldo Cruz 110:23–47

    Article  PubMed  PubMed Central  Google Scholar 

  • Pinto SB, Lombardo F, Koutsos AC, Waterhouse RM, McKay K et al. (2009) Discovery of Plasmodium modulators by genome-wide analysis of circulating hemocytes in Anopheles gambiae. Proc Natl Acad Sci USA 106:21270–21275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Povelones M, Waterhouse RM, Kafatos FC, Christophides GK (2009) Leucine-rich repeat protein complex activates mosquito complement in defense against Plasmodium parasites. Science 324:258–261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Povelones M, Bhagavatula L, Yassine H, Tan LA, Upton LM et al. (2013) The CLIP-domain serine protease homolog SPCLIP1 regulates complement recruitment to microbial surfaces in the malaria mosquito Anopheles gambiae. PLoS Pathog 9, e1003623. doi:10.1371/journal.ppat.1003623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Queiroz RM, Charneau S, Motta FN, Santana JM, Roepstorff P et al. (2013) Comprehensive proteomic analysis of Trypanosoma cruzi epimastigote cell surface proteins by two complementary methods. J Proteome Res 12:3255–3263

    Article  CAS  PubMed  Google Scholar 

  • Ramalho-Ortigão M, Jochim RC, Anderson JM, Lawyer PG, Pham V et al. (2007) Exploring the midgut transcriptome of Phlebotomus papatasi: comparative analysis of expression profiles of sugar-fed, blood-fed and Leishmania-major-infected sandflies. BMC Genomics 8:300. doi:10.1186/1471-2164-8-300

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ramasamy R (2014) Zoonotic malaria – global overview and research and policy needs. Front Public Health 2:123. doi:10.3389/fpubh.2014.00123

    Article  PubMed  PubMed Central  Google Scholar 

  • Ramirez JL, Garver LS, Brayner FA, Alves LC, Rodrigues J et al. (2014) The role of hemocytes in Anopheles gambiae antiplasmodial immunity. J Innate Immun 6:119–128

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro JMC, Francischetti IMB (2003) Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annu Rev Entomol 48:73–88

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro JMC, Genta FA, Sorgine MHF, Logullo R, Mesquita RD et al. (2014) An insight into the transcriptome of the digestive tract of the bloodsucking bug, Rhodnius prolixus. PLoS Negl Trop Dis 8(1):e2594. doi:10.1371/journal.pntd.0002594

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rico E, Rojas F, Mony BM, Szoor B, MacGregor P, Matthews KR (2013) Bloodstream form pre-adaptation to the tsetse fly in Trypanosoma brucei. Front Cell Infect Microbiol 14:78. doi:10.3389/fcimb.2013.00078

    Google Scholar 

  • Roditi I, Lehane MJ (2008) Interactions between trypanosomes and tsetse flies. Curr Opin Microbiol 11:345–351

    Article  PubMed  Google Scholar 

  • Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C (2010) Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 329:1353–1355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodrigues JCF, Godinho JLP, de Souza W (2014) Biology of human pathogenic trypanosomatids: epidemiology, lifecycle and ultrastructure. In: Santos ALS, Branquinha MH, d’Avila-Levy CM, Kneipp LF, Sodré CL (eds) Proteins and proteomics of Leishmania and Trypanosoma, Subcellular biochemistry, vol 74. Springer, Dordrecht, pp 1–42. doi:10.1007/978-94-007-7305-9_1

    Google Scholar 

  • Rogers MB, Downing T, Smith BA, Imamura H, Sanders M et al. (2014) Genomic confirmation of hybridisation and recent inbreeding in a vector-isolated Leishmania population. PLoS Genet 10(1), e1004092. doi:10.1371/journal.pgen.1004092

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rose C, Belmonte R, Armstrong SD, Molyneux G, Haines LR et al. (2014) An investigation into the protein composition of the teneral Glossina morsitans morsitans peritrophic matrix. PLoS Negl Trop Dis 8:e2691. doi:10.1371/journal.pntd.0002691

