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A new landscape of host–protozoa interactions involving the extracellular vesicles world

Published online by Cambridge University Press:  10 July 2018

Bruno Gavinho ,
Izadora Volpato Rossi ,
Ingrid Evans-Osses ,
Jameel Inal  and
Marcel I. Ramirez Open the ORCID record for Marcel I. Ramirez [Opens in a new window]
Bruno Gavinho
Affiliation:
Departamento de Bioquímica e Biologia molecular, Universidade Federal de Paraná, Curitiba, Paraná, Brazil
Izadora Volpato Rossi
Affiliation:
Departamento de Bioquímica e Biologia molecular, Universidade Federal de Paraná, Curitiba, Paraná, Brazil
Ingrid Evans-Osses
Affiliation:
Departamento de Bioquímica e Biologia molecular, Universidade Federal de Paraná, Curitiba, Paraná, Brazil
Jameel Inal
Affiliation:
Bioscience Research Group, School of Life and Medical Sciences, University of Hertfordshire, Hatfield, UK
Marcel I. Ramirez*
Affiliation:
Departamento de Bioquímica e Biologia molecular, Universidade Federal de Paraná, Curitiba, Paraná, Brazil Instituto Oswaldo Cruz- Fiocruz, Rio de Janeiro, Brazil
*
Author for correspondence: Marcel I. Ramirez, E-mail: marcel.ivan.ramirez@gmail.com
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Abstract

Extracellular vesicles (EVs) are released by a wide number of cells including blood cells, immune system cells, tumour cells, adult and embryonic stem cells. EVs are a heterogeneous group of vesicles (~30–1000 nm) including microvesicles and exosomes. The physiological release of EVs represents a normal state of the cell, raising a metabolic equilibrium between catabolic and anabolic processes. Moreover, when the cells are submitted to stress with different inducers or in pathological situations (malignancies, chronic diseases, infectious diseases.), they respond with an intense and dynamic release of EVs. The EVs released from stimulated cells vs those that are released constitutively may themselves differ, both physically and in their cargo. EVs contain protein, lipids, nucleic acids and biomolecules that can alter cell phenotypes or modulate neighbouring cells. In this review, we have summarized findings involving EVs in certain protozoan diseases. We have commented on strategies to study the communicative roles of EVs during host–pathogen interaction and hypothesized on the use of EVs for diagnostic, preventative and therapeutic purposes in infectious diseases. This kind of communication could modulate the innate immune system and reformulate concepts in parasitism. Moreover, the information provided within EVs could produce alternatives in translational medicine.

Keywords

Exosomesextracellular vesiclesimmunologymicrovesiclesprotozoan
Type
Review Article
Information
Parasitology , Volume 145 , Issue 12 , October 2018 , pp. 1521 - 1530
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Copyright
Copyright © Cambridge University Press 2018 

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References

Alegre, E, Sanmamed, MF, Rodriguez, C, Carranza, O, Martín-Algarra, S and González, A (2014) Study of circulating MicroRNA-125b levels in serum exosomes in advanced melanoma. Archives of Pathology & Laboratory Medicine 138, 828–832.Google Scholar
Alexander, M, Hu, R, Runtsch, MC, Kagele, DA, Mosbruger, TL, Tolmachova, T, Seabra, MC, Round, JL, Ward, D and O´Connell, RM (2015) Exosome-delivered microRNAs modulate the inflammatory response to endotoxin. Nature Communications 6, 1–16.Google Scholar
Aline, F, Bout, D, Amigorena, S, Roingeard, P and Dimier-Poisson, I (2004) Toxoplasma gondii Antigen-pulsed-dendritic cell derived exosomes induce a protective immune response against T. gondii infection. Infection and Immunity 72, 4127–4137.Google Scholar
