Extracellular vesicles and vesicle-free secretome of the protozoa Acanthamoeba castellanii under homeostasis and nutritional stress and their damaging potential to host cells

References

• Magnet A, et al. Molecular characterization of Acanthamoeba isolated in water treatment plants and comparison with clinical isolates. Parasitol Res. 2012;111:383–392.
   PubMed Web of Science ®Google Scholar
• Gianinazzi C, et al. Screening Swiss water bodies for potentially pathogenic free-living amoebae. Res Microbiol. 2009;160:367–374.
   PubMed Web of Science ®Google Scholar
• Tan SK, et al. Fatal acanthamoeba encephalitis in a patient with a total artificial heart (syncardia) device. Open Forum Infect Dis. 2014;1:ofu057.
   PubMedGoogle Scholar
• Rodriguez-Zaragoza S. Ecology of free-living amoebae. Crit Rev Microbiol. 1994;20:225–241.
   PubMed Web of Science ®Google Scholar
• Booton GC, et al. Molecular and physiological evaluation of subtropical environmental isolates of Acanthamoeba spp., causal agent of Acanthamoeba keratitis. J Eukaryot Microbiol. 2004;51:192–200.
   PubMed Web of Science ®Google Scholar
• Khan NA. Acanthamoeba: biology and increasing importance in human health. FEMS Microbiol Rev. 2006;30:564–595.
   PubMed Web of Science ®Google Scholar
• Huang FC, et al. Characterizing clinical isolates of Acanthamoeba castellanii with high resistance to polyhexamethylene biguanide in Taiwan. J Microbiol Immunol Infect. 2015.
   Google Scholar
• Huang SW, et al. Isolation and identification of Legionella and their host amoebae from weak alkaline carbonate spring water using a culture method combined with PCR. Parasitol Res. 2011;109:1233–1241.
   PubMed Web of Science ®Google Scholar
• Marciano-Cabral F, Han K, Powell E, et al. Interaction of an Acanthamoeba human isolate harboring bacteria with murine peritoneal macrophages. J Eukaryot Microbiol. 2003;50 Suppl:516–519.
   PubMed Web of Science ®Google Scholar
• Marciano-Cabral F, Cabral G. Acanthamoeba spp. as agents of disease in humans. Clin Microbiol Rev. 2003;16:273–307.
   PubMed Web of Science ®Google Scholar
• Martinez AJ, Visvesvara GS. Free-living, amphizoic and opportunistic amebas. Brain Pathol. 1997;7:583–598.
   PubMed Web of Science ®Google Scholar
• Siddiqui R, Aqeel Y, Khan NA. The development of drugs against Acanthamoeba infections. Antimicrob Agents Chemother. 2016.
   Web of Science ®Google Scholar
• Lorenzo-Morales J, Khan NA, Walochnik J. An update on Acanthamoeba keratitis: diagnosis, pathogenesis and treatment. Parasite. 2015;22:10.
   PubMed Web of Science ®Google Scholar
• Lorenzo-Morales J, et al. Acanthamoeba keratitis: an emerging disease gathering importance worldwide? Trends Parasitol. 2013;29:181–187.
   PubMed Web of Science ®Google Scholar
• Wynter-Allison Z, et al. Acanthamoeba infection as a cause of severe keratitis in a soft contact lens wearer in Jamaica. Am J Trop Med Hyg. 2005;73:92–94.
   PubMed Web of Science ®Google Scholar
• Alsam S, Sissons J, Jayasekera S, et al. Extracellular proteases of Acanthamoeba castellanii (encephalitis isolate belonging to T1 genotype) contribute to increased permeability in an in vitro model of the human blood-brain barrier. J Infect. 2005;51:150–156.
   PubMed Web of Science ®Google Scholar
• Sant'ana VP, et al. Cytotoxic activity and degradation patterns of structural proteins by corneal isolates of Acanthamoeba spp. Graefes Arch Clin Exp Ophthalmol. 2015;253:65–75.
   PubMed Web of Science ®Google Scholar
• Hadas E, Mazur T. Biochemical markers of pathogenicity and virulence of Acanthamoeba sp. strains. Parasitol Res. 1993;79:696–698.
   PubMed Web of Science ®Google Scholar
• Choi DH, Na BK, Seo MS, et al. Purification and characterization of iron superoxide dismutase and copper-zinc superoxide dismutase from Acanthamoeba castellanii. J Parasitol. 2000;86:899–907.
