4,554
Views
164
CrossRef citations to date
0
Altmetric
Review Articles

Extracellular vesicles in parasitic diseases

, , , , , , , & show all
Article: 25040 | Received 26 May 2014, Accepted 21 Oct 2014, Published online: 22 Dec 2014

References

  • Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013; 200: 373–83.
  • Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol. 2009; 9: 581–93.
  • Simons M, Raposo G. Exosomes – vesicular carriers for intercellular communication. Curr Opin Cell Biol. 2009; 21: 575–81.
  • Bobrie A, Colombo M, Raposo G, Thery C. Exosome secretion: molecular mechanisms and roles in immune responses. Traffic. 2011; 12: 1659–68.
  • Hugel B, Martinez MC, Kunzelmann C, Freyssinet JM. Membrane microparticles: two sides of the coin. Physiology. 2005; 20: 22–7.
  • Laulagnier K, Motta C, Hamdi S, Roy S, Fauvelle F, Pageaux JF et al. Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem J. 2004; 380: 161–71.
  • Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008; 319: 1244–7.
  • Wubbolts R, Leckie RS, Veenhuizen PT, Schwarzmann G, Mobius W, Hoernschemeyer J et al. Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J Biol Chem. 2003; 278: 10963–72.
  • Thery C, Boussac M, Veron P, Ricciardi-Castagnoli P, Raposo G, Garin J et al. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol. 2001; 166: 7309–18.
  • Choi DS, Kim DK, Kim YK, Gho YS. Proteomics, transcriptomics and lipidomics of exosomes and ectosomes. Proteomics. 2013; 13: 1554–71.
  • Kastelowitz N, Yin H. Exosomes and microvesicles: identification and targeting by particle size and lipid chemical probes. Chembiochem. 2014; 15: 923–8.
  • Cox FE. History of human parasitology. Clin Microbiol Rev. 2002; 15: 595–612.
  • Schorey JS, Bhatnagar S. Exosome function: from tumor immunology to pathogen biology. Traffic. 2008; 9: 871–81.
  • Barteneva NS, Maltsev N, Vorobjev IA. Microvesicles and intercellular communication in the context of parasitism. Front Cell Infect Microbiol. 2013; 3: 49.
  • Twu O, Johnson PJ. Parasite extracellular vesicles: mediators of intercellular communication. PLoS Pathog. 2014; 10: e1004289.
  • Reid AJ. Large, rapidly evolving gene families are at the forefront of host-parasite interactions in Apicomplexa. Parasitology. 2014; 1–14.
  • Tulane. Apicomplexa. 2010. [cited 2012 Dec 20]. Available from: http://www.tulane.edu/~wiser/protozoology/notes/api.html.
  • Singh B, Kim Sung L, Matusop A, Radhakrishnan A, Shamsul SS, Cox-Singh J et al. A large focus of naturally acquired Plasmodium knowlesi infections in human beings. Lancet. 2004; 363: 1017–24.
  • WHO. Malaria Fact Sheet No 94. 2014; Geneva. Available from: http://www.who.int/mediacentre/factsheets/fs094/en/.
  • Garnham PC. Malaria in mammals excluding man. Adv Parasitol. 1967; 5: 139–204. [PubMed Abstract].
  • Escalante AA, Ayala FJ. Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. Proc Natl Acad Sci USA. 1994; 91: 11373–7.
  • Cox FE. History of the discovery of the malaria parasites and their vectors. Parasites Vectors. 2010; 3: 5.
  • Campos FM, Franklin BS, Teixeira-Carvalho A, Filho AL, de Paula SC, Fontes CJ et al. Augmented plasma microparticles during acute Plasmodium vivax infection. Malar J. 2010; 9: 327.
  • Nantakomol D, Dondorp AM, Krudsood S, Udomsangpetch R, Pattanapanyasat K, Combes V et al. Circulating red cell-derived microparticles in human malaria. J Infect Dis. 2011; 203: 700–6.
  • Combes V, Taylor TE, Juhan-Vague I, Mege JL, Mwenechanya J, Tembo M et al. Circulating endothelial microparticles in Malawian children with severe falciparum malaria complicated with coma. JAMA. 2004; 291: 2542–4. [PubMed Abstract].