Alvarez-Erviti, L, Seow, Y, Yin, H, Betts, C, Lakhal, S and Wood, MJA (2011) Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nature Biotechnology 29, 341–345.Google Scholar
Atayde, VD, Hassani, K, Filho, ASL, Borges, AR, Adhikari, A, Martel, C and Olivier, M (2016) Leishmania exosomes and other virulence factors: impact on innate immune response and macrophage functions. Cellular Immunology 309, 7–18.Google Scholar
Barile, L and Vassali, G (2017) Pharmacology & therapeutics exosomes: therapy delivery tools and biomarkers of diseases. Pharmacology & Therapeutics 174, 63–78.Google Scholar
Bautista-López, NL, Ndao, M and Camargo, V (2017) Characterization and diagnostic application of T rypanosoma cruzi Trypomastigote excreted-secreted antigens shed in extracellular vesicles released from infected mammalian cells. Journal of Clinical Microbiology 55, 744–758.Google Scholar
Bayer-Santos, E, Aguilar-Bonavides, C, Rodrigues, SP, Cordero, EM, Marques, AF, Varela-Ramirez, A, Choi, H, Yoshida, N, da Silveira, JF and Almeida, IC (2013) Proteomic analysis of T rypanosoma cruzi secretome: characterization of two populations of extracellular vesicles and soluble proteins. Journal of Proteome Research 12, 883–897.Google Scholar
Bayer-Santos, E, Lima, FM, Ruiz, JC, Almeida, IC and Silveira, JF (2014) Characterization of the small RNA content of Trypanosoma cruzi extracellular vesicles. Molecular Biochemistry Parasitology 193, 71–74.Google Scholar
Beauvillain, C, Ruiz, S, Guiton, R, Bout, D and Dimier-Poisson, I (2007) A vaccine based on exosomes secreted by a dendritic cell line confers protection against T. gondii infection in syngeneic and allogeneic mice. Microbes and Infection 9, 1614–1622.Google Scholar
Beauvillain, C, Juste, MO, Dion, S, Pierre, J and Dimier-Poisson, I (2009) Exosomes are an effective vaccine against congenital toxoplasmosis in mice. Vaccine 27, 1750–1757.Google Scholar
Birkeland, SR, Preheim, SP, Davids, BJ, Cipriano, MJ, Palm, D, Reiner, DS, Svärd, SG, Gillin, FD and McArthur, AG (2010) Transcriptome analyses of the Giardia lamblia life cycle. Molecular & Biochemical Parasitology 174, 62–65.Google Scholar
Bruno, S, Grange, C, Collino, F, Deregibus, MC, Cantaluppi, V, Biancone, L, Tetta, C and Camussi, G (2012) Microvesicles derived from mesenchymal stem cells enhance survival in a lethal model of acute kidney injury. PLoS ONE 7, 1–11.Google Scholar
Buck, AH, Coakley, G, Simbari, F, McSorley, HJ, Quintana, JF, Bihan, TL, Kumar, S, Abreu-Goodger, C, Lear, M, Harcus, Y, Ceroni, A, Babayan, SA, Blaxter, M, Ivens, A and Maizels, RM (2014) Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nature Communications 5.Google Scholar
Campos, FMF, Franklin, BS, Teixeira-Carvalho, A, Filho, ALS, de Paula, SCO, Fontes, CJ, Brito, CF and Carvalho, LH (2010) Augmented plasma microparticles during acute P lasmodium vivax infection. Malaria Journal 9, 327–334.Google Scholar
CDC–Center for Disease Control and Prevention (2015). https://www.cdc.gov/malaria/about/index.html.Google Scholar
Cestari, I, Ansa-Addo, E, Deolindo, P, Inal, JM and Ramirez, MI (2012) Trypanosoma cruzi immune evasion mediated by host cell-derived microvesicles. The Journal of Immunology 188, 1942–1952.Google Scholar
Chira, S, Gulei, D, Hajitou, A, Zimta, A, Cordelier, P and Berindan-Neagoe, I (2017) CRISPR/cas9: transcending the reality of genome editing. Molecular Therapy. Nucleic Acids 7, 211–222.Google Scholar
Coakley, G, McCaskill, JL, Borger, JG, Simbari, F, Robertson, E, Millar, M, Harcus, Y, McSorley, HJ, Maizels, RM and Buck, AH (2017) Extracellular vesicles from a helminth parasite suppress macrophage activation and constitute an effective vaccine for protective immunity. Cell Reports 19, 1545–1557.Google Scholar