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rotureau B, Van Den Abbeele J (2013) Through the dark continent: African trypanosome development in the tsetse fly. Front Cell Infect Microbiol 3:53. doi:10.3389/fcimb.2013.00053

    Article  PubMed  PubMed Central  Google Scholar 

  • Rotureau B, Subota I, Buisson J, Bastin P (2012) A new asymmetric division contributes to the continuous production of infective trypanosomes in the tsetse fly. Development 139:1842–1850

    Article  CAS  PubMed  Google Scholar 

  • Rotureau B, Ooi C-P, Huet D, Perrot S, Bastin P (2013) Forward motility is essential for trypanosome infection in the tsetse fly. Cell Microbiol 16:425–433

    Article  PubMed  CAS  Google Scholar 

  • Sacks DL (2001) Leishmania-sandfly interactions controlling species-specific vector competence. Cell Microbiol 3:189–196

    Article  CAS  PubMed  Google Scholar 

  • Sacks DL, Kamhawi S (2001) Molecular aspects of parasite-vector and vector-host interactions in leishmaniasis. Annu Rev Microbiol 55:453–483

    Article  CAS  PubMed  Google Scholar 

  • Sant'Anna MR, Diaz-Albiter H, Mubaraki M, Dillon RJ, Bates PA (2009) Inhibition of trypsin expression in Lutzomyia longipalpis using RNAi enhances the survival of Leishmania. Parasit Vectors 2:62. doi:10.1186/1756-3305-2-62

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sassera D, Epis S, Pajoro M, Bandi C (2013) Microbial symbiosis and the control of vector-borne pathogens in tsetse flies, human lice and triatomine bugs. Pathog Global Health 107:285–292. doi:10.1179/2047773213Y.0000000109

    Article  Google Scholar 

  • Savage AF, Cerqueira GC, Regmi S, Wu Y, El Sayed NM, Aksoy S (2012) Transcript expression analysis of putative Trypanosoma brucei GPI-anchored surface proteins during development in the tsetse and mammalian host. PLoS Negl Trop Dis 6:ee1708. doi:10.1371/journal.pntd.0001708

    Article  CAS  Google Scholar 

  • Schaub GA (1989a) Trypanosoma cruzi: quantitative studies of development of two strains in small intestine and rectum of the vector Triatoma infestans. Exp Parasitol 68:260–273

    Article  CAS  PubMed  Google Scholar 

  • Schaub GA (1989b) Does Trypanosoma cruzi stress its vector? Parasitol Today 5:185–188

    Article  CAS  PubMed  Google Scholar 

  • Schaub GA (in press a) Mosquitoes. In: Mehlhorn H (ed) Encyclopedia of parasitology, 4th edn. Springer, Heidelberg

    Google Scholar 

  • Schaub GA (in press b) Sandflies. In: Mehlhorn H (ed) Encyclopedia of parasitology, 4th edn. Springer, Heidelberg

    Google Scholar 

  • Schaub GA (in press c) Tsetse flies. In: Mehlhorn H (ed) Encyclopedia of parasitology, 4th edn. Springer, Heidelberg

    Google Scholar 

  • Schaub GA, Lösch P (1988) Trypanosoma cruzi: origin of metacyclic trypomastigotes in the urine of the vector Triatoma infestans. Exp Parasitol 65:174–186

    Article  CAS  PubMed  Google Scholar 

  • Schaub GA, Hölscher C, Mossmann H (2001) Development of high numbers of blood trypomastigotes of Trypanosoma cruzi in nude rats. Parasitol Res 87:245–247

    Article  CAS  PubMed  Google Scholar 

  • Schaub GA, Meiser CK, Balczun C (2011) Interactions of Trypanosoma cruzi and triatomines. In: Mehlhorn H (ed) Parasitology research monographs, vol 2, Progress in parasitology. Springer, Berlin, pp 155–178

    Google Scholar 

  • Schmidt J, Kleffmann T, Schaub GA (1998) Hydrophobic attachment of Trypanosoma cruzi to a superficial layer of the rectal cuticle in the bug Triatoma infestans. Parasitol Res 84:527–536