  • Pankoui Mfonkeu JB, Gouado I, Fotso Kuate H, Zambou O, Amvam Zollo PH, Grau GE et al. Elevated cell-specific microparticles are a biological marker for cerebral dysfunctions in human severe malaria. PLoS One. 2010; 5: e13415.
  • Coltel N, Combes V, Wassmer SC, Chimini G, Grau GE. Cell vesiculation and immunopathology: implications in cerebral malaria. Microbes Infect. 2006; 8: 2305–16.
  • Couper KN, Barnes T, Hafalla JC, Combes V, Ryffel B, Secher T et al. Parasite-derived plasma microparticles contribute significantly to malaria infection-induced inflammation through potent macrophage stimulation. PLoS Pathog. 2010; 6: e1000744.
  • Combes V, Coltel N, Alibert M, van Eck M, Raymond C, Juhan-Vague I et al. ABCA1 gene deletion protects against cerebral malaria: potential pathogenic role of microparticles in neuropathology. Am J Pathol. 2005; 166: 295–302.
  • Martin-Jaular L, Nakayasu ES, Ferrer M, Almeida IC, Del Portillo HA. Exosomes from Plasmodium yoelii-infected reticulocytes protect mice from lethal infections. PLoS One. 2011; 6: e26588.
  • Regev-Rudzki N, Wilson DW, Carvalho TG, Sisquella X, Coleman BM, Rug M et al. Cell-cell communication between malaria-infected red blood cells via exosome-like vesicles. Cell. 2013; 153: 1120–33.
  • Mantel PY, Hoang AN, Goldowitz I, Potashnikova D, Hamza B, Vorobjev I et al. Malaria-infected erythrocyte-derived microvesicles mediate cellular communication within the parasite population and with the host immune system. Cell Host Microbe. 2013; 13: 521–34.
  • Alano P, Carter R. Sexual differentiation in malaria parasites. Ann Rev Microbiol. 1990; 44: 429–49.
  • Dyer M, Day KP. Commitment to gametocytogenesis in Plasmodium falciparum. Parasitol Today. 2000; 16: 102–7.
  • Dyer M, Day KP. Regulation of the rate of asexual growth and commitment to sexual development by diffusible factors from in vitro cultures of Plasmodium falciparum. Am J Trop Med Hyg. 2003; 68: 403–9. [PubMed Abstract].
  • Del Portillo HA, Chitnis CE. Talking to each other to initiate sexual differentiation. Cell. 2013; 153: 945–7.
  • El-Assaad F, Wheway J, Hunt NH, Grau GE, Combes V. Production, fate and pathogenicity of plasma microparticles in murine cerebral malaria. PLoS Pathog. 2014; 10: e1003839.
  • CDC. Parasites – Toxoplasmosis (Toxoplasma infection). 2013. [cited 2013 Jan 10]. Available from: http://www.cdc.gov/parasites/toxoplasmosis/epi.html.
  • Aline F, Bout D, Amigorena S, Roingeard P, Dimier-Poisson I. Toxoplasma gondii antigen-pulsed-dendritic cell-derived exosomes induce a protective immune response against T. gondii infection. Infect Immun. 2004; 72: 4127–37.
  • Chaput N, Thery C. Exosomes: immune properties and potential clinical implementations. Semin Immunopathol. 2011; 33: 419–40.
  • Bhatnagar S, Shinagawa K, Castellino FJ, Schorey JS. Exosomes released from macrophages infected with intracellular pathogens stimulate a proinflammatory response in vitro and in vivo. Blood. 2007; 110: 3234–44.
  • Beauvillain C, Ruiz S, Guiton R, Bout D, Dimier-Poisson I. A vaccine based on exosomes secreted by a dendritic cell line confers protection against T. gondii infection in syngeneic and allogeneic mice. Microbes Infect. 2007; 9: 1614–22.
  • Pope SM, Lasser C. Toxoplasma gondii infection of fibroblasts causes the production of exosome-like vesicles containing a unique array of mRNA and miRNA transcripts compared to serum starvation. J Extracell Vesicles. 2013; 2 22484, doi: http://dx.doi.org/10.3402/jev.v2i0.22484.