Cocucci, E and Meldolesi, J (2015) Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biology 25, 364–372.Google Scholar
Combes, V, Taylor, TE, Juhan-Vague, I, Mège, JL, Mwenechanya, J, Tembo, M, Grau, GE and Molyneux, ME (2004) Circulating endothelial microparticles in Malawian children with severe falciparum malaria complicated with coma. Journal of American Medical Association 291, 2542–2544.Google Scholar
del Cacho, E, Gallego, M, Lee, SH, Lillehoj, HS, Quilez, J, Lillehoj, EP and Sánchez-Acedo, C (2012) Induction of protective immunity against Eimeria tenella, Eimeria maxima, and Eimeria acervulina infections using dendritic cell-derived exosomes. Infection and Immunity 80, 1909–1916.Google Scholar
Dlugonska, H and Gatkowska, J (2016) Exosomes in the context of Toxoplasma gondii–host communication. Annals of Parasitology 62, 169–174.Google Scholar
Eirin, A, Riester, SM, Zhu, XY, Tang, H, Evans, JM, O´Brien, D, van Wijnen, AJ and Lerman, LO (2014) MicroRNA and mRNA cargo of extracellular vesicles from porcine adipose tissue-derived mesenchymal stem cells. Gene 551, 55–64.Google Scholar
El-Assaad, F, Wheway, J, Hunt, NH, Grau, GER and Combes, V (2014) Production, fate and pathogenicity of plasma microparticles in murine cerebral malaria. Plos Pathogens 10.Google Scholar
Eliaz, D, Kannan, S, Shaked, H, Arvatz, G, Tkacz, ID, Binder, L, Ben-Asher, HW, Okalang, U, Chikne, V, Cohen-Chalamish, S and Michaeli, S (2017) Exosome secretion affects social motility in Trypanosoma brucei. PLoS Pathogens 13. doi: 10.1371/journal.ppat.1006245Google Scholar
Escudier, B, Dorval, T, Chaput, N, André, F, Caby, MP, Novault, S, Flament, C, Leboulaire, C, Borq, C, Amigorena, S, Boccaccio, C, Bonnerot, C, Dhellin, O, Movassaqh, M, Piperno, S, Robert, C, Serra, V, Valente, N, Le Pecq, JB, Spatz, A, Lantz, O, Tursz, T, Angevin, E and Zitvogel, L (2005) Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of the first phase I clinical trial. Journal of Translational Medicine 3, 10.Google Scholar
Evans-Osses, I, Reichembach, LH and Ramirez, MI (2015) Exosomes or microvesicles? Two kinds of extracellular vesicles with different routes to modify protozoan-host cell interaction. Parasitology Research 114, 3567–3575.Google Scholar
Evans-Osses, I, Mojoli, A, Monguió-Tortajada, MM, Marcilla, A, Aran, V, Amorin, M, Inal, J, Borràs, FE and Ramirez, MI (2017) Microvesicles released from Giardia intestinalis disturbs host-pathogen response in vitro. European Journal of Cell Biology 96, 131–142.Google Scholar
Fontana, JM, Alexander, E and Salvatore, M (2012) Translational research in infectious diseases: current paradigms and challenges ahead. Translational Research 159, 430–456.Google Scholar
Fujii, T, Sakata, A, Nishimura, S, Eto, K and Nagata, S (2015) TMEM16F is required for phosphatidylserine exposure and microparticle release in activated mouse platelets. Proceedings of the National Academy of Sciences of the USA 112, 12800–5.Google Scholar
Gardiner, C, Ferreira, YJ, Dragovic, RA, Redman, CWG and Sargent, IL (2013) Extracellular vesicle sizing and enumeration by nanoparticle tracking analysis. Journal of Extracellular Vesicles 2, 19671.Google Scholar
Geiger, A, Hirtz, C, Bécue, T, Bellard, E, Centeno, D, Gargani, D, Rossignol, M, Cuny, G and Peltier, J (2010) Exocytosis and protein secretion in Trypanosoma. BMC Microbiology 10, 20.Google Scholar
Gonçalves, MF, Umezawa, ES, Katzin, AM, de Souza, W, Alves, MJ, Zingales, B and Colli, W (1991) Trypanosoma cruzi: shedding of surface antigens as membrane vesicles. Experimental Parasitology 72, 43–53.Google Scholar
