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Review

Extracellular vesicles from parasitic helminths and their potential utility as vaccines

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Pages 197-205 | Received 30 Nov 2017, Accepted 18 Jan 2018, Published online: 30 Jan 2018

References

  • WHO/Regional Office for the Western Pacific. Food-borne trematode infections in Asia: report. Manila, Philippines: World Health Organization, Regional Office for the Western Pacific; 2004.
  • Mathers C, Fat DM, Boerma JT, World Health Organization. The global burden of disease: 2004 update. Geneva: World Health Organization; 2008.
  • Bethony J, Brooker S, Albonico M, et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006;367(9521):1521–1532.
  • Hotez PJ, Brindley PJ, Bethony JM, et al. Helminth infections: the great neglected tropical diseases. J Clin Investig. 2008;118(4):1311–1321.
  • Maizels RM, Holland MF, Falcone FH, et al. Vaccination against helminth parasites-the ultimate challenge for vaccinologists? Immunol Rev. 1999;171:125–147.
  • Toledo R, Bernal MD, Marcilla A. Proteomics of foodborne trematodes. J Proteomics. 2011;74(9):1485–1503.
  • Sotillo J, Toledo R, Mulvenna J, et al. Exploiting helminth-host interactomes through big data. Trends Parasitol. 2017;33(11):875–888.
  • Mulvenna J, Sripa B, Brindley PJ, et al. The secreted and surface proteomes of the adult stage of the carcinogenic human liver fluke Opisthorchis viverrini. Proteomics. 2010;10(5):1063–1078.
  • Sotillo J, Pearson M, Becker L, et al. A quantitative proteomic analysis of the tegumental proteins from Schistosoma mansoni schistosomula reveals novel potential therapeutic targets. Int J Parasitol. 2015;45(8):505–516.
  • Cancela M, Acosta D, Rinaldi G, et al. A distinctive repertoire of cathepsins is expressed by juvenile invasive Fasciola hepatica. Biochimie. 2008;90(10):1461–1475.
  • Crowe J, Lumb FE, Harnett MM, et al. Parasite excretory-secretory products and their effects on metabolic syndrome. Parasite Immunol. 2017;39(5):e12410-n/a.
  • Marcilla A, Trelis M, Cortés A, et al. Extracellular vesicles from parasitic helminths contain specific excretory/secretory proteins and are internalized in intestinal host cells. PLoS One. 2012;7(9):e45974.
  • Marcilla A, Martin-Jaular L, Trelis M, et al. Extracellular vesicles in parasitic diseases. J Extracell Vesicles. 2014;3:25040.
  • Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013;200(4):373–383.
  • Evans-Osses I, Reichembach LH, Ramirez MI. Exosomes or microvesicles? Two kinds of extracellular vesicles with different routes to modify protozoan-host cell interaction. Parasitol Res. 2015;114(10):3567–3575.
  • Akers JC, Gonda D, Kim R, et al. Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies. J Neurooncol. 2013;113(1):1–11.
  • Edgar JR. Q&A: what are exosomes, exactly? BMC Biol. 2016;14(1):46.
  • Yáñez-Mó M, Pia RMS, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015;4(Generic):1–60.
  • Falker C, Hartmann A, Guett I, et al. Exosomal cellular prion protein drives fibrillization of amyloid beta and counteracts amyloid beta-mediated neurotoxicity. J Neurochem. 2016;137(1):88–100.
  • Al-Nedawi K, May L, Meehan B, et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol. 2008;10(5):619–624.
  • Sellam J, Proulle V, Jüngel A, et al. Increased levels of circulating microparticles in primary Sjögren’s syndrome, systemic lupus erythematosus and rheumatoid arthritis and relation with disease activity. Arthritis Res Ther. 2009;11(5):R156–R156.
  • Esteva-Font C, Wang X, Ars E, et al. Are sodium transporters in urinary exosomes reliable markers of tubular sodium reabsorption in hypertensive patients? Nephron Physiol. 2010;114(3):p25–p34.