  • Hu G, Gong AY, Roth AL, Huang BQ, Ward HD, Zhu G et al. Release of luminal exosomes contributes to TLR4-mediated epithelial antimicrobial defense. PLoS Pathog. 2013; 9: e1003261.
  • Tulane. Kinetoplastids. 1999; New Orleans: Tulane University. [cited 2013 Oct 16]. Available from: http://www.tulane.edu/~wiser/protozoology/notes/kinet.html.
  • Barrett MP, Burchmore RJ, Stich A, Lazzari JO, Frasch AC, Cazzulo JJ et al. The trypanosomiases. Lancet. 2003; 362: 1469–80.
  • Rodrigues JC, Godinho JL, de Souza W. Biology of human pathogenic trypanosomatids: epidemiology, lifecycle and ultrastructure. Subcell Biochem. 2014; 74: 1–42. [PubMed Abstract].
  • Geiger A, Hirtz C, Becue T, Bellard E, Centeno D, Gargani D et al. Exocytosis and protein secretion in Trypanosoma. BMC Microbiol. 2010; 10: 20.
  • Ouaissi A, Aguirre T, Plumas-Marty B, Piras M, Schoneck R, Gras-Masse H et al. Cloning and sequencing of a 24-kDa Trypanosoma cruzi specific antigen released in association with membrane vesicles and defined by a monoclonal antibody. Biol Cell. 1992; 75: 11–17.
  • da Silveira JF, Abrahamsohn PA, Colli W. Plasma membrane vesicles isolated from epimastigote forms of Trypanosoma cruzi. Biochim Biophys Acta. 1979; 550: 222–32.
  • Gonçalves MF, Umezawa ES, Katzin AM, de Souza W, Alves MJ, Zingales B et al. Trypanosoma cruzi: shedding of surface antigens as membrane vesicles. Exp Parasitol. 1991; 72: 43–53.
  • Trocoli Torrecilhas AC, Tonelli RR, Pavanelli WR, da Silva JS, Schumacher RI, de Souza W et al. Trypanosoma cruzi: parasite shed vesicles increase heart parasitism and generate an intense inflammatory response. Microbes Infect. 2009; 11: 29–39.
  • Brun R, Blum J. Human African trypanosomiasis. Infect Dis Clin North Am. 2012; 26: 261–73.
  • Brun R, Blum J, Chappuis F, Burri C. Human African trypanosomiasis. Lancet. 2010; 375: 148–59.
  • Kennedy PG. Clinical features, diagnosis, and treatment of human African trypanosomiasis (sleeping sickness). Lancet Neurol. 2013; 12: 186–94.
  • Atyame Nten CM, Sommerer N, Rofidal V, Hirtz C, Rossignol M, Cuny G et al. Excreted/secreted proteins from trypanosome procyclic strains. J Biomed Biotechnol. 2010; 2010: 212817.
  • Alarcon de Noya B, Diaz-Bello Z, Colmenares C, Ruiz-Guevara R, Mauriello L, Zavala-Jaspe R et al. Large urban outbreak of orally acquired acute Chagas disease at a school in Caracas, Venezuela. J Infect Dis. 2010; 201: 1308–15.
  • Yoshida N, Tyler KM, Llewellyn MS. Invasion mechanisms among emerging food-borne protozoan parasites. Trends Parasitol. 2011; 27: 459–66.
  • Tarleton RL, Reithinger R, Urbina JA, Kitron U, Gurtler RE. The challenges of Chagas disease – grim outlook or glimmer of hope. PLoS Med. 2007; 4: e332.
  • Coura JR. Chagas disease: control, elimination and eradication. Is it possible?. Mem Inst Oswaldo Cruz. 2013; 108: 962–7.
  • Coura JR, Vinas PA. Chagas disease: a new worldwide challenge. Nature. 2010; 465: S6–7.
  • Gascon J, Vilasanjuan R, Lucas A. The need for global collaboration to tackle hidden public health crisis of Chagas disease. Expert Rev Anti Infect Ther. 2014; 12: 393–5.