Grébaut, P, Chuchana, P, Brizard, JP, Demettre, E, Seveno, M, Bossard, G, Jouin, P, Vincendeau, P, Bengaly, Z, Boulangé, A, Cuny, G and Holzmuller, P (2009) Identification of total and differentially expressed excreted-secreted proteins from Trypanosoma congolense strains exhibiting different virulence and pathogenicity. International Journal for Parasitology 39, 1137–1150.Google Scholar
Greening, DW, Gopal, SK, Xu, R, Simpson, RJ and Chen, W (2015) Exosomes and their roles in immune regulation and cancer. Seminars in Cell & Development Biology 40, 72–81.Google Scholar
Hart, CJS, Munro, T, Andrews, KT, Ryan, JH, Riches, AG and Skinner-Adams, TS (2017) A novel in vitro image-based assay identifies new drug leads for giardiasis. International Journal for Parasitology: Drugs and Drug Resistance 7, 83–89.Google Scholar
Hassani, K and Olivier, M (2013) Immunomodulatory impact of leishmania-induced macrophage exosomes: a comparative proteomic and functional analysis. Plos Neglected Tropical Diseases 7. doi: 10.1371/journal.pntd.0002185Google Scholar
Hassani, K, Shio, MT, Martel, C, Faubert, D and Olivier, M (2014) Absence of metalloprotease GP63 alters the protein content of leishmania exosomes. Plos ONE 9. doi: 10.1371/journal.pone.0095007Google Scholar
Hotez, PJ, Basañez, M, Acosta-Serrano, A and Grillet, ME (2017) Venezuela and its rising vector-borne neglected diseases. PLoS Neglected Tropical Diseases 11. doi: org/10.1371/journal.pntd.0005423Google Scholar
Inamdar, S, Nitiyanandan, R and Rege, K (2017) Emerging applications of exosomes in cancer therapeutics and diagnostics. Bioengineering & Translational Medicine 2, 70–80.Google Scholar
Kalra, H, Simpson, RJ, Ji, H, Aikawa, E, Atevogt, P, Askenase, P, Bond, VC, Borràs, FE, Breakefield, X, Budnik, V, Buzas, E, Camussi, G and Clayton, A (2012) Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biology 10, e1001450.Google Scholar
Kaur, H, Ghosh, S, Samra, H, Vinayak, VK and Ganguly, NK (2001) Identification and characterization of an excretory-secretory product from Giardia lamblia. Parasitology 123, 347–356.Google Scholar
Kho, WH, Geurden, T, Paget, T, O´Handley, R, Steuart, RF, Thompson, RC and Buret, AG (2013) Giardia duodenalis assemblage-specific induction of apoptosis and tight junction disruption in human intestinal epithelial cells: effects of apoptosis and tight junction disruption in human intestinal epithelial cells: effects of mixed infections. Journal of Parasitology 99, 353–358.Google Scholar
Kim, MJ, Jung, B, Cho, J, Song, H, Pyo, K, Lee, JM, Kim, M and Chai, J (2016) Exosomes secreted by Toxoplasma gondii-infected L6 cells: their effects on host cell proliferation and cell cycle changes. Korean Journal of Parasitology 54, 147–154.Google Scholar
Kim, SM, Yang, Y, Ih, SJ, Hong, Y, Seo, M and Jang, M (2017) Cancer-derived exosomes as a delivery platform of CRISPR/Cas9 confer cancer cell tropism-dependent targeting. Journal of Controlled Release 28, 8–16.Google Scholar
Klokousas, A, Shani, S, Hladky, SB, Barrand, MA and Veen, HW (2003) ABC transporters and drug resistance in parasitic protozoa. International Journal of Antimicrobial Agents 22, 301–317.Google Scholar
Lambertz, U, Oviedo Ovando, ME, Vasconcelos, EJ, Unrau, PJ, Myler, PJ and Reiner, NE (2015) Small RNAs derived from tRNAs and rRNAs are highly enriched in exosomes from both old and new world Leishmania providing evidence for conserved exosomal RNA packaging. BMC Genomics 16, 1–16.Google Scholar
Lechartier, B, Rybniker, J, Zumla, A and Cole, ST (2014) Tuberculosis drug discovery in the post-post-genomic era. EMBO Molecular Medicine 6, 158–168.Google Scholar
Lee, HY, Hyung, S, Lee, NY, Yog, TS, Han, SH and Park, SJ (2012) Excretory-secretory products of Giardia lamblia induce interleukin-8 production in human colonic cells via activation of p38, ERK1/2, NK-κB and AP-1. Parasite Immunology 34, 183–198.Google Scholar
