Extracellular vesicles in parasitic diseases

Journal of Extracellular Vesicles

Volumn 3, Issue 1, 2014, Pages

  Marcilla, Antonio ^a   Martin Jaular, Lorena ^b   Trelis, Maria ^a   de Menezes Neto, Armando ^b   Osuna, Antonio ^c   Bernal, Dolores ^a   Fernandez Becerra, Carmen ^b   Almeida, Igor C ^d   del Portillo, Hernando A ^b,e  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSITY OF GRANADA   (Spain)

^d UNIVERSITY OF TEXAS AT EL PASO   (United States)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

Exosomes; Extracellular vesicles; Helminths; Microvesicles; Parasites; Protozoa

Indexed keywords

APICOMPLEXA; CELL COMMUNICATION; CRYPTOSPORIDIUM; CRYPTOSPORIDIUM PARVUM; DICROCOELIUM DENDRITICUM; ECHINOSTOMA CAPRONI; EXOSOME; FASCIOLA HEPATICA; GIARDIA INTESTINALIS; HELIGMOSOMOIDES POLYGYRUS; HELMINTH; HUMAN; IMMUNOMODULATION; KINETOPLASTIDA; LEISHMANIA; NEMATODE; NONHUMAN; PARASITE IMMUNITY; PARASITOSIS; PLASMODIUM; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; PLASMODIUM YOELII; PLATYHELMINTH; PROTOZOON; REVIEW; TOXOPLASMA; TOXOPLASMA GONDII; TRICHOMONAS VAGINALIS; TRYPANOSOMA; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI;

EID: 85015287454     PISSN: None     EISSN: 20013078     Source Type: Journal    
DOI: 10.3402/jev.v3.25040     Document Type: Review

References (133)

1. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013;200:373-83.
2. Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol. 2009;9:581-93.
3. Simons M, Raposo G. Exosomes-vesicular carriers for intercellular communication. Curr Opin Cell Biol. 2009;21:575-81.
4. Bobrie A, Colombo M, Raposo G, Thery C. Exosome secretion: molecular mechanisms and roles in immune responses. Traffic. 2011;12:1659-68.
5. Hugel B, Martinez MC, Kunzelmann C, Freyssinet JM. Membrane microparticles: two sides of the coin. Physiology. 2005;20:22-7.
6. 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.
7. 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.
8. Wubbolts R, Leckie RS, Veenhuizen PT, Schwarzmann G, MobiusW, 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.
9. 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.
10. Choi DS, Kim DK, Kim YK, Gho YS. Proteomics, transcriptomics and lipidomics of exosomes and ectosomes. Proteomics. 2013;13:1554-71.
11. Kastelowitz N, Yin H. Exosomes and microvesicles: identification and targeting by particle size and lipid chemical probes. Chembiochem. 2014;15:923-8.
12. Cox FE. History of human parasitology. Clin Microbiol Rev. 2002;15:595-612.
13. Schorey JS, Bhatnagar S. Exosome function: from tumor immunology to pathogen biology. Traffic. 2008;9:871-81.
14. Barteneva NS, Maltsev N, Vorobjev IA. Microvesicles and intercellular communication in the context of parasitism. Front Cell Infect Microbiol. 2013;3:49.
15. Twu O, Johnson PJ. Parasite extracellular vesicles: mediators of intercellular communication. PLoS Pathog. 2014;10: e1004289.
16. Reid AJ. Large, rapidly evolving gene families are at the forefront of host-parasite interactions in Apicomplexa. Parasitology. 2014:1-14.
17. Tulane. Apicomplexa 2010 [cited 2012 Dec 20]. Available from: http://www.tulane.edu/-wiser/protozoology/notes/api. html.
18. 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.
19. WHO. Malaria Fact Sheet No 94. Geneva; 2014. Available from: http://www.who.int/mediacentre/factsheets/fs094/en/.
20. Garnham PC. Malaria in mammals excluding man. Adv Parasitol. 1967;5:139-204.
21. Escalante AA, Ayala FJ. Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. Proc Natl Acad Sci USA. 1994;91:11373-7.
22. Cox FE. History of the discovery of the malaria parasites and their vectors. Parasites Vectors. 2010;3:5.
23. 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.
24. Nantakomol D, Dondorp AM, Krudsood S, Udomsangpetch R, Pattanapanyasat K, Combes V, et al. Circulating red cellderived microparticles in human malaria. J Infect Dis. 2011;203:700-6.
25. 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.
26. 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.
27. Coltel N, Combes V, Wassmer SC, Chimini G, Grau GE. Cell vesiculation and immunopathology: implications in cerebral malaria. Microbes Infect. 2006;8:2305-16.
28. 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.
29. 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.
30. 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.
31. Regev-Rudzki N, Wilson DW, Carvalho TG, Sisquella X, Coleman BM, RugM, et al. Cell-cell communication between malaria-infected red blood cells via exosome-like vesicles. Cell. 2013;153:1120-33.
32. Mantel PY, Hoang AN, Goldowitz I, Potashnikova D, Hamza B, Vorobjev I, et al. Malaria-infected erythrocytederived microvesicles mediate cellular communication within the parasite population and with the host immune system. Cell Host Microbe. 2013;13:521-34.
33. Alano P, Carter R. Sexual differentiation in malaria parasites. Ann Rev Microbiol. 1990;44:429-49.
34. Dyer M, Day KP. Commitment to gametocytogenesis in Plasmodium falciparum. Parasitol Today. 2000;16:102-7.
35. 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.
36. Del Portillo HA, Chitnis CE. Talking to each other to initiate sexual differentiation. Cell. 2013;153:945-7.
37. 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.
38. CDC. Parasites-Toxoplasmosis (Toxoplasma infection) 2013 [cited 2013 Jan 10]. Available from: http://www.cdc.gov/parasites/toxoplasmosis/epi.html.
39. 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.
40. Chaput N, Thery C. Exosomes: immune properties and potential clinical implementations. Semin Immunopathol. 2011;33: 419-40.
41. 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.
42. 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.
43. 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.
44. 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.
45. Tulane. Kinetoplastids. New Orleans: Tulane University; 1999 [cited 2013 Oct 16]. Available from: http://www.tulane. edu/-wiser/protozoology/notes/kinet.html.
46. Barrett MP, Burchmore RJ, Stich A, Lazzari JO, Frasch AC, Cazzulo JJ, et al. The trypanosomiases. Lancet. 2003;362: 1469-80.
47. Rodrigues JC, Godinho JL, de Souza W. Biology of human pathogenic trypanosomatids: epidemiology, lifecycle and ultrastructure. Subcell Biochem. 2014;74:1-42.
48. 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.
49. 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;75:11-7.
50. da Silveira JF, Abrahamsohn PA, Colli W. Plasma membrane vesicles isolated from epimastigote forms of Trypanosoma cruzi. Biochim Biophys Acta. 1979;550:222-32.
51. Gonçalves MF, Umezawa ES, Katzin AM, de SouzaW, Alves MJ, Zingales B, et al. Trypanosoma cruzi: shedding of surface antigens as membrane vesicles. Exp Parasitol. 1991;72:43-53.
52. 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.
53. Brun R, Blum J. Human African trypanosomiasis. Infect Dis Clin North Am. 2012;26:261-73.
54. Brun R, Blum J, Chappuis F, Burri C. Human African trypanosomiasis. Lancet. 2010;375:148-59.
55. Kennedy PG. Clinical features, diagnosis, and treatment of human African trypanosomiasis (sleeping sickness). Lancet Neurol. 2013;12:186-94.
56. 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.
57. 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.
58. Yoshida N, Tyler KM, Llewellyn MS. Invasion mechanisms among emerging food-borne protozoan parasites. Trends Parasitol. 2011;27:459-66.
59. 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.
60. Coura JR. Chagas disease: control, elimination and eradication. Is it possible? Mem Inst Oswaldo Cruz. 2013;108:962-7.
61. Coura JR, Vinas PA. Chagas disease: a new worldwide challenge. Nature. 2010;465:S6-7.
62. 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.