   PubMed Web of Science ®Google Scholar
• Kim WT, et al. Comparison of specific activity and cytopathic effects of purified 33 kDa serine proteinase from Acanthamoeba strains with different degree of virulence. Korean J Parasitol. 2006;44:321–330.
   PubMedGoogle Scholar
• Ramirez-Rico G, Martinez-Castillo M, de la Garza M, et al. Acanthamoeba castellanii Proteases are Capable of Degrading Iron-Binding Proteins as a Possible Mechanism of Pathogenicity. J Eukaryot Microbiol. 2015;62:614–622.
   PubMed Web of Science ®Google Scholar
• Ferrante A, Bates EJ. Elastase in the pathogenic free-living amoebae Naegleria and Acanthamoeba spp. Infect Immun. 1988;56:3320–3321.
   PubMed Web of Science ®Google Scholar
• Hadas E, Mazur T. Proteolytic enzymes of pathogenic and non-pathogenic strains of Acanthamoeba spp. Trop Med Parasitol. 1993;44:197–200.
   PubMedGoogle Scholar
• Khan NA, Jarroll EL, Panjwani N, et al. Proteases as markers for differentiation of pathogenic and nonpathogenic species of Acanthamoeba. J Clin Microbiol. 2000;38:2858–2861.
   PubMed Web of Science ®Google Scholar
• Mitra MM, Alizadeh H, Gerard RD, et al. Characterization of a plasminogen activator produced by Acanthamoeba castellanii. Mol Biochem Parasitol. 1995;73:157–164.
   PubMed Web of Science ®Google Scholar
• Serrano-Luna Jde J, et al. Protease activities of Acanthamoeba polyphaga and Acanthamoeba castellanii. Can J Microbiol. 2006;52:16–23.
   PubMed Web of Science ®Google Scholar
• Joffe LS, Nimrichter L, Rodrigues ML, et al. Potential Roles of Fungal Extracellular Vesicles during Infection. mSphere. 2016;1.
   PubMed Web of Science ®Google Scholar
• Kalluri R. The biology and function of exosomes in cancer. J Clin Invest. 2016;126:1208–1215.
   PubMed Web of Science ®Google Scholar
• Schorey JS, Harding CV. Extracellular vesicles and infectious diseases: new complexity to an old story. J Clin Invest. 2016;126:1181–1189.
   PubMed Web of Science ®Google Scholar
• Turpin D, et al. Role of extracellular vesicles in autoimmune diseases. Autoimmun Rev. 2016;15:174–183.
   PubMed Web of Science ®Google Scholar
• Oliveira DL, et al. Extracellular vesicles from Cryptococcus neoformans modulate macrophage functions. Infect Immun. 2010;78:1601–1609.
   PubMed Web of Science ®Google Scholar
• Rodrigues ML, Godinho RM, Zamith-Miranda D, et al. Traveling into Outer Space: Unanswered Questions about Fungal Extracellular Vesicles. PLoS Pathog. 2015;11:e1005240.
   PubMed Web of Science ®Google Scholar
• Oliveira DL, et al. Biogenesis of extracellular vesicles in yeast: Many questions with few answers. Commun Integr Biol. 2010;3:533–535.
   PubMedGoogle Scholar
• Oliveira DL, et al. Characterization of yeast extracellular vesicles: evidence for the participation of different pathways of cellular traffic in vesicle biogenesis. PLoS One. 2010;5:e11113.
   PubMed Web of Science ®Google Scholar
• 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;114:3567–3575.
   PubMed Web of Science ®Google Scholar
• Rodrigues ML, et al. Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot Cell. 2008;7:58–67.
   PubMed Web of Science ®Google Scholar
• Vargas G, et al. Compositional and immunobiological analyses of extracellular vesicles released by Candida albicans. Cell Microbiol. 2015;17:389–407.
   PubMed Web of Science ®Google Scholar
• Rodrigues ML, et al. Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport. Eukaryot Cell. 2007;6:48–59.
   PubMed Web of Science ®Google Scholar
• Albuquerque PC, et al. Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes. Cell Microbiol. 2008;10:1695–1710.
   PubMed Web of Science ®Google Scholar
• Mugnier MR, Papavasiliou FN, Schulz D. Vesicles as Vehicles for Virulence. Trends Parasitol. 2016;32:435–436.