Leitherer, S, Clos, J, Liebler-Tenorio, EM, Schleicher, U, Bogdan, C and Soulat, D (2017) Characterization of the protein tyrosine phosphatase LmPRL-1 secreted by Leishmania major via the exosome pathway. Infection and Immunity 85, 1–19.Google Scholar
Lieshout, VL and Roestenberg, M (2015) Clinical consequences of new diagnostic tools for intestinal parasites. Clinical Microbiology and Infection 21, 520–528.Google Scholar
Liu, S, da Cunha, AP, Rezende, RM, Cialic, R, Wei, Z, Bry, L, Comstock, LE, Gandhi, R and Weiner, HL (2016) The host shapes the Gut Microbiota via fecal MicroRNA. Cell Host & Microbe 19, 32–43.Google Scholar
Mantel, P, Hoang, AN, Goldowitz, I, Potashnikova, D, Hamza, B, Vorobjev, I, Ghiran, I, Toner, M, Irimia, D, Ivanov, AR, Barteneva, N and Marti, M (2013) Malaria-infected erythrocyte-derived microvesicles mediate cellular communication within the parasite population and with the host immune system. Cell Host and Microbe 13, 521–534.Google Scholar
Martin-Jaular, L, Nakayasu, ES, Ferrer, M, Almeida, IC and Portillo, HA (2011) Exosomes from Plasmodium yoelii-infected reticulocytes protect mice from lethal infections. PLoS ONE 6. doi: 10.1371/journal.pone.0026588.Google Scholar
Melo, SA, Luecke, LB, Kahlert, C, Fernandez, AF, Gammon, ST, Kaye, J, LeBleu, VS, Mittendorf, EA, Weitz, J, Rahbari, N, Reissfelder, C, Pilarsky, C, Fraga, MF, Piwnica-Worms, D and Kalluri, R (2015) Glypican1 identifies cancer exosomes and facilitates early detection of cancer. Nature 523, 177–182.Google Scholar
Menegon, M, Nurahmed, AM, Talha, AA, Nour, BYM and Severini, C (2016) Molecular surveillance of antimalarial drug resistance related genes in Plasmodium falciparum isolates from Eritrea. Acta Tropica 157, 158–161.Google Scholar
Momem-Heravi, F, Bala, S, Bukong, T and Szabo, G (2014) Exosome-mediated delivery of functionally active miRNA-155 inhibitor to macrophages. Nanomedicine: Nanotechnology, Biology, and Medicine 10, 1517–1527.Google Scholar
Moore, C, Kosgodage, U, Lange, S and Inal, JM (2017) The emerging role of exosome and microvesicle–(EMV-) based cancer therapeutics and immunotherapy. International Journal of Cancer 141, 428–436.Google Scholar
Morishita, M, Takahashi, Y, Matsumoto, A, Nishikawa, M and Takakura, Y (2016) Exosome-based tumor antigens-adjuvant co-delivery utilizing genetically engineered tumor cell-derived exosomes with immunostimulatory CpG DNA. Biomaterials 111, 55–65.Google Scholar
Morse, D, Daoust, P and Benribaque, S (2016) A transcriptome-based perspective of cell cycle regulation in dinoflagellates. Protist 167, 610–621.Google Scholar
Nantakomol, D, Dondorp, AM, Krudsood, S, Udomsanqpetch, R, Pattanapanyasat, K, Combes, V, Grau, GE, White, NJ, Viriyavejakul, P, Day, NP and Chotivanich, K (2011) Circulating red cell–derived microparticles in human malaria. The Journal of Infectious Diseases 203, 700–706.Google Scholar
Neves, RFC, Fernandes, ACS, Meyer-Fernandes, JR and Souto-Padrón, T (2014) Trypanosoma cruzi -secreted vesicles have acid and alkaline phosphatase activities capable of increasing parasite adhesion and infection. Parasitology Research 113, 2961–2972.Google Scholar
Nogueira, PM, Ribeiro, K, Silveira, AC, Campos, JH, Martins-Filho, OA, Bela, SR, Campos, MA, Pessoa, NL, Colli, W, Alves, MJ, Soares, RP and Torrecilhas, AC (2015) Vesicles from different Trypanosoma cruzi strains trigger differential innate and chronic immune responses. Journal of Extracellular Vesicles 4, 1–16.Google Scholar
Nten, CMA, Sommerer, N, Rofidal, V, Hirtz, C, Rossignol, M, Cuny, G, Peltier, J and Geiger, A (2010) Excreted/secreted proteins from Trypanosome procyclic strains. Journal of Biomedicine and Biotechnology 2010. doi: 10.1155/2010/212817Google Scholar