    Article  CAS  PubMed  Google Scholar 

  • Secundino N, Kimblin N, Peters NC, Lawyer P, Capul AA et al. (2010) Proteophosphoglycan confers resistance of Leishmania major to midgut digestive enzymes induced by blood feeding in vector sandflies. Cell Microbiol 12:906–918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma R, Peacock L, Gluenz E, Gull K, Gibson W et al. (2008) Asymmetric cell division as a route to reduction in cell length and change in cell morphology in trypanosomes. Protist 159:137–151

    Article  PubMed  Google Scholar 

  • Sharma R, Gluenz E, Peacock L, Gibson W, Gull K et al. (2009) The heart of darkness: growth and form of Trypanosoma brucei in the tsetse fly. Trends Parasitol 25:517–524

    Article  PubMed  PubMed Central  Google Scholar 

  • Sidén-Kiamos I, Vlachou D, Margos G, Beetsma A, Waters AP et al. (2000) Distinct roles for pbs21 and pbs25 in the in vitro ookinete to oocyst transformation of Plasmodium berghei. J Cell Sci 113:3419–3426

    PubMed  Google Scholar 

  • Sidjanski SP, Vanderberg JP, Sinnis P (1997) Anopheles stephensi salivary glands bear receptors for region I of the circumsporozoite protein of Plasmodium falciparum. Mol Biochem Parasitol 90:33–41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simonetti AB (1996) The biology of malarial parasite in the mosquito – a review. Mem Inst Oswaldo Cruz 91:519–541

    Article  CAS  PubMed  Google Scholar 

  • Simpson GB, Stevens JR, Lukes J (2006) The evolution and diversity of kinetoplastid flagellates. Trends Parasitol 22:168–174

    Article  CAS  PubMed  Google Scholar 

  • Sinden RE (1999) Plasmodium differentiation in the mosquito. Parassitologia 41:139–148

    CAS  PubMed  Google Scholar 

  • Sinka ME, Bangs MJ, Manguin S, Rubio-Palis Y, Chareonviriyaphap T et al. (2012) A global map of dominant malaria vectors. Parasit Vectors 5:69. doi:10.1186/1756-3305-5-69

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith RC, Jacobs-Lorena M (2010) Plasmodium-mosquito interactions: a tale of roadblocks and detours. Adv Insect Phys 39:119–149

    Article  Google Scholar 

  • Smith RC, Vega-Rodríguez J, Jacobs-Lorena M (2014) The Plasmodium bottleneck: malaria parasite losses in the mosquito vector. Mem Inst Oswaldo Cruz 109:644–661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soares TS, Buarque DS, Queiroz BR, Gomez CM, Braz GRC et al. (2015) A Kazal-type inhibitor is modulated by Trypanosoma cruzi to control microbiota inside the anterior midgut of Rhodnius prolixus. Biochimie 112:41–48

    Article  CAS  PubMed  Google Scholar 

  • Stadler A, Meiser CK, Schaub GA (2011) “Living syringes”: use of haematophagous bugs as blood samplers from small and wild animals. In: Mehlhorn H (ed) Parasitology research monographs, vol 1, Nature helps…How plants and other organisms contribute to solve health problems. Springer, Berlin, pp 243–271

    Google Scholar 

  • Stierhof YD, Bates PA, Jacobson RL, Rogers ME, Schlein Y et al. (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

    Article  CAS  PubMed  Google Scholar 

  • Subota I, Rotureau B, Blisnick T, Ngwabyt S, Durand-Dubief M et al. (2011) ALBA proteins are stage regulated during trypanosome development in the tsetse fly and participate in differentiation. Mol Biol Cell 22:4205–4219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sultan AA, Thathy V, Frevert U, Robson KJ, Crisanti A et al. (1997) TRAP is necessary for gliding motility and infectivity of Plasmodium sporozoites. Cell 90:511–522

    Article  CAS  PubMed  Google Scholar 

  • Synder AK, Rio RVM (2013) Interwoven biology of the tsetse symbiont. J Bacteriol 195:4322–4330

