The lysosome represents a central degradative compartment of eukaryote cells, yet little is known about the biogenesis and function of this organelle in parasitic protists. Whereas the mannose 6-phosphate (M6P)-dependent system is dominant for lysosomal targeting in metazoans, oligosaccharide-independent sorting has been reported in other eukaryotes. In this study, we investigated the phagolysosomal proteome of the human parasite Trichomonas vaginalis, its protein targeting and the involvement of lysosomes in hydrolase secretion. The organelles were purified using Percoll and OptiPrep gradient centrifugation and a novel purification protocol based on the phagocytosis of lactoferrin-covered magnetic nanoparticles. The analysis resulted in a lysosomal proteome of 462 proteins, which were sorted into 21 classes. Hydrolases represented the largest functional class and included proteases, lipases, phosphatases, and glycosidases. Identification of a large set of proteins involved in vesicular trafficking (80) and turnover of actin cytoskeleton rearrangement (29) indicate a dynamic phagolysosomal compartment. Several cysteine proteases such as TvCP2 were previously shown to be secreted. Our experiments showed that secretion of TvCP2 was strongly inhibited by chloroquine, which increases intralysosomal pH, thus indicating that TvCP2 secretion occurs through lysosomes rather than the classical secretory pathway. Unexpectedly, we identified divergent homologues of the M6P receptor TvMPR in the phagolysosomal proteome, although T. vaginalis lacks enzymes for M6P formation. To test whether oligosaccharides are involved in lysosomal targeting, we selected the lysosome-resident cysteine protease CLCP, which possesses two glycosylation sites. Mutation of any of the sites redirected CLCP to the secretory pathway. Similarly, the introduction of glycosylation sites to secreted β-amylase redirected this protein to lysosomes. Thus, unlike other parasitic protists, T. vaginalis seems to utilize glycosylation as a recognition marker for lysosomal hydrolases. Our findings provide the first insight into the complexity of T. vaginalis phagolysosomes, their biogenesis, and role in the unconventional secretion of cysteine peptidases.

Department of Parasitology Faculty of Science Charles University BIOCEV Vestec Czech Republic

Department of Parasitology Faculty of Science Charles University BIOCEV Vestec Czech Republic; Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czech Republic

Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czech Republic; Division of Infectious Diseases Department of Medicine University of Alberta Edmonton Alberta Canada

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World Health Organisation . WHO Press, World Health Organization; Geneva, Switzerland: 2012. Global Incidence and Prevalence of Selected Curable Sexually Transmitted Infections 2008.

Twu O., Dessí D., Vu A., Mercer F., Stevens G.C., De Miguel N., Rappelli P., Cocco A.R., Clubb R.T., Fiori P.L., Johnson P.J. Trichomonas vaginalis homolog of macrophage migration inhibitory factor induces prostate cell growth, invasiveness, and inflammatory responses. Proc. Natl. Acad. Sci. U. S. A. 2014;111:8179–8184. PubMed PMC

Kissinger P. Trichomonas vaginalis: A review of epidemiologic, clinical and treatment issues. BMC Infect. Dis. 2015;15:307. PubMed PMC

Petrin D., Delgaty K., Bhatt R., Garber G. Clinical and microbiological aspects of Trichomonas vaginalis. Clin. Microbiol. Rev. 1998;11:300–317. PubMed PMC

Kissinger P., Adamski A. Trichomoniasis and HIV interactions: A review. Sex. Transm. Infect. 2013;89:426–433. PubMed PMC

Benchimol M., De Andrade Rosa I., Da Silva Fontes R., Burla Dias Â.J. Trichomonas adhere and phagocytose sperm cells: Adhesion seems to be a prominent stage during interaction. Parasitol. Res. 2008;102:597–604. PubMed

Midlej V., Benchimol M. Trichomonas vaginalis kills and eats - Evidence for phagocytic activity as a cytopathic effect. Parasitology. 2010;137:65–76. PubMed

Pereira-Neves A., Benchimol M. Phagocytosis by Trichomonas vaginalis: New insights. Biol. Cell. 2007;99:87–101. PubMed

Rendón-Maldonado J.G., Espinosa-Cantellano M., González-Robles A., Martínez-Palomo A. Trichomonas vaginalis: In vitro phagocytosis of lactobacilli, vaginal epithelial cells, leukocytes, and erythrocytes. Exp. Parasitol. 1998;89:241–250. PubMed