  • Berckmans RJ, Sturk A, Tienen VLM, et al. Cell-derived vesicles exposing coagulant tissue factor in saliva. Blood. 2011;117(11):3172–3180.
  • Aline F, Bout D, Amigorena S, et al. Toxoplasma gondii antigen-pulsed-dendritic cell-derived exosomes induce a protective immune response against T. gondii infection. Infect Immun. 2004;72(7):4127–4137.
  • Coakley G, McCaskill JL, Borger JG, et al. Extracellular vesicles from a helminth parasite suppress macrophage activation and constitute an effective vaccine for protective immunity. Cell Rep. 2017;19(8):1545–1557.
  • Coakley G, Maizels RM, Buck AH. Exosomes and other extracellular vesicles: the new communicators in parasite infections. Trends Parasitol. 2015;31(10):477–489.
  • Montaner S, Galiano A, Trelis M, et al. The role of extracellular vesicles in modulating the host immune response during parasitic infections. Front Immunol. 2014;5:433.
  • Bernal D, Trelis M, Montaner S, et al. Surface analysis of Dicrocoelium dendriticum. The molecular characterization of exosomes reveals the presence of miRNAs. J Proteomics. 2014;105:232.
  • Nowacki FC, Swain MT, Klychnikov OI, et al. Protein and small non-coding RNA-enriched extracellular vesicles are released by the pathogenic blood fluke Schistosoma mansoni. J Extracell Vesicles. 2015;4(1):1–16.
  • Buck AH, Coakley G, Simbari F, et al. Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nat Commun. 2014;5:5488.
  • Zamanian M, Fraser LM, Agbedanu PN, et al. Release of small RNA-containing exosome-like vesicles from the human filarial parasite Brugia malayi: e0004069. PLoS Negl Trop Dis. 2015;9(9):e0004069.
  • Fromm B, Trelis M, Hackenberg M, et al. The revised microRNA complement of Fasciola hepatica reveals a plethora of overlooked microRNAs and evidence for enrichment of immuno-regulatory microRNAs in extracellular vesicles. Int J Parasitol. 2015;45(11):697–702.
  • Sotillo J, Pearson M, Potriquet J, et al. Extracellular vesicles secreted by Schistosoma mansoni contain protein vaccine candidates. Int J Parasitol. 2016;46(1):1–5.
  • Zhu L, Liu J, Dao J, et al. Molecular characterization of S. japonicum exosome-like vesicles reveals their regulatory roles in parasite-host interactions. Sci Rep. 2016;6:25885.
  • Zhu S, Wang S, Lin Y, et al. Release of extracellular vesicles containing small RNAs from the eggs of Schistosoma japonicum. Parasites Vectors. 2016;9(1):574.
  • Chaiyadet S, Sotillo J, Smout M, et al. Carcinogenic liver fluke secretes extracellular vesicles that promote cholangiocytes to adopt a tumorigenic phenotype. J Infect Dis. 2015;212(10):1636–1645.
  • Cwiklinski K, de la Torre-Escudero E, Trelis M, et al. The extracellular vesicles of the helminth pathogen, Fasciola hepatica: biogenesis pathways and cargo molecules involved in parasite pathogenesis. Mol Cell Proteomics. 2015;14(12):3258–3273.
  • Ancarola ME, Marcilla A, Herz M, et al. Cestode parasites release extracellular vesicles with microRNAs and immunodiagnostic protein cargo. Int J Parasitol. 2017;47(10–11):675–686.
  • Greening DW, Xu R, Ji H, et al. A protocol for exosome isolation and characterization: evaluation of ultracentrifugation, density-gradient separation, and immunoaffinity capture methods. Methods Mol Biol. 2015;1295:179–209.
  • Livshits MA, Livshts MA, Khomyakova E, et al. Isolation of exosomes by differential centrifugation: theoretical analysis of a commonly used protocol. Sci Rep. 2015;5:17319.