    Article  CAS  Google Scholar 

  • Szoor B, Wilson J, McElhinney H, Tabernero L, Matthews KR (2006) Protein tyrosine phosphatase TbPTP1, a molecular switch controlling life cycle differentiation in trypanosomes. J Cell Biol 175:293–303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szoor B, Dyer N, Ruberto I, Acosta-Serrano A, Matthews KR (2013) Independent pathways can transduce the life-cycle differentiation signal in Trypanosoma brucei. PloS Pathog 9:e1003689. doi:10.101371/journal.ppat.1003689

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Telleria EL, de Araújo APO, Secundino NF, d’Avila-Levy CM, Traub-Csekö YM (2010) Trypsin-like serine proteases in Lutzomyia longipalpis-expression, activity and possible modulation by Leishmania infantum chagasi. PLoS ONE 5, e10697. doi:10.1371/journal.pone.0010697

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Telleria EL, Sant'Anna MRV, Ortigão-Farias JR, Pitaluga AN, Dillon VM et al. (2012) Caspar-like gene depletion reduces Leishmania infection in sandfly host Lutzomyia longipalpis. J Biol Chem 287:12985–12993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Telleria EL, Sant'Anna MRV, Alkurbi MO, Pitaluga AN, Dillon RJ et al. (2013) Bacterial feeding, Leishmania infection and distinct infection routes induce differential defensin expression in Lutzomyia longipalpis. Parasit Vectors 6:12. doi:10.1186/1756-3305-6-12

    Article  PubMed  PubMed Central  Google Scholar 

  • Telleria EL, Benoit JB, Zhao X, Savage AF, Regmi S et al. (2014) Insights into the trypanosome-host interactions revealed through transcriptomic analysis of parasitized tsetse fly salivary glands. PLoS Negl Trop Dis 8, e2649. doi:10.1371/journal.pntd.0002649

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tomás AM, Miles MA, Kelly JM (1997) Overexpression of cruzipain, the major cysteine proteinase of Trypanosoma cruzi, is associated with enhanced metacyclogenesis. Eur J Biochem 244:596–603

    Article  PubMed  Google Scholar 

  • Tsai YL, Hayward RE, Langer RC, Fidock DA, Vinetz JM (2001) Disruption of Plasmodium falciparum chitinase markedly impairs parasite invasion of mosquito midgut. Infect Immun 69:4048–4054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uehara LA, Moreira OC, Oliveira AC, Azambuja P, Lima APCA et al. (2012) Cruzipain promotes Trypanosoma cruzi adhesion to Rhodnius prolixus midgut. PLOS Neglect Trop D 6(12), e1958. doi:10.1371/journal.pntd.0001958

    Article  CAS  Google Scholar 

  • Urbaniak MD, Guther ML, Ferguson MA (2012) Comparative SILAC proteomic analysis of Trypanosoma brucei bloodstream and procyclic lifecycle stages. PLoS ONE 7, e36619. doi:10.1371/journal.pone.0036619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Urwyler S, Vassella E, Van Den Abbeele J, Renggli CK, Blundell P, Barry JD, Roditi I (2005) Expression of procyclin mRNAs during cyclical transmission of Trypanosoma brucei. PloS Pathog 1, e22. doi:10.1371/journal.ppat.0010022

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vallejo GA, Guhl F, Schaub GA (2009) Triatominae-Trypanosoma cruzi/T. rangeli: vector-parasite interactions. Acta Trop 110:137–147

    Article  CAS  PubMed  Google Scholar 

  • Van den Abbeele J, Claes Y, van Bockstaele D, Le Ray D, Coosemans M (1999) Trypanosoma brucei spp. development in the tsetse fly: characterization of the post-mesocyclic stages in the foregut and proboscis. Parasitology 118:469–478

    Article  Google Scholar 

  • Van den Abbeele J, Caljon G, De RK, De Baetselier D, Coosemans M (2010) Trypanosoma brucei modifies the tsetse salivary composition, altering the fly feeding behaviour that favors parasite transmission. PLoS Pathog 6, e1000926. doi:10.1371/journal.ppat.1000926