Štáfková J., Rada P., Meloni D., Zárský V., Smutná T., Zimmann N., Harant K., Pompach P., Hrdý I., Tachezy J. Dynamic secretome of Trichomonas vaginalis: Case study of β-amylases. Mol. Cell. Proteomics. 2018;17:304–320. PubMed PMC

Pinheiro J., Biboy J., Vollmer W., Hirt R.P., Keown J.R., Artuyants A., Black M.M., Goldstone D.C., Simoes-Barbosa A. The protozoan Trichomonas vaginalis targets bacteria with laterally acquired NlpC/P60 peptidoglycan hydrolases. MBio. 2018;9 PubMed PMC

Twu O., de Miguel N., Lustig G., Stevens G.C., Vashisht A.A., Wohlschlegel J.A., Johnson P.J. Trichomonas vaginalis exosomes deliver cargo to host cells and mediate host:parasite interactions. PLoS Pathog. 2013;9 PubMed PMC

Hyttinen J.M.T., Niittykoski M., Salminen A., Kaarniranta K. Maturation of autophagosomes and endosomes: A key role for Rab7. Biochim. Biophys. Acta Mol. Cell Res. 2013;1833:503–510. PubMed

Ganley I.G. Autophagosome maturation and lysosomal fusion. Essays Biochem. 2013;55:65–78. PubMed

Xu H., Ren D. Lysosomal physiology. Annu. Rev. Physiol. 2015;77:57–80. PubMed PMC

Kinchen J.M., Ravichandran K.S. Phagosome maturation: Going through the acid test. Nat. Rev. Mol. Cell Biol. 2008;9:781–795. PubMed PMC

Yu L., Chen Y., Tooze S.A. Autophagy pathway: Cellular and molecular mechanisms. Autophagy. 2018;14:207–215. PubMed PMC

Benchimol M. Hydrogenosome autophagy: An ultrastructural and cytochemical study. Biol. Cell. 1999;91:165–174. PubMed

Sun Z., Brodsky J.L. Protein quality control in the secretory pathway. J. Cell Biol. 2019;218:3171–3187. PubMed PMC

Peden A.A., Oorschot V., Hesser B.A., Austin C.D., Scheller R.H., Klumperman J. Localization of the AP-3 adaptor complex defines a novel endosomal exit site for lysosomal membrane proteins. J. Cell Biol. 2004;164:1065–1076. PubMed PMC

Janvier K., Bonifacino J.S. Role of the endocytic machinery in the sorting of lysosome-associated membrane proteins. Mol. Biol. Cell. 2005;16:4231–4242. PubMed PMC

Castonguay A.C., Lasanajak Y., Song X., Olson L.J., Cummings R.D., Smith D.F., Dahms N.M. The glycan-binding properties of the cation-independent mannose 6-phosphate receptor are evolutionary conserved in vertebrates. Glycobiology. 2012;22:983–996. PubMed PMC

Lousa C.D.M., Denecke J. Lysosomal and vacuolar sorting: Not so different after all. Biochem. Soc. Trans. 2016;44:891–897. PubMed PMC

Braulke T., Bonifacino J.S. Sorting of lysosomal proteins. Biochim. Biophys. Acta Mol. Cell Res. 2009;1793:605–614. PubMed

Coutinho M.F., Prata M.J., Alves S. Mannose-6-phosphate pathway: A review on its role in lysosomal function and dysfunction. Mol. Genet. Metab. 2012;105:542–550. PubMed

Nakada-Tsukui K., Tsuboi K., Furukawa A., Yamada Y., Nozaki T. A novel class of cysteine protease receptors that mediate lysosomal transport. Cell. Microbiol. 2012;14:1299–1317. PubMed PMC

Bonifacino J.S., Traub L.M. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 2003;72:395–447. PubMed

Puertollano R., Aguilar R.C., Gorshkova I., Crouch R.J., Bonifacino J.S. Sorting of mannose 6-phosphate receptors mediated by the GGAs. Science. 2001;292:1712–1716. PubMed

Höning S., Sandoval I., Von Figura K. A di-leucine-based motif in the cytoplasmic tail of LIMP-II and tyrosinase mediates selective binding of AP-3. EMBO J. 1998;17:1304–1314. PubMed PMC

Kyttälä A., Yliannala K., Schu P., Jalanko A., Luzio J.P. AP-1 and AP-3 facilitate lysosomal targeting of Batten disease protein CLN3 via its dileucine motif. J. Biol. Chem. 2005;280:10277–10283. PubMed