  • Momen-Heravi F, Balaj L, Alian S, et al. Current methods for the isolation of extracellular vesicles. Biol Chem. 2013;394(10):1253.
  • Webber J, Clayton A. How pure are your vesicles? J Extracell Vesicles. 2013;2:1–6.
  • Taylor DD, Shah S. Methods of isolating extracellular vesicles impact down-stream analyses of their cargoes. Methods. 2015;87:3–10.
  • Théry C, Amigorena S, Raposo G, et al. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Current Protocol Biology. 2006. Chapter 3, Unit 3.22. Wiley.
  • Abels ER, Breakefield XO. Introduction to extracellular vesicles: biogenesis, RNA cargo selection, content, release, and uptake. Cell Mol Neurobiol. 2016;36(3):301–312.
  • Cheng G, Luo R, Hu C, et al. Deep sequencing-based identification of pathogen-specific microRNAs in the plasma of rabbits infected with Schistosoma japonicum. Parasitology. 2013;140(14):1751.
  • Hoy AM, Lundie RJ, Ivens A, et al. Parasite-derived microRNAs in host serum as novel biomarkers of helminth infection. PLoS Negl Trop Dis. 2014;8(2):e2701.
  • Meningher T, Lerman G, Regev-Rudzki N, et al. Schistosomal microRNAs isolated from extracellular vesicles in sera of infected patients: a new tool for diagnosis and follow-up of human schistosomiasis. J Infect Dis. 2017;215(3):378–386.
  • Banerjee S, Xie N, Cui H, et al. MicroRNA let-7c regulates macrophage polarization. J Immunol. 2013;190(12):6542–6549.
  • Don TA, Bethony JM, Loukas A. Saposin-like proteins are expressed in the gastrodermis of Schistosoma mansoni and are immunogenic in natural infections. Int J Infect Dis. 2008;12(6):e39–e47.
  • Robinson MW, Corvo I, Jones PM, et al. Collagenolytic activities of the major secreted cathepsin L peptidases involved in the virulence of the helminth pathogen Fasciola hepatica. PLoS Negl Trop Dis. 2011;5(4):e1012.
  • Donnelly S, O’Neill SM, Sekiya M, et al. Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages. Infect Immun. 2005;73(1):166–173.
  • Lgg P, Fonseca CT, Chiari L, et al. Immunization with Schistosoma mansoni 22.6 kDa antigen induces partial protection against experimental infection in a recombinant protein form but not as DNA vaccine. Immunobiology. 2006;211(1):97–104.
  • Han Y, Zhao B, Zhang M, et al. Biochemical properties and vaccine effect of recombinant TPx-3 from Schistosoma japonicum. Parasitol Res. 2017;116(4):1361–1372.
  • Figueiredo BC, Assis NRG, Morais SB, et al. Schistosome syntenin partially protects vaccinated mice against Schistosoma mansoni infection. PLoS Negl Trop Dis. 2014;8(8):e3107.
  • Diniz PP, Nakajima E, Miyasato PA, et al. Two SmDLC antigens as potential vaccines against schistosomiasis. Acta Trop. 2014;140:193–201.
  • Romeih MH, Hassan HM, Shousha TSA, et al. Immunization against Egyptian Schistosoma mansoni infection by multivalent DNA vaccine. Acta Biochim Biophys Sin (Shanghai). 2008;40(4):327–338.
  • Duan MM, Xu RM, Yuan CX, et al. SjHSP70, a recombinant Schistosoma japonicum heat shock protein 70, is immunostimulatory and induces protective immunity against cercarial challenge in mice. Parasitol Res. 2015;114(9):3415–3429.
  • Schechtman D, Tarrab‐Hazdai R, Arnon R. The 14-3-3 protein as a vaccine candidate against schistosomiasis. Parasite Immunol. 2001;23(4):213–217.