  • Alvarez JM, Fonseca R, Borges da Silva H, Marinho CR, Bortoluci KR, Sardinha LR et al. Chagas disease: still many unsolved issues. Mediators Inflamm. 2014; 2014: 912965.
  • Alves MJ, Colli W. Glycoproteins from Trypanosoma cruzi: partial purification by gel chromatography. FEBS Lett. 1975; 52: 188–90.
  • Acosta-Serrano A, Almeida IC, Freitas-Junior LH, Yoshida N, Schenkman S. The mucin-like glycoprotein super-family of Trypanosoma cruzi: structure and biological roles. Mol Biochem Parasitol. 2001; 114: 143–50.
  • Buscaglia CA, Campo VA, Frasch AC, Di Noia JM. Trypanosoma cruzi surface mucins: host-dependent coat diversity. Nat Rev Microbiol. 2006; 4: 229–36.
  • Mendonca-Previato L, Penha L, Garcez TC, Jones C, Previato JO. Addition of alpha-O-GlcNAc to threonine residues define the post-translational modification of mucin-like molecules in Trypanosoma cruzi. Glycoconj J. 2013; 30: 659–66.
  • de Lederkremer RM, Colli W. Galactofuranose-containing glycoconjugates in trypanosomatids. Glycobiology. 1995; 5: 547–52.
  • Macrae JI, Acosta-Serrano A, Morrice NA, Mehlert A, Ferguson MA. Structural characterization of NETNES, a novel glycoconjugate in Trypanosoma cruzi epimastigotes. J Biol Chem. 2005; 280: 12201–11.
  • Alves MJ, Colli W. Role of the gp85/trans-sialidase superfamily of glycoproteins in the interaction of Trypanosoma cruzi with host structures. Subcell Biochem. 2008; 47: 58–69. [PubMed Abstract].
  • Frasch AC. Functional diversity in the trans-sialidase and mucin families in Trypanosoma cruzi. Parasitol Today. 2000; 16: 282–6.
  • Ouaissi MA, Dubremetz JF, Kusnierz JP, Cornette J, Loyens M, Taibi A et al. Trypanosoma cruzi: differential expression and distribution of an 85-kDa polypeptide epitope by in vitro developmental stages. Exp Parasitol. 1990; 71: 207–17.
  • Maric D, McGwire BS, Buchanan KT, Olson CL, Emmer BT, Epting CL et al. Molecular determinants of ciliary membrane localization of Trypanosoma cruzi flagellar calcium-binding protein. J Biol Chem. 2011; 286: 33109–17.
  • Nakayasu ES, Almeida IC. Proteomics studies in Trypanosoma cruzi. 2008; Bethesda, MD: National Center for Biotechnological Information (US).
  • Torrecilhas AC, Schumacher RI, Alves MJ, Colli W. Vesicles as carriers of virulence factors in parasitic protozoan diseases. Microbes Infect. 2012; 14: 1465–74.
  • Magdesian MH, Tonelli RR, Fessel MR, Silveira MS, Schumacher RI, Linden R et al. A conserved domain of the gp85/trans-sialidase family activates host cell extracellular signal-regulated kinase and facilitates Trypanosoma cruzi infection. Exp Cell Res. 2007; 313: 210–18.
  • Magdesian MH, Giordano R, Ulrich H, Juliano MA, Juliano L, Schumacher RI et al. Infection by Trypanosoma cruzi. Identification of a parasite ligand and its host cell receptor. J Biol Chem. 2001; 276: 19382–9.
  • Almeida IC, Gazzinelli RT. Proinflammatory activity of glycosylphosphatidylinositol anchors derived from Trypanosoma cruzi: structural and functional analyses. J Leukoc Biol. 2001; 70: 467–77. [PubMed Abstract].
  • Bermejo DA, Jackson SW, Gorosito-Serran M, Acosta-Rodriguez EV, Amezcua-Vesely MC, Sather BD et al. Trypanosoma cruzi trans-sialidase initiates a program independent of the transcription factors RORgammat and Ahr that leads to IL-17 production by activated B cells. Nat Immunol. 2013; 14: 514–22.