    Article  CAS  Google Scholar 

  • Vassella E, Acosta-Serrano A, Studer E, Lee SH, Englund PT (2001) Multiple procyclin isoforms are expressed differentially during the development of insect forms of Trypanosoma brucei. J Mol Biol 312:597–607

    Article  CAS  PubMed  Google Scholar 

  • Vassella E, Oberle M, Urwyler S, Kunz Renggli C, Studer E, Hemphill A et al. (2009) Major surface glycoproteins of insect forms of Trypanosoma brucei are not essential for cyclical transmission by tsetse. PLoS ONE 4, e4493. doi:10.1371/journal.pone.0004493

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vega-Rodríguez J, Ghosh AK, Kanzok SM, Dinglasan RR, Wang S et al. (2014) Multiple pathways for Plasmodium ookinete invasion of the mosquito midgut. Proc Natl Acad Sci USA 111:E492–E500

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vickerman K (1985) Developmental cycles and biology of pathogenic trypanosomes. Br Med Bull 41:105–114

    CAS  PubMed  Google Scholar 

  • Vieira CS, Waniek PJ, Mattos DP, Castro DP, Mello CB et al. (2014) Humoral responses in Rhodnius prolixus: bacterial feeding induces differential patterns of antibacterial activity and enhances mRNA levels of antimicrobial peptides in the midgut. Parasite Vector 7:232. doi:10.1186/1756-3305-7-232

    Article  CAS  Google Scholar 

  • Vieira CS, Mattos DP, Waniek PJ, Santangelo JM, Figueiredo MB et al. (2015) Rhodnius prolixus interaction with Trypanosoma rangeli: modulation of the immune system and microbiota population. Parasite Vector 8:135. doi:10.1186/s13071-015-0736-2

    Article  Google Scholar 

  • Vinetz JM, Valenzuela JG, Specht CA, Aravind L, Langer RC et al. (2000) Chitinases of the avian malaria parasite Plasmodium gallinaceum, a class of enzymes necessary for parasite invasion of the mosquito midgut. J Biol Chem 275:10331–10341

    Article  CAS  PubMed  Google Scholar 

  • Vlachou D, Lycett G, Sidén-Kiamos I, Blass C, Sinden RE et al. (2001) Anopheles gambiae laminin interacts with the P25 surface protein of Plasmodium berghei ookinetes. Mol Biochem Parasitol 112:229–237

    Article  CAS  PubMed  Google Scholar 

  • Walshe DP, Lehane MJ, Haines LR (2011) Post eclosion age predicts the prevalence of midgut trypanosome infections in Glossina. PLoS ONE 6, e26984. doi:10.1371/journal.pone.0026984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Aksoy S (2012) PGRP-LB is a maternally transmitted immune milk protein that influences symbiosis and parasitism in tsetse’s offspring. Proc Natl Acad Sci USA 109:10552–10557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Wu Y, Yang G, Aksoy S (2009) Interactions between mutualist Wigglesworthia and tsetse peptidoglycan recognition protein (PGRP-LB) influence trypanosome transmission. Proc Natl Acad Sci USA 106:12133–12138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Weiss BL, Aksoy S (2013a) Tsetse fly microbiota: form and function. Front Cell Infect Microbiol 3:69. doi:10.3389/fcimb.2013.00069

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Zhang Y, Zhao YO, Li MWM, Zhang L et al. (2013b) Anopheles gambiae circumsporozoite protein-binding protein facilitates Plasmodium infection of mosquito salivary glands. J Infect Dis 208:1161–1169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waniek PJ, Jansen AM, Araújo CA (2011) Trypanosoma cruzi infection modulates the expression of Triatoma brasiliensis def1 in the midgut. Vector Borne Zoonotic Dis 11:845–847

    Article  PubMed  Google Scholar 

  • Warburg A, Touray M, Krettli AU, Miller LH (1992) Plasmodium gallinaceum: antibodies to circumsporozoite protein prevent sporozoites from invading the salivary glands of Aedes aegypti. Exp Parasitol 75:303–307