Koumandou V.L., Klute M.J., Herman E.K., Nunez-Miguel R., Dacks J.B., Field M.C. Evolutionary reconstruction of the retromer complex and its function in Trypanosoma brucei. J. Cell Sci. 2011;124:1496–1509. PubMed PMC

Carlton J.M., Hirt R.P., Silva J.C., Delcher A.L., Schatz M., Zhao Q., Wortman J.R., Bidwell S.L., Alsmark U.C.M., Besteiro S., Sicheritz-Ponten T., Noel C.J., Dacks J.B., Foster P.G., Simillion C., et al. Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science. 2007;315:207–212. PubMed PMC

Hernández H.M., Marcet R., Sarracent J. Biological roles of cysteine proteinases in the pathogenesis of Trichomonas vaginalis. Parasite. 2014;21:54. PubMed PMC

Scott D.A., North M.J., Coombs G.H. The pathway of secretion of proteinases in Trichomonas vaginalis. Int. J. Parasitol. 1995;25:657–666. PubMed

Cárdenas-Guerra R.E., Arroyo R., Rosa de Andrade I., Benchimol M., Ortega-López J. The iron-induced cysteine proteinase TvCP4 plays a key role in Trichomonas vaginalis haemolysis. Microbes Infect. 2013;15:958–968. PubMed

Tai J.H., Su H.M., Tsai J., Shaio M.F., Wang C.C. The divergence of Trichomonas vaginalis virus RNAs among various isolates of Trichomonas vaginalis. Exp. Parasitol. 1993;76:278–286. PubMed

Kulda J., Vojtechovska M., Tachezy J., Demes P., Kunzová E. Metronidazole resistance of Trichomonas vaginalis as a cause of treatment failure in trichomoniasis. A case report. Br. J. Vener. Dis. 1982;58:394–399. PubMed PMC

Hrdy I., Hirt R.P., Dolezal P., Bardonová L., Foster P.G., Tachezy J., Embley T.M. Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature. 2004;432:618–622. PubMed

Janssen B.D., Chen Y.P., Molgora B.M., Wang S.E., Simoes-Barbosa A., Johnson P.J. CRISPR/Cas9-mediated gene modification and gene knock out in the human-infective parasite Trichomonas vaginalis. Sci. Rep. 2018;8:270. PubMed PMC

Bradley P.J., Lahti C.J., Plumper E., Johnson P.J. Targeting and translocation of proteins into the hydrogenosome of the protist Trichomonas: Similarities with mitochondrial protein import. EMBO J. 1997;16:3484–3493. PubMed PMC

Nývltová E., Smutná T., Tachezy J., Hrdý I. OsmC and incomplete glycine decarboxylase complex mediate reductive detoxification of peroxides in hydrogenosomes of Trichomonas vaginalis. Mol. Biochem. Parasitol. 2016;206:29–38. PubMed

Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., Tinevez J.Y., White D.J., Hartenstein V., Eliceiri K., Tomancak P., et al. Fiji: An open-source platform for biological-image analysis. Nat. Methods. 2012;9:676–682. PubMed PMC

Woessner D.J., Dawson S.C. The Giardia median body protein is a ventral disc protein that is critical for maintaining a domed disc conformation during attachment. Eukaryot. Cell. 2012;11:292–301. PubMed PMC

Méchin V., Damerval C., Zivy M. Total protein extraction with TCA-acetone. Methods Mol. Biol. 2007;355:1–8. PubMed

Masuda T., Tomita M., Ishihama Y. Phase transfer surfactant-aided trypsin digestion for membrane proteome analysis. J.Proteome.Res. 2008;7:731–740. PubMed

Cox J., Hein M.Y., Luber C.A., Paron I., Nagaraj N., Mann M. Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, Termed MaxLFQ. Mol. Cell. Proteomics. 2014;13:2513–2526. PubMed PMC

Warrenfeltz S., Basenko E., Crouch K., Harb O., Kissinger J., Roos D., Shanmugasundram A., Silva-Franco F. EuPathDB: The eukaryotic pathogen genomics database resource. Methods Mol. Biol. 2018;1757:69–113. PubMed PMC

Madeira F., Park Y.M., Lee J., Buso N., Gur T., Madhusoodanan N., Basutkar P., Tivey A.R.N., Potter S.C., Finn R.D., Lopez R. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res. 2019;47:W636–W641. PubMed PMC