  • Freire-de-Lima L, Oliveira IA, Neves JL, Penha LL, Alisson-Silva F, Dias WB et al. Sialic acid: a sweet swing between mammalian host and Trypanosoma cruzi. Front Immunol. 2012; 3: 356.
  • Pereira-Chioccola VL, Acosta-Serrano A, Correia de Almeida I, Ferguson MA, Souto-Padron T, Rodrigues MM et al. Mucin-like molecules form a negatively charged coat that protects Trypanosoma cruzi trypomastigotes from killing by human anti-alpha-galactosyl antibodies. J Cell Sci. 2000; 113: 1299–307. [PubMed Abstract].
  • Almeida IC, Ferguson MA, Schenkman S, Travassos LR. Lytic anti-alpha-galactosyl antibodies from patients with chronic Chagas’ disease recognize novel O-linked oligosaccharides on mucin-like glycosyl-phosphatidylinositol-anchored glycoproteins of Trypanosoma cruzi. Biochem J. 1994; 304: 793–802. [PubMed Abstract] [PubMed CentralFull Text].
  • Almeida IC, Milani SR, Gorin PA, Travassos LR. Complement-mediated lysis of Trypanosoma cruzi trypomastigotes by human anti-alpha-galactosyl antibodies. J Immunol. 1991; 146: 2394–400. [PubMed Abstract].
  • Giordano R, Fouts DL, Tewari D, Colli W, Manning JE, Alves MJ. Cloning of a surface membrane glycoprotein specific for the infective form of Trypanosoma cruzi having adhesive properties to laminin. J Biol Chem. 1999; 274: 3461–8.
  • Marroquin-Quelopana M, Oyama S Jr, Aguiar Pertinhez T, Spisni A, Aparecida Juliano M, Juliano L et al. Modeling the Trypanosoma cruzi Tc85–11 protein and mapping the laminin-binding site. Biochem Biophys Res Commun. 2004; 325: 612–18.
  • De Pablos LM, Osuna A. Multigene families in Trypanosoma cruzi and their role in infectivity. Infect Immun. 2012; 80: 2258–64.
  • Bayer-Santos E, Aguilar-Bonavides C, Rodrigues SP, Cordero EM, Marques AF, Varela-Ramirez A et al. Proteomic analysis of Trypanosoma cruzi secretome: characterization of two populations of extracellular vesicles and soluble proteins. J Proteome Res. 2013; 12: 883–97.
  • Almeida IC, Krautz GM, Krettli AU, Travassos LR. Glycoconjugates of Trypanosoma cruzi: a 74 kD antigen of trypomastigotes specifically reacts with lytic anti-alpha-galactosyl antibodies from patients with chronic Chagas disease. J Clin Lab Anal. 1993; 7: 307–16.
  • Cestari I, Ansa-Addo E, Deolindo P, Inal JM, Ramirez MI. Trypanosoma cruzi immune evasion mediated by host cell-derived microvesicles. J Immunol. 2012; 188: 1942–52.
  • Ghildiyal M, Zamore PD. Small silencing RNAs: an expanding universe. Nat Rev Genet. 2009; 10: 94–108.
  • Garcia-Silva MR, das Neves RF, Cabrera-Cabrera F, Sanguinetti J, Medeiros LC, Robello C et al. Extracellular vesicles shed by Trypanosoma cruzi are linked to small RNA pathways, life cycle regulation, and susceptibility to infection of mammalian cells. Parasitol Res. 2014; 113: 285–304.
  • Bayer-Santos E, Lima FM, Ruiz JC, Almeida IC, da Silveira JF. Characterization of the small RNA content of Trypanosoma cruzi extracellular vesicles. Mol Biochem Parasitol. 2014; 193: 71–4.
  • Garcia-Silva MR, Cabrera-Cabrera F, das Neves RF, Souto-Padron T, de Souza W, Cayota A. Gene expression changes induced by Trypanosoma cruzi shed microvesicles in mammalian host cells: relevance of tRNA-derived halves. BioMed Res Int. 2014; 2014: 305239.
  • Gazos-Lopes F, Oliveira MM, Hoelz LV, Vieira DP, Marques AF, Nakayasu ES et al. Structural and functional analysis of a platelet-activating lysophosphatidylcholine of Trypanosoma cruzi. PLoS Negl Trop Dis. 2014; 8: e3077.