   PubMed Web of Science ®Google Scholar
• Marti M, Johnson PJ. Emerging roles for extracellular vesicles in parasitic infections. Curr Opin Microbiol. 2016;32:66–70.
   PubMed Web of Science ®Google Scholar
• Silverman JM, et al. An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages. J Cell Sci. 2010;123:842–852.
   PubMed Web of Science ®Google Scholar
• Silverman JM, et al. Leishmania exosomes modulate innate and adaptive immune responses through effects on monocytes and dendritic cells. J Immunol. 2010;185:5011–5022.
   PubMed Web of Science ®Google Scholar
• Geiger A, et al. Exocytosis and protein secretion in Trypanosoma. BMC Microbiol. 2010;10:20.
   PubMed Web of Science ®Google Scholar
• Szempruch AJ, et al. Extracellular Vesicles from Trypanosoma brucei Mediate Virulence Factor Transfer and Cause Host Anemia. Cell. 2016;164:246–257.
   PubMed Web of Science ®Google Scholar
• Cordero EM, et al. Proteomic analysis of detergent-solubilized membrane proteins from insect-developmental forms of Trypanosoma cruzi. J Proteome Res. 2009;8:3642–3652.
   PubMed Web of Science ®Google Scholar
• Sant'Anna C, et al. Subcellular proteomics of Trypanosoma cruzi reservosomes. Proteomics. 2009;9:1782–1794.
   PubMed Web of Science ®Google Scholar
• Marcilla A, et al. Extracellular vesicles from parasitic helminths contain specific excretory/secretory proteins and are internalized in intestinal host cells. PLoS One. 2012;7:e45974.
   PubMed Web of Science ®Google Scholar
• Buck AH, et al. Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nat Commun. 2014;5:5488.
   PubMed Web of Science ®Google Scholar
• Tzelos T, et al. A preliminary proteomic characterisation of extracellular vesicles released by the ovine parasitic nematode, Teladorsagia circumcincta. Vet Parasitol. 2016;221:84–92.
   PubMed Web of Science ®Google Scholar
• Bernal D, et al. Surface analysis of Dicrocoelium dendriticum. The molecular characterization of exosomes reveals the presence of miRNAs. J Proteomics. 2014;105:232–241.
   PubMed Web of Science ®Google Scholar
• Tatischeff I, et al. Dictyostelium extracellular vesicles containing hoechst 33342 transfer the dye into the nuclei of living cells: a fluorescence study. J Fluoresc. 2008;18:319–328.
   PubMed Web of Science ®Google Scholar
• Nosanchuk JD, Nimrichter L, Casadevall A, et al. A role for vesicular transport of macromolecules across cell walls in fungal pathogenesis. Commun Integr Biol. 2008;1:37–39.
   PubMedGoogle Scholar
• Casadevall A, Nosanchuk JD, Williamson P, et al. Vesicular transport across the fungal cell wall. Trends Microbiol. 2009;17:158–162.
   PubMed Web of Science ®Google Scholar
• Rodrigues ML, et al. Vesicular transport systems in fungi. Future Microbiol. 2011;6:1371–1381.
   PubMed Web of Science ®Google Scholar
• Simons M, Raposo G. Exosomes–vesicular carriers for intercellular communication. Curr Opin Cell Biol. 2009;21:575–581.
   PubMed Web of Science ®Google Scholar
• Record M, Carayon K, Poirot M, et al. Exosomes as new vesicular lipid transporters involved in cell-cell communication and various pathophysiologies. Biochim Biophys Acta. 2014;1841:108–120.
   PubMed Web of Science ®Google Scholar
• Rao MB, Tanksale AM, Ghatge MS, et al. Molecular and biotechnological aspects of microbial proteases. Microbiol Mol Biol Rev. 1998;62:597–635.
   PubMed Web of Science ®Google Scholar
• Diao J, et al. A single vesicle-vesicle fusion assay for in vitro studies of SNAREs and accessory proteins. Nat Protoc. 2012;7:921–934.
   PubMed Web of Science ®Google Scholar
• Nicola AM, Frases S, Casadevall A. Lipophilic dye staining of Cryptococcus neoformans extracellular vesicles and capsule. Eukaryot Cell. 2009;8:1373–1380.