Olmos-Ortiz, LM, Barajas-Mendiola, MA, Barrios-Rodiles, M, Castellano, LE, Arias-Negrete, S, Avila, EE and Cuéllar-Mata, P (2017) Trichomonas vaginalis exosome-like vesicles modify the cytokine profile and reduce inflammation in parasite-infected mice. Parasite Immunology 39. doi: 10.1111/pim.12426.Google Scholar
Pisitkun, T, Shen, R and Knepper, MA (2004) Identification and proteomic profiling of exosomes in human urine. Proceedings of the National Academy of Sciences 101, 13368–13373.Google Scholar
Pope, SM and Lässer, C (2013) 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. Journal of Extracellular vesicles 2, 22484.Google Scholar
Ramirez, MI, Deolindo, P, de Messias-Reason, IJ, Arigi, EA, Choi, H, Almeida, IC and Evans-Osses, I (2017) Dynamic flux of microvesicles modulate parasite–host cell interaction of Trypanosoma cruzi in eukaryotic cells. Cellular Microbiology 19, 1–15.Google Scholar
Rastrojo, A, Carrasco-Ramiro, F, Martín, D, Crespillo, A, Reguera, RM, Aguado, B and Requena, JM (2013) The transcriptome of Leishmania major in the axenic promastigote stage: transcript annotation and relative expression levels by RNA-seq. BMC Genomics 14, 223.Google Scholar
Regev-Rudzki, N, Wilson, DW, Carvalho, TG, Sisquella, X, Coleman, BM, Rug, M, Bursac, D, Angrisano, F, Gee, M, Hill, AF, Bum, J and Cowman, AF (2013) Cell-Cell communication between malaria-infected red blood cells via exosome-like vesicles. Cell 153, 1120–1133.Google Scholar
Revenfeld, AL, Baek, R, Nielsen, HM, Stenballe, A, Varming, K and Jorgensen, M (2014) Diagnostic and prognostic potential of extracellular vesicles in peripheral blood. Clinical Therapeutics 36, 830–846.Google Scholar
Sánchez-Ovejero, C, Benito-Lopez, F, Díez, P, Casulli, A, Siles-Lucas, M, Fuentes, M and Manzano-Román, R (2016) Sensing parasites: proteomic and advanced bio-detection alternatives. Journal of Proteomics 136, 145–156.Google Scholar
Santiago-Dieppa, DR, Steinberg, J, Gonda, D, Cheung, VJ, Carter, BS and Chen, CC (2014) Extracellular vesicles as a platform for “liquid biopsy” in glioblastoma patients. Expert Review of Molecular Diagnostics 14, 819–825.Google Scholar
Schnitzer, JK, Berzel, S, Fajardo-Moser, M, Remer, KA and Moll, H (2010) Fragments of antigen-loaded dendritic cells (DC) and DC-derived exosomes induce protective immunity against Leishmania major. Vaccine 28, 5785–5793.Google Scholar
Schorey, JS, Cheng, Y, Singh, PP and Smith, VL (2015) Exosomes and other extracellular vesicles in host-pathogen interactions. EMBO Reports 16, 24–43.Google Scholar
Silva, AK, Luciani, N, Gazeau, F, Aubertin, K, Bonneau, S, Chauvierre, C, Letourneur, D and Wilhelm, C (2015) Combining magnetic nanoparticles with cell derived microvesicles for drug loading and targeting. Nanomedicine: Nanotechnology, Biology, and Medicine 11, 645–655.Google Scholar
Silva, AM, Teixeira, JH, Almeida, MI, Gonçalves, RM, Barbosa, MA and Santos, SG (2017) Extracellular vesicles: immunomodulatory messengers in the context of tissue repair/regeneration. European Journal of Pharmaceutical Sciences 98, 86–95.Google Scholar
Silveira, JFDA, Abrahamsohn, PA and Colli, W (1979) Plasma membrane vesicles isolated from epimastigote forms of Trypanosoma cruzi. Biochimica et Biophysica Acta 550, 222–232.Google Scholar
Silverman, JM, Chan, SK, Robinson, DP, Dwyer, D, Nandan, D, Foster, LJ and Reiner, NE (2008) Proteomic analysis of the secretome of Leishmania donovani. Genome Biology 9, 1–21.Google Scholar
Silverman, JM, Clos, J, de´Oliveira, CC, Shirvani, O, Fang, Y, Wang, C, Foster, LJ and Reiner, NE (2010) An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages. Journal of Cell Science 123, 842–852.Google Scholar