Lal K., Field M.C., Carlton J.M., Warwicker J., Hirt R.P. Identification of a very large Rab GTPase family in the parasitic protozoan Trichomonas vaginalis. Mol. Biochem. Parasitol. 2005;143:226–235. PubMed

Beltrán N.C., Horváthová L., Jedelský P.L., Šedinová M., Rada P., Marcinčiková M., Hrdý I., Tachezy J. Iron-induced changes in the proteome of Trichomonas vaginalis hydrogenosomes. PLoS One. 2013;8 PubMed PMC

Sommer U., Costello C.E., Hayes G.R., Beach D.H., Gilbert R.O., Lucas J.J., Singh B.N. Identification of Trichomonas vaginalis cysteine proteases that induce apoptosis in human vaginal epithelial cells. J. Biol. Chem. 2005;280:23853–23860. PubMed

Rendón-Gandarilla F.J., Ramón-Luing L.D.L.A., Ortega-López J., Rosa De Andrade I., Benchimol M., Arroyo R. The TvLEGU-1, a legumain-like cysteine proteinase, plays a key role in Trichomonas vaginalis cytoadherence. Biomed. Res. Int. 2013;2013 PubMed PMC

Ma L., Meng Q., Cheng W., Sung Y., Tang P., Hu S., Yu J. Involvement of the GP63 protease in infection of Trichomonas vaginalis. Parasitol. Res. 2011;109:71–79. PubMed

De Miguel N., Lustig G., Twu O., Chattopadhyay A., Wohlschlegel J.A., Johnson P.J. Proteome analysis of the surface of Trichomonas vaginalis reveals novel proteins and strain-dependent differential expression. Mol. Cell. Proteomics. 2010;9:1554–1566. PubMed PMC

Srivastava N., Traynor D., Piel M., Kabla A.J., Kay R.R. Pressure sensing through Piezo channels controls whether cells migrate with blebs or pseudopods. Proc. Natl. Acad. Sci. U. S. A. 2020;117:2506–2512. PubMed PMC

Guerra F., Bucci C. Multiple roles of the small GTPase Rab7. Cells. 2016;5:34. PubMed PMC

Hu Z.Q., Rao C.L., Tang M.L., Zhang Y., Lu X.X., Chen J.G., Mao C., Deng L., Li Q., Mao X.H. Rab32 GTpase, as a direct target of miR-30b/c, controls the intracellular survival of Burkholderia pseudomallei by regulating phagosome maturation. PLoS Pathog. 2019;15 PubMed PMC

Patwardhan A., Bardin S., Miserey-Lenkei S., Larue L., Goud B., Raposo G., Delevoye C. Routing of the RAB6 secretory pathway towards the lysosome related organelle of melanocytes. Nat. Commun. 2017;8 PubMed PMC

Egami Y., Fukuda M., Araki N. Rab35 regulates phagosome formation through recruitment of ACAP2 in macrophages during FcγR-mediated phagocytosis. J. Cell Sci. 2011;124:3557–3567. PubMed

Verma K., Datta S. The Monomeric GTPase Rab35 regulates phagocytic cup formation and phagosomal maturation in Entamoeba histolytica. J. Biol. Chem. 2017;292:4960–4975. PubMed PMC

Gutierrez M.G. Functional role(s) of phagosomal Rab GTPases. Small GTPases. 2013;4:148–158. PubMed PMC

Ohno H., Stewart J., Fournier M.C., Bosshart H., Rhee I., Miyatake S., Saito T., Gallusser A., Kirchhausen T., Bonifacino J.S. Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science. 1995;269:1872–1875. PubMed

Caviston J.P., Holzbaur E.L.F. Microtubule motors at the intersection of trafficking and transport. Trends Cell Biol. 2006;16:530–537. PubMed

Krendel M., Mooseker M.S. Myosins: Tails (and heads) of functional diversity. Physiology. 2005;20:239–251. PubMed

Bálint Š., Vilanova I.V., Álvarez Á.S., Lakadamyali M. Correlative live-cell and superresolution microscopy reveals cargo transport dynamics at microtubule intersections. Proc. Natl. Acad. Sci. U. S. A. 2013;110:3375–3380. PubMed PMC

Lübke T., Lobel P., Sleat D.E. Proteomics of the lysosome. Biochim. Biophys. Acta. 2009;1793:625–635. PubMed PMC