  • Zafra R, Pérez-Écija RA, Buffoni L, et al. Early and late peritoneal and hepatic changes in goats immunized with recombinant cathepsin L1 and infected with Fasciola hepatica. J Comp Pathol. 2013;148(4):373–384.
  • Chen N, Yuan Z-G, Xu M-J, et al. Ascaris suum enolase is a potential vaccine candidate against ascariasis. Vaccine. 2012;30(23):3478–3482.
  • Han K, Xu LF, Yan R, et al. Vaccination of goats with glyceraldehyde-3-phosphate dehydrogenase DNA vaccine induced partial protection against Haemonchus contortus. Vet Immunol Immunopathol. 2012;149(3–4):177–185.
  • Levy S, Shoham T. The tetraspanin web modulates immune-signalling complexes. Nat Rev Immunol. 2005;5(2):136–148.
  • Hemler ME. Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define anovel type of membrane microdomain. Annu Rev Cell Dev Biol. 2003;19(1):397–422.
  • Piratae S, Tesana S, Jones MK, et al. Molecular characterization of a tetraspanin from the human liver fluke opisthorchis viverrini. PLoS Negl Trop Dis. 2012;6(12):e1939.
  • Tran MH, Freitas TC, Cooper L, et al. Suppression of mRNAs encoding tegument tetraspanins from Schistosoma mansoni results in impaired tegument turnover. PLoS Pathog. 2010;6(4):e1000840.
  • Tran MH, Pearson MS, Bethony JM, et al. Tetraspanins on the surface of Schistosoma mansoni are protective antigens against schistosomiasis. Nat Med. 2006;12(7):835–840.
  • ClinicalTrials.gov. A phase I study of the safety, reactogenicity, and immunogenicity of Sm-TSP-2/alhydrogel® with or without GLA-AF for intestinal schistosomiasis in healthy adults. Available from: https://clinicaltrials.gov/ct2/show/NCT02337855
  • Dai Y, Zhu Y, Harn DA, et al. DNA vaccination by electroporation and boosting with recombinant proteins enhances the efficacy of DNA vaccines for Schistosomiasis japonica. Clin Vaccine Immunol. 2009;16(12):1796–1803.
  • Zhu L, Liu H-F, Lu M-B, et al. Construction, purification, and evaluation of multivalent DNA vaccine against Schistosoma japonicum. Parasitol Res. 2011;108(1):115–121.
  • Zhu Z, Fu Z, Zhang M, et al. Protective efficacy evaluation induced by recombinant protein LHD-Sj23-GST of Schistosoma japonicum emulsified with three different adjuvants: protective efficacy evaluation induced by recombinant protein LHD-Sj23-GST of S. japonicum. Parasite Immunol. 2012;34(6):341–344.
  • Yuan W, Qi X, Tsang P, et al. Saposin B is the dominant saposin that facilitates lipid binding to human CD1d molecules. Proc Natl Acad Sci U S A. 2007;104(13):5551–5556.
  • Espino AM, Hillyer GV. A novel Fasciola hepatica saposinlike recombinant protein with immunoprophylactic potential. J Parasitol. 2004;90(4):876–879.
  • Cardoso FC, Pacifico RNA, Mortara RA, et al. Human antibody responses of patients living in endemic areas for schistosomiasis to the tegumental protein Sm29 identified through genomic studies. Clin Exp Immunol. 2006;144(3):382–391.
  • de Assis NRG, de Morais SB, Figueiredo BCP, et al. DNA vaccine encoding the chimeric form of Schistosoma mansoni Sm-TSP2 and Sm29 confers partial protection against challenge infection. PLoS One. 2015;10(5):e0125075.
  • Cardoso FC, Macedo GC, Gava E, et al. Schistosoma mansoni tegument protein Sm29 is able to induce a Th1-type of immune response and protection against parasite infection. Plos Neglected Trop Dis. 2008;2(10):e308.
  • Ewaisha RE, Bahey-El-Din M, Mossallam SF, et al. Combination of the two schistosomal antigens Sm14 and Sm29 elicits significant protection against experimental Schistosoma mansoni infection. Exp Parasitol. 2014;145(1):51–60.