  • Neves RF, Fernandes AC, Meyer-Fernandes JR, Souto-Padron T. Trypanosoma cruzi-secreted vesicles have acid and alkaline phosphatase activities capable of increasing parasite adhesion and infection. Parasitol Res. 2014; 113: 2961–72.
  • WHO. Leishmaniasis. World Health Organization. 2014. Available from: http://www.who.int/mediacentre/factsheets/fs375/en/.
  • Silverman JM, Chan SK, Robinson DP, Dwyer DM, Nandan D, Foster LJ et al. Proteomic analysis of the secretome of Leishmania donovani. Genome Biol. 2008; 9: R35.
  • Silverman JM, Clos J, de'Oliveira CC, Shirvani O, Fang Y, Wang C et al. An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages. J Cell Sci. 2010; 123: 842–52.
  • Silverman JM, Clos J, Horakova E, Wang AY, Wiesgigl M, Kelly I et al. Leishmania exosomes modulate innate and adaptive immune responses through effects on monocytes and dendritic cells. J Immunol. 2010; 185: 5011–22.
  • Hassani K, Olivier M. Immunomodulatory impact of Leishmania-induced macrophage exosomes: a comparative proteomic and functional analysis. PLoS Negl Trop Dis. 2013; 7: e2185.
  • Ghosh J, Bose M, Roy S, Bhattacharyya SN. Leishmania donovani targets Dicer1 to downregulate miR-122, lower serum cholesterol, and facilitate murine liver infection. Cell Host Microbe. 2013; 13: 277–88.
  • Schnitzer JK, Berzel S, Fajardo-Moser M, Remer KA, Moll H. Fragments of antigen-loaded dendritic cells (DC) and DC-derived exosomes induce protective immunity against Leishmania major. Vaccine. 2010; 28: 5785–93.
  • Hassani K, Shio MT, Martel C, Faubert D, Olivier M. Absence of metalloprotease GP63 alters the protein content of Leishmania exosomes. PLoS One. 2014; 9: e95007.
  • de Miguel N, Lustig G, Twu O, Chattopadhyay A, Wohlschlegel JA, Johnson PJ. Proteome analysis of the surface of Trichomonas vaginalis reveals novel proteins and strain-dependent differential expression. Mol Cell Proteomics. 2010; 9: 1554–66.
  • de Miguel N, Riestra A, Johnson PJ. Reversible association of tetraspanin with Trichomonas vaginalis flagella upon adherence to host cells. Cell Microbiol. 2012; 14: 1797–807.
  • Twu O, de Miguel N, Lustig G, Stevens GC, Vashisht AA, Wohlschlegel JA et al. Trichomonas vaginalis exosomes deliver cargo to host cells and mediate hostratioparasite interactions. PLoS Pathog. 2013; 9: e1003482.
  • Deolindo P, Evans-Osses I, Ramirez MI. Microvesicles and exosomes as vehicles between protozoan and host cell communication. Biochem Soc Trans. 2013; 41: 252–7.
  • Wampfler PB, Tosevski V, Nanni P, Spycher C, Hehl AB. Proteomics of secretory and endocytic organelles in Giardia lamblia. PLoS One. 2014; 9: e94089.
  • Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J. Helminth infections: the great neglected tropical diseases. J Clin Investig. 2008; 118: 1311–21.
  • Toledo R, Bernal MD, Marcilla A. Proteomics of foodborne trematodes. J Proteomics. 2011; 74: 1485–503.
  • Hewitson JP, Ivens AC, Harcus Y, Filbey KJ, McSorley HJ, Murray J et al. Secretion of protective antigens by tissue-stage nematode larvae revealed by proteomic analysis and vaccination-induced sterile immunity. PLoS Pathog. 2013; 9: e1003492.
  • Marcilla A, Trelis M, Cortes A, Sotillo J, Cantalapiedra F, Minguez MT et al. Extracellular vesicles from parasitic helminths contain specific excretory/secretory proteins and are internalized in intestinal host cells. PLoS One. 2012; 7: e45974.