    Article  CAS  PubMed  Google Scholar 

  • Waterhouse RM, Kriventseva EV, Meister S, Xi Z, Alvarez KS et al. (2007) Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 316:1738–1743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weiss BL, Wang JW, Aksoy S (2011) Tsetse immune system maturation requires the presence of obligate symbionts in larvae. PLoS Biol 9, e1000619. doi:10.1371/journal.pbio.1000619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weiss BL, Maltz M, Aksoy S (2012) Obligate symbionts activate immune system development in the tsetse fly. J Immunol 188:3395–3403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weiss BL, Wang J, Maltz MA, Wu Y, Aksoy S (2013) Trypanosome infection establishment in the tsetse fly gut is influenced by microbiome-regulated host immune barriers. PLoS Pathog 9, e1003318. doi:10.1371/journal.ppat.1003318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weiss BL, Savage AF, Griffith BC, Wu Y, Aksoy S (2014) The peritrophic matrix mediates differential infection outcomes in the tsetse fly gut following challenge with commensal, pathogenic and parasitic microbes. J Immunol 193:773–782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Welburn SC, Arnold K, Maudlin I, Gooday GW (1993) Rickettsia-like organisms and chitinase production in relation to transmission of trypanosomes by tsetse flies. Parasitology 107:141–145

    Article  PubMed  Google Scholar 

  • Welburn SC, Maudlin I (1999) Tsetse-trypanosome interactions: rites of passage. Parasitol Today 15:399–403

    Article  CAS  PubMed  Google Scholar 

  • Wenyon CM (1926) Protozoology: a manual for medical men, veterinarians and zoologists, vol 1. Wood, New York

    Book  Google Scholar 

  • WHO (2008) Chagas disease: control and elimination. Report of the Secretariat. EB124/17:1–4

    Google Scholar 

  • WHO (2010) Control of the leishmaniases: report of a meeting of the WHO Expert Committee on the Control of Leishmaniases, Geneva, 22–26 March 2010. WHO technical report series, no 949. World Health Organization, Geneva

    Google Scholar 

  • WHO (2014) World Malaria Report 2014. World Health Organization, Geneva

    Google Scholar 

  • WHO (2015a) Fact Sheet No 259: Trypanosomiasis, human African (sleeping sickness)

    Google Scholar 

  • WHO (2015b) Fact sheet No. 340: Chagas disease (American trypanosomiasis)

    Google Scholar 

  • Wirth CC, Bennink S, Scheuermayer M, Fischer R, Pradel G (2015) Perforin-like protein PPLP4 is crucial for mosquito midgut infection by Plasmodium falciparum. Mol Biochem Parasitol 201:90–99

    Article  CAS  PubMed  Google Scholar 

  • Yassine H, Kamareddine L, Chamat S, Christophides GK, Osta MA (2014) A serine protease homolog negatively regulates TEP1 consumption in systemic infections of the malaria vector Anopheles gambiae. J Innate Immun 6:806–818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Q, Hu H, Li Z (2014) New insights into the molecular mechanisms of mitosis and cytokinesis in trypanosomes. Int Rev Cell Mol Biol 308:127–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zieler H, Nawrocki JP, Shahabuddin M (1999) Plasmodium gallinaceum ookinetes adhere specifically to the midgut epithelium of Aedes aegypti by interaction with a carbohydrate ligand. J Exp Biol 202:485–495

    CAS  PubMed  Google Scholar 

  • Zingales B, Miles MA, Campbell DA, Tibayrenc M, Macedo AM et al. (2012) The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological relevance and research applications. Infect Genet Evol 12:240–253

    Article  PubMed  Google Scholar 

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Acknowledgments

We are very grateful to many colleagues who provided us with most recently published results and especially to Keith Gull for his indication to Wenyon’s textbook.

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Schaub, G.A., Vogel, P., Balczun, C. (2016). Parasite-Vector Interactions. In: Walochnik, J., Duchêne, M. (eds) Molecular Parasitology. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1416-2_14

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