   PubMed Web of Science ®Google Scholar
• Goncalves MF, et al. Trypanosoma cruzi: shedding of surface antigens as membrane vesicles. Exp Parasitol. 1991;72:43–53.
   PubMed Web of Science ®Google Scholar
• Chaiyadet S, et al. Excretory/secretory products of the carcinogenic liver fluke are endocytosed by human cholangiocytes and drive cell proliferation and IL6 production. Int J Parasitol. 2015;45:773–781.
   PubMed Web of Science ®Google Scholar
• Lane RE, Korbie D, Trau M, et al. Purification Protocols for Extracellular Vesicles. Methods Mol Biol. 2017;1660:111–130.
   PubMedGoogle Scholar
• Mateescu B, et al. Obstacles and opportunities in the functional analysis of extracellular vesicle RNA – an ISEV position paper. J Extracell Vesicles. 2017;6:1286095.
   PubMed Web of Science ®Google Scholar
• Momen-Heravi F, et al. Current methods for the isolation of extracellular vesicles. Biol Chem. 2013;394:1253–1262.
   PubMed Web of Science ®Google Scholar
• Stetefeld J, McKenna SA, Patel TR. Dynamic light scattering: a practical guide and applications in biomedical sciences. Biophys Rev. 2016;8:409–427.
   PubMedGoogle Scholar
• Frases S, Viana NB, Casadevall A. Biophysical methods for the study of microbial surfaces. Front Microbiol. 2011;2:207.
   PubMed Web of Science ®Google Scholar
• Alexander-Lindo RL, Morrison EY, Nair MG. Hypoglycaemic effect of stigmast-4-en-3-one and its corresponding alcohol from the bark of Anacardium occidentale (cashew). Phytother Res. 2004;18:403–407.
   PubMed Web of Science ®Google Scholar
• Raederstorff D, Rohmer M. Sterol biosynthesis de nova via cycloartenol by the soil amoeba Acanthamoeba polyphaga. Biochem J. 1985;231:609–615.
   PubMed Web of Science ®Google Scholar
• Jones AL, Hann AC, Harwood JL, et al. Temperature-induced membrane-lipid adaptation in Acanthamoeba castellanii. Biochem J. 1993;290(Pt 1):273–278.
   PubMed Web of Science ®Google Scholar
• Bayer-Santos E, et al. Proteomic analysis of Trypanosoma cruzi secretome: characterization of two populations of extracellular vesicles and soluble proteins. J Proteome Res. 2013;12:883–897.
   PubMed Web of Science ®Google Scholar
• Mantel PY, et al. Malaria-infected erythrocyte-derived microvesicles mediate cellular communication within the parasite population and with the host immune system. Cell Host Microbe. 2013;13:521–534.
   PubMed Web of Science ®Google Scholar
• Tatischeff I. Assets of the non-pathogenic microorganism Dictyostelium discoideum as a model for the study of eukaryotic extracellular vesicles. F1000Res. 2013;2:73.
   Google Scholar
• Loomis WF. Cell signaling during development of Dictyostelium. Dev Biol. 2014;391:1–16.
   PubMed Web of Science ®Google Scholar
• Du Q, Kawabe Y, Schilde C, et al. The Evolution of Aggregative Multicellularity and Cell-Cell Communication in the Dictyostelia. J Mol Biol. 2015;427:3722–3733.
   PubMed Web of Science ®Google Scholar
• Bouyer S, Rodier MH, Guillot A, et al. Acanthamoeba castellanii: proteins involved in actin dynamics, glycolysis, and proteolysis are regulated during encystation. Exp Parasitol. 2009;123:90–94.
   PubMed Web of Science ®Google Scholar
• Kucknoor AS, Mundodi V, Alderete JF. The proteins secreted by Trichomonas vaginalis and vaginal epithelial cell response to secreted and episomally expressed AP65. Cell Microbiol. 2007;9:2586–2597.
   PubMed Web of Science ®Google Scholar
• Ringqvist E, et al. Release of metabolic enzymes by Giardia in response to interaction with intestinal epithelial cells. Mol Biochem Parasitol. 2008;159:85–91.
   PubMed Web of Science ®Google Scholar
• Vincensini L, et al. Proteomic analysis identifies novel proteins of the Maurer's clefts, a secretory compartment delivering Plasmodium falciparum proteins to the surface of its host cell. Mol Cell Proteomics. 2005;4:582–593.