Stensvold, CR, Lebbad, M and Verweij, JJ (2011) The impact of genetic diversity in protozoa on molecular diagnostics. Trends in Parasitology 27, 53–58.Google Scholar
Stratton, D, Moore, C, Antwi-Baffour, S, Lange, S and Inal, J (2015) Microvesicles released constitutively from prostate cancer cells differ biochemically and functionally to stimulated microvesicles released through sublytic C5b-9. Biochemical and Biophysical Research Communications 460, 589–595.Google Scholar
Szempruch, AJ, Sykes, SE, Kief, R, Denison, L, Becker, AC, Gartrell, A, Martin, WJ, Nakayasu, ES, Aldeida, IC, Hajduk, SL and Harrington, JM (2016) Extracellular vesicles from Trypanosoma brucei mediate virulence factor transfer and cause host anemia. Cell 164, 246–257.Google Scholar
Trelis, M, Galiano, A, Bolado, A, Toledo, R, Marcilla, A and Bernal, D (2016) Subcutaneous injection of exosomes reduces symptom severity and mortality induced by Echinostoma caproni infection in BALB/c mice. International Journal for Parasitology 46, 799–808.Google Scholar
Trocoli Torrecilhas, AC, Tonelli, RR, Pavanelli, WR, da Silva, JS, Schumacher, RI, de Souza, W, E Silva, NC, de Aldeida Abrahamsihn, I, Colli, W and Manso Alves, MJ (2009) Trypanosoma cruzi: parasite shed vesicles increase heart parasitism and generate an intense inflammatory response. Microbes And Infection 11, 29–39.Google Scholar
Twu, O, de Miguel, N, Lustig, G, Stevens, GC, Vashisht, AA, Wohlschlegel, JA and Johnson, PJ (2013) Trichomonas vaginalis exosomes deliver cargo to host cells and mediate host:parasite interactions. PLoS Pathogens 9. doi: 10.1371/journal.ppat.1003482Google Scholar
Weigelt, J (2010) Structural genomics - Impact on biomedicine and drug discovery. Experimental Cell Research 316, 1332–1338.Google Scholar
Wekesa, AL, Cross, KS, O´Donovan, O, Dowdall, JF, O´Brien, O, Doyle, M, Byrne, L, Phelan, JP, Ross, MD, Landers, R and Harrison, M (2014) Predicting carotid artery disease and plaque instability from cell-derived microparticles. European Journal of vascular and endovascular Surgery 48, 489–495.Google Scholar
World Health Organization (2002) Control of Chagas Disease: Second Report of the WHO Expert Committee. Geneva, WHO Technical Report Series, No. 905.Google Scholar
WHO–World Health Organization (2016). World Malaria Report 2016.Google Scholar
Wowk, PF, Zardo, ML, Miot, HT, Goldenberg, S, Carvalho, PC and Mörking, PA (2017) Proteomic profiling of extracellular vesicles secreted from Toxoplasma gondii. Proteomics 17, 15–16.Google Scholar
Wyllie, MP and Ramirez, MI (2017) Microvesicles released during the interaction between Trypanosoma cruzi TcI and TcII strains and host blood cells inhibit complement system and increase the infectivity of metacyclic forms of host cells in a strain-independent process. Pathogens and Disease 75, 1–10.Google Scholar
Zhang, X, Yuan, X, Shi, H, Wu, L, Qian, H and Xu, W (2015) Exosomes in cancer: small particle, big player. Journal of Hematology & Oncology 8, 83.Google Scholar
Zhou, Y, Xu, H, Xu, W, Wang, B, Wu, H, Tao, Y, Zhang, B, Wang, M, Mao, F, Yan, Y, Gao, S, Gu, H, Zhu, W and Qian, H (2013) Exosomes released by human umbilical cord mesenchymal stem cells protect against cisplatin-induced renal oxidative stress and apoptosis in vivo and in vitro. Stem Cell Research & Theraphy 4, 34.Google Scholar
Zingales, B (2017) Trypanosoma cruzi genetic diversity: something new for something known about chagas disease manifestations, serodiagnosis and drug sensitivity. Acta Tropica xx, xxxx-xxxx, https://doi.org/10.1016/j.Google Scholar
Zitvogel, L, Regnault, A, Lozier, A, Wolfers, J, Flament, C, Tenza, D, Ricciardi-Castagnoli, P, Raposo, G and Amigorena, S (1998) Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nature Medicine 4, 594–600.Google Scholar