  • Pinheiro CS, Ribeiro APD, Cardoso FC, et al. A multivalent chimeric vaccine composed of Schistosoma mansoni SmTSP-2 and Sm29 was able to induce protection against infection in mice. Parasite Immunol. 2014;36(7):303–312.
  • McManus DP, Loukas A. Current status of vaccines for schistosomiasis. Clin Microbiol Rev. 2008;21(1):225–242.
  • Le L, Zhang W, Karmakar S, et al. Simultaneous priming with DNA encoding Sm-p80 and boosting with Sm-p80 protein confers protection against challenge infection with Schistosoma mansoni in mice. Parasitol Res. 2014;113(3):1195–1200.
  • Ahmad G, Zhang W, Torben W, et al. Protective effects of Sm-p80 in the presence of resiquimod as an adjuvant against challenge infection with Schistosoma mansoni in mice. Int J Infect Dis. 2010;14(9):e781–e787.
  • Ahmad G, Zhang W, Torben W, et al. Prime-boost and recombinant protein vaccination strategies using Sm-p80 protects against Schistosoma mansoni infection in the mouse model to levels previously attainable only by the irradiated cercarial vaccine. Parasitol Res. 2009;105(6):1767–1777.
  • Karmakar S, Zhang W, Ahmad G, et al. Cross-species protection: Schistosoma mansoni Sm-p80 vaccine confers protection against Schistosoma haematobium in hamsters and baboons. Vaccine. 2014;32(11):1296.
  • Chen HG, Nara T, Zeng XJ, et al. Vaccination of domestic pig with recombinant paramyosin against Schistosoma japonicum in China. Vaccine. 2000;18(20):2142–2146.
  • Ramirez BL, Kurtis JD, Wiest PM, et al. Paramyosin: a candidate vaccine antigen against Schistosoma japonicum. Parasite Immunol. 1996;18(1):49–52.
  • Matsui M, Fowler JH, Walling LL. Leucine aminopeptidases: diversity in structure and function. Biol Chem. 2006;387(12):1535.
  • Maggioli G, Acosta D, Silveira F, et al. The recombinant gut-associated M17 leucine aminopeptidase in combination with different adjuvants confers a high level of protection against Fasciola hepatica infection in sheep. Vaccine. 2011;29(48):9057.
  • Piacenza L, Acosta D, Basmadjian I, et al. Vaccination with cathepsin L proteinases and with leucine aminopeptidase induces high levels of protection against fascioliasis in sheep. Infect Immun. 1999;67(4):1954–1961.
  • Dalton JP, McGonigle S, Rolph TP, et al. Induction of protective immunity in cattle against infection with Fasciola hepatica by vaccination with cathepsin L proteinases and with hemoglobin. Infect Immun. 1996;64(12):5066–5074.
  • Golden O, Flynn RJ, Read C, et al. Protection of cattle against a natural infection of Fasciola hepatica by vaccination with recombinant cathepsin L1 (rFhCL1). Vaccine. 2010;28(34):5551–5557.
  • Ricciardi A, Dalton JP, Ndao M. Evaluation of the immune response and protective efficacy of Schistosoma mansoni Cathepsin B in mice using CpG dinucleotides as adjuvant. Vaccine. 2015;33(2):346–353.
  • Nebert DW, Vasiliou V. Analysis of the glutathione S-transferase (GST) gene family. Hum Genomics. 2004;1(6):460–464.
  • Xu C-B, Xu CB, Verwaerde C, et al. A monoclonal antibody blocking the Schistosoma mansoni 28-kDa glutathione S-transferase activity reduces female worm fecundity and egg viability. Eur J Immunol. 1991;21(8):1801–1807.
  • ClinicalTrials.gov. Efficacy of vaccine Sh28GST in association with praziquantel (PZQ) for prevention of clinical recurrences of Schistosoma haematobium pathology (Bilhvax). Available from: https://clinicaltrials.gov/ct2/show/NCT00870649.