   PubMed Web of Science ®Google Scholar
• Lidell ME, Moncada DM, Chadee K, et al. Entamoeba histolytica cysteine proteases cleave the MUC2 mucin in its C-terminal domain and dissolve the protective colonic mucus gel. Proc Natl Acad Sci U S A. 2006;103:9298–9303.
   PubMed Web of Science ®Google Scholar
• Ocadiz R, et al. EhCP112 is an Entamoeba histolytica secreted cysteine protease that may be involved in the parasite-virulence. Cell Microbiol. 2005;7:221–232.
   PubMed Web of Science ®Google Scholar
• Mattana A, et al. ADP and other metabolites released from Acanthamoeba castellanii lead to human monocytic cell death through apoptosis and stimulate the secretion of proinflammatory cytokines. Infect Immun. 2002;70:4424–4432.
   PubMed Web of Science ®Google Scholar
• Dudley R, Alsam S, Khan NA. The role of proteases in the differentiation of Acanthamoeba castellanii. FEMS Microbiol Lett. 2008;286:9–15.
   PubMed Web of Science ®Google Scholar
• Huang JM, et al. Pathogenic Acanthamoeba castellanii Secretes the Extracellular Aminopeptidase M20/M25/M40 Family Protein to Target Cells for Phagocytosis by Disruption. Molecules. 2017;22.
   Web of Science ®Google Scholar
• Guimaraes AJ, Gomes KX, Cortines JR, et al. Acanthamoeba spp. as a universal host for pathogenic microorganisms: One bridge from environment to host virulence. Microbiol Res. 2016;193:30–38.
   PubMed Web of Science ®Google Scholar
• Rizzo J, et al. Analysis of multiple components involved in the interaction between Cryptococcus neoformans and Acanthamoeba castellanii. Fungal Biol. 2017;121:602–614.
   PubMed Web of Science ®Google Scholar
• Sangenito LS, et al. HIV aspartic peptidase inhibitors are effective drugs against the trypomastigote form of the human pathogen Trypanosoma cruzi. Int J Antimicrob Agents. 2016;48:440–444.
   PubMed Web of Science ®Google Scholar
• Park AJ, Surette MD, Khursigara CM. Antimicrobial targets localize to the extracellular vesicle-associated proteome of Pseudomonas aeruginosa grown in a biofilm. Front Microbiol. 2014;5:464.
   PubMed Web of Science ®Google Scholar
• Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957;226:497–509.
   PubMed Web of Science ®Google Scholar
• Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959;37:911–917.
   PubMedGoogle Scholar
• Arthington-Skaggs BA, Jradi H, Desai T, et al. Quantitation of ergosterol content: novel method for determination of fluconazole susceptibility of Candida albicans. J Clin Microbiol. 1999;37:3332–3337.
   PubMed Web of Science ®Google Scholar
• Skogerson K, Wohlgemuth G, Barupal DK, et al. The volatile compound BinBase mass spectral database. BMC Bioinformatics. 2011;12:321.
   PubMed Web of Science ®Google Scholar
• Shevchenko A, Tomas H, Havlis J, et al. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc. 2006;1:2856–2860.
   PubMed Web of Science ®Google Scholar
• Santos AL, Abreu CM, Alviano CS, et al. Use of proteolytic enzymes as an additional tool for trypanosomatid identification. Parasitology. 2005;130:79–88.
   PubMed Web of Science ®Google Scholar
• Abboud N, et al. A requirement for FcgammaR in antibody-mediated bacterial toxin neutralization. J Exp Med. 2010;207:2395–2405.
   PubMed Web of Science ®Google Scholar
• Wu CA, Yang YW. Induction of cell death by saponin and antigen delivery. Pharm Res. 2004;21:271–277.
   PubMed Web of Science ®Google Scholar
• Jamur MC, Oliver C. Permeabilization of cell membranes. Methods Mol Biol. 2010;588:63–66.
   PubMedGoogle Scholar
• Arqués O, Chicote I, Tenbaum S, et al. Standardized Relative Quantification of Immunofluorescence Tissue Staining. Protocol Exchange. 2012.
   Google Scholar
• Abramoff MD, Magalhaes PJ, Ram SJ. Image Processing with image J. Biophoton Int. 2004.
   Google Scholar