  • Andresen K, Simonsen PE, Andersen BJ, Birch-Andersen A. Echinostoma caproni in mice: shedding of antigens from the surface of an intestinal trematode. Int J Parasitol. 1989; 19: 111–18.
  • Threadgold LT. The ultrastructure of the “cuticle” of Fasciola hepatica. Exp Cell Res. 1963; 30: 238–42.
  • Wilson RA, Wright JM, de Castro-Borges W, Parker-Manuel SJ, Dowle AA, Ashton PD et al. Exploring the Fasciola hepatica tegument proteome. Int J Parasitol. 2011; 41: 1347–59.
  • Wilson RA, Barnes PE. The formation and turnover of the membranocalyx on the tegument of Schistosoma mansoni. Parasitology. 1977; 74: 61–71.
  • Robinson MW, Menon R, Donnelly SM, Dalton JP, Ranganathan S. An integrated transcriptomics and proteomics analysis of the secretome of the helminth pathogen Fasciola hepatica: proteins associated with invasion and infection of the mammalian host. Mol Cell Proteomics. 2009; 8: 1891–907.
  • Sotillo J, Valero ML, Sanchez Del Pino MM, Fried B, Esteban JG, Marcilla A et al. Excretory/secretory proteome of the adult stage of Echinostoma caproni. Parasitol Res. 2010; 107: 691–7.
  • Kalra H, Simpson RJ, Ji H, Aikawa E, Altevogt P, Askenase P et al. Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol. 2012; 10: e1001450.
  • Mulvenna J, Moertel L, Jones MK, Nawaratna S, Lovas EM, Gobert GN et al. Exposed proteins of the Schistosoma japonicum tegument. Int J Parasitol. 2010; 40: 543–54.
  • Garg G, Bernal D, Trelis M, Forment J, Ortiz J, Valero ML et al. The transcriptome of Echinostoma caproni adults: further characterization of the secretome and identification of new potential drug targets. J Proteomics. 2013; 89: 202–14.
  • Young ND, Hall RS, Jex AR, Cantacessi C, Gasser RB. Elucidating the transcriptome of Fasciola hepatica – a key to fundamental and biotechnological discoveries for a neglected parasite. Biotechnol Adv. 2010; 28: 222–31.
  • Gallo A, Tandon M, Alevizos I, Illei GG. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS One. 2012; 7: e30679.
  • Xu L, Yang BF, Ai J. MicroRNA transport: a new way in cell communication. J Cell Physiol. 2013; 228: 1713–19.
  • Li H, Huang S, Guo C, Guan H, Xiong C. Cell-free seminal mRNA and microRNA exist in different forms. PLoS One. 2012; 7: e34566.
  • Vickers KC, Remaley AT. Lipid-based carriers of microRNAs and intercellular communication. Curr Opin Lipidol. 2012; 23: 91–7.
  • Bernal D, Trelis M, Montaner S, Cantalapiedra F, Galiano A, Hackenberg M et al. Surface analysis of Dicrocoelium dendriticum. The molecular characterization of exosomes reveals the presence of miRNAs. J Proteomics. 2014; 105: 232–41.
  • Liegeois S, Benedetto A, Garnier JM, Schwab Y, Labouesse M. The V0-ATPase mediates apical secretion of exosomes containing Hedgehog-related proteins in Caenorhabditis elegans. J Cell Biol. 2006; 173: 949–61.
  • Buck AH, Coakley G, Simbari F, McSorley HJ, Quintana JF, Le Bihan T et al. Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nat Commun. 2014; 5: 5488.
  • Wang T, Van Steendam K, Dhaenens M, Vlaminck J, Deforce D, Jex AR et al. Proteomic analysis of the excretory-secretory products from larval stages of Ascaris suum reveals high abundance of glycosyl hydrolases. PLoS Negl Trop Dis. 2013; 7: e2467.
  • Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med. 1996; 183: 1161–72.
  • Properzi F, Logozzi M, Fais S. Exosomes: the future of biomarkers in medicine. Biomark Med. 2013; 7: 769–78.
  • WHO. 2014. Available from: http://www.who.int/mediacentre/factsheets/en/.