  • Wei F, Liu Q, Gao S, et al. Enhancement by IL-18 of the protective effect of a Schistosoma japonicum 26 kDa GST plasmid DNA vaccine in mice. Vaccine. 2008;26(33):4145–4149.
  • Morrison CA, Colin T, Sexton JL, et al. Protection of cattle against Fasciola hepatica infection by vaccination with glutathione S-transferase. Vaccine. 1996;14(17):1603–1612.
  • Boulanger D, Reid GDF, Sturrock RF, et al. Immunization of mice and baboons with the recombinant Sm28GST affects both worm viability and fecundity after experimental infection with Schistosoma mansoni. Parasite Immunol. 1991;13(5):473–490.
  • Capron M, Capron A, Riveau G, et al. Schistosomes: the road from host–parasite interactions to vaccines in clinical trials. Trends Parasitol. 2005;21(3):143–149.
  • Riveau G, Deplanque D, Remoué F, et al. Safety and immunogenicity of rSh28GST antigen in humans: phase 1 randomized clinical study of a vaccine candidate against urinary schistosomiasis. PLoS Negl Trop Dis. 2012;6(7):e1704.
  • Bourke CD, Nausch N, Rujeni N, et al. Cytokine responses to the anti-schistosome vaccine candidate antigen glutathione-S-transferase vary with host age and are boosted by praziquantel treatment. PLoS Negl Trop Dis. 2014;8(5):e2846.
  • Spithill TW, Sexton PMS,JL, Bozas E, et al. The development of vaccines against fasciolosis. In: Dalton JP, editor. Fasciolosis. Oxon: CABI Publishing; 1999. p. 377–410.
  • Tendler M, Simpson AJG. The biotechnology-value chain: development of Sm14 as a schistosomiasis vaccine. Acta Trop. 2008;108(2):263–266.
  • Hillyer GV, Haroun ETM, Hernandez A, et al. Acquired resistance to Fasciola hepatica in cattle using a purified adult worm antigen. Am J Trop Med Hyg. 1987;37(2):363–369.
  • Liu JM, Cai XZ, Lin JJ, et al. Gene cloning, expression and vaccine testing of Schistosoma japonicum SjFABP. Parasite Immunol. 2004;26(89):351–358.
  • Tendler M, Brito CA, Vilar MM, et al. A Schistosoma mansoni fatty acid-binding protein, Sm14, is the potential basis of a dual-purpose anti-helminth vaccine. Proc Natl Acad Sci U S A. 1996;93(1):269–273.
  • Martínez-Fernández AR, Nogal-Ruiz JJ, López-Abán J, et al. Vaccination of mice and sheep with Fh12 FABP from Fasciola hepatica using the new adjuvant/immunomodulator system ADAD. Vet Parasitol. 2004;126(3):287–298.
  • López-Abán J, Casanueva P, Nogal J, et al. Progress in the development of Fasciola hepatica vaccine using recombinant fatty acid binding protein with the adjuvant adaptation system ADAD. Vet Parasitol. 2007;145(3):287–296.
  • Wei F, Liu Q, Liu W, et al. IL-18 enhances protective effect in mice immunized with a Schistosoma japonicum FABP DNA vaccine. Acta Trop. 2009;111(3):284–288.
  • Trelis M, Galiano A, Bolado A, et al. Subcutaneous injection of exosomes reduces symptom severity and mortality induced by Echinostoma caproni infection in BALB/c mice. Int J Parasitol. 2016;46(12):799–808.
  • Palevich N, Britton C, Kamenetzky L, et al. Tackling hypotheticals in helminth genomes. Trends Parasitol. 2017;1471-4922(17):30281–30287.
  • Egesa M, Hoffmann KF, Hokke CH, et al. Rethinking schistosomiasis vaccine development: synthetic vesicles. Trends Parasitol. 2017;33(12):918–921.

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