63. 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.
64. Alves MJ, Colli W. Glycoproteins from Trypanosoma cruzi: partial purification by gel chromatography. FEBS Lett. 1975; 52:188-90.
65. 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.
66. Buscaglia CA, Campo VA, Frasch AC, Di Noia JM. Trypanosoma cruzi surface mucins: host-dependent coat diversity. Nat Rev Microbiol. 2006;4:229-36.
67. 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.
68. de Lederkremer RM, Colli W. Galactofuranose-containing glycoconjugates in trypanosomatids. Glycobiology. 1995;5: 547-52.
69. 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.
70. 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.
71. Frasch AC. Functional diversity in the trans-sialidase and mucin families in Trypanosoma cruzi. Parasitol Today. 2000; 16:282-6.
72. 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.
73. Maric D, McGwire BS, Buchanan KT, Olson CL, Emmer BT, Epting CL, et al. Molecular determinants of ciliary membrane localization of Trypanosoma cruzi flagellar calciumbinding protein. J Biol Chem. 2011;286:33109-17.
74. Nakayasu ES, Almeida IC. Proteomics studies in Trypanosoma cruzi. Bethesda, MD: National Center for Biotechnological Information (US); 2008.
75. Torrecilhas AC, Schumacher RI, Alves MJ, Colli W. Vesicles as carriers of virulence factors in parasitic protozoan diseases. Microbes Infect. 2012;14:1465-74.
76. 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;313:210-8.
77. 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.
78. Almeida IC, Gazzinelli RT. Proinflammatory activity of glycosylphosphatidylinositol anchors derived from Trypanosoma cruzi: structural and functional analyses. J Leukoc Biol. 2001;70:467-77.
79. 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.
80. 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.
81. 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.
82. 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.
83. Almeida IC, Milani SR, Gorin PA, Travassos LR. Complementmediated lysis of Trypanosoma cruzi trypomastigotes by human anti-alpha-galactosyl antibodies. J Immunol. 1991;146:2394-400.
84. 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.
85. 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 lamininbinding site. Biochem Biophys Res Commun. 2004;325:612-8.
86. De Pablos LM, Osuna A. Multigene families in Trypanosoma cruzi and their role in infectivity. Infect Immun. 2012;80: 2258-64.
87. 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.
88. 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.
89. Cestari I, Ansa-Addo E, Deolindo P, Inal JM, Ramirez MI. Trypanosoma cruzi immune evasion mediated by host cellderived microvesicles. J Immunol. 2012;188:1942-52.
90. Ghildiyal M, Zamore PD. Small silencing RNAs: an expanding universe. Nat Rev Genet. 2009;10:94-108.
91. 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.
92. 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.
93. 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.
94. 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.
95. 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.
96. WHO. Leishmaniasis. World Health Organization; 2014. Available from: http://www.who.int/mediacentre/factsheets/fs375/en/.
97. 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.
98. 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.
99. 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.
100. Hassani K, Olivier M. Immunomodulatory impact of Leishmania-induced macrophage exosomes: a comparative proteomic and functional analysis. PLoS Negl Trop Dis. 2013;7:e2185.
101. 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.
102. 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.
103. 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.
104. deMiguel 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.
105. 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.
106. 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.
107. 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.
108. Wampfler PB, Tosevski V, Nanni P, Spycher C, Hehl AB. Proteomics of secretory and endocytic organelles in Giardia lamblia. PLoS One. 2014;9:e94089.
109. 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.
110. Toledo R, Bernal MD, Marcilla A. Proteomics of foodborne trematodes. J Proteomics. 2011;74:1485-503.
111. Hewitson JP, Ivens AC, Harcus Y, Filbey KJ, McSorley HJ, Murray J, et al. Secretion of protective antigens by tissuestage nematode larvae revealed by proteomic analysis and vaccination-induced sterile immunity. PLoS Pathog. 2013;9: e1003492.
112. 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.
113. 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: 111-8.
114. Threadgold LT. The ultrastructure of the ''cuticle'' of Fasciola hepatica. Exp Cell Res. 1963;30:238-42.
115. 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.
116. Wilson RA, Barnes PE. The formation and turnover of the membranocalyx on the tegument of Schistosoma mansoni. Parasitology. 1977;74:61-71.
117. 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.
118. 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.
119. 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.
120. 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.
121. 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.
122. 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.
123. 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.
124. Xu L, Yang BF, Ai J. MicroRNA transport: a new way in cell communication. J Cell Physiol. 2013;228:1713-9.
125. 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.
126. Vickers KC, Remaley AT. Lipid-based carriers of microRNAs and intercellular communication. Curr Opin Lipidol. 2012; 23:91-7.
127. 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.
128. 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.
129. 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.
130. Wang T, Van Steendam K, Dhaenens M, Vlaminck J, Deforce D, Jex AR, et al. Proteomic analysis of the excretorysecretory products from larval stages of Ascaris suum reveals high abundance of glycosyl hydrolases. PLoS Negl Trop Dis. 2013;7:e2467.
131. 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.
132. Properzi F, Logozzi M, Fais S. Exosomes: the future of biomarkers in medicine. Biomark Med. 2013;7:769-78.
133. WHO. 2014. Available from: http://www.who.int/mediacentre/factsheets/en/.