Miranda-Ozuna J.F.T., Rivera-Rivas L.A., Cárdenas-Guerra R.E., Hernández-García M.S., Rodríguez-Cruz S., González-Robles A., Chavez-Munguía B., Arroyo R. Glucose-restriction increases Trichomonas vaginalis cellular damage towards HeLa cells and proteolytic activity of cysteine proteinases (CPs), such as TvCP2. Parasitology. 2019;146:1156–1166. PubMed

Dahms N.M., Hancock M.K. P-type lectins. Biochim. Biophys. Acta. 2002;1572:317–340. PubMed

Liu L., Lee W.S., Doray B., Kornfeld S. Role of spacer-1 in the maturation and function of GlcNAc-1-phosphotransferase. FEBS Lett. 2017;591:47–55. PubMed PMC

Gonzalez-Noriega A., Grubb J.H., Talkad V., Sly W.S. Chloroquine inhibits lysosomal enzyme pinocytosis and enhances lysosomal enzyme secretion by impairing receptor recycling. J. Cell Biol. 1980;85:839–852. PubMed PMC

Fedele A.O., Proud C.G. Chloroquine and bafilomycin A mimic lysosomal storage disorders and impair mTORC1 signalling. Biosci. Rep. 2020;40 BSR20200905. PubMed PMC

Chardin P., McCormick F. Brefeldin A: The advantage of being uncompetitive. Cell. 1999;97:153–155. PubMed

Doyle P., Sajid M., O'Brien T., DuBois K., Engel J., Mackey Z., Reed S. Drugs targeting parasite lysosomes. Curr. Pharm. Des. 2008;14:889–900. PubMed

Gao Y., Chen Y., Zhan S., Zhang W., Xiong F., Ge W. Comprehensive proteome analysis of lysosomes reveals the diverse function of macrophages in immune responses. Oncotarget. 2017;8:7420–7440. PubMed PMC

Schröder B.A., Wrocklage C., Hasilik A., Saftig P. The proteome of lysosomes. Proteomics. 2010;10:4053–4076. PubMed

Peterson K.M., Alderete J.F. Iron uptake and increased intracellular enzyme activity follow host lactoferrin binding by Trichomonas vaginalis receptors. J. Exp. Med. 1984;160:398–410. PubMed PMC

Mosen P., Sanner A., Singh J., Winter D. Targeted quantification of the lysosomal proteome in complex samples. Proteomes. 2021;9:1–17. PubMed PMC

Noël C.J., Diaz N., Sicheritz-Ponten T., Safarikova L., Tachezy J., Tang P., Fiori P.L., Hirt R.P. Trichomonas vaginalis vast BspA-like gene family: Evidence for functional diversity from structural organisation and transcriptomics. BMC Genomics. 2010;11:99. PubMed PMC

Molgora B.M., Rai A.K., Sweredoski M.J., Moradian A., Hess S., Johnson P.J. A novel Trichomonas vaginalis surface protein modulates parasite attachment via protein:Host cell proteoglycan interaction. MBio. 2021;12:1–17. PubMed PMC

Arroyo R., Cárdenas-Guerra R.E., Figueroa-Angulo E.E., Puente-Rivera J., Zamudio-Prieto O., Ortega-López J. Trichomonas vaginalis cysteine proteinases: Iron response in gene expression and proteolytic activity. Biomed. Res. Int. 2015;2015 PubMed PMC

Ramón-Luing L.A., Rendón-Gandarilla F.J., Cárdenas-Guerra R.E., Rodríguez-Cabrera N.A., Ortega-López J., Avila-González L., Angel-Ortiz C., Herrera-Sánchez C.N., Mendoza-García M., Arroyo R. Immunoproteomics of the active degradome to identify biomarkers for Trichomonas vaginalis. Proteomics. 2010;10:435–444. PubMed

Hernández-Romano P., Hernández R., Arroyo R., Alderete J.F., López-Villaseñor I. Identification and characterization of a surface-associated, subtilisin-like serine protease in Trichomonas vaginalis. Parasitology. 2010;137:1621–1635. PubMed

Hu G., St. Leger R.J. A phylogenomic approach to reconstructing the diversification of serine proteases in fungi. J. Evol. Biol. 2004;17:1204–1214. PubMed

Li J., Yu L., Yang J., Dong L., Tian B., Yu Z., Liang L., Zhang Y., Wang X., Zhang K. New insights into the evolution of subtilisin-like serine protease genes in Pezizomycotina. BMC Evol. Biol. 2010;10:1–14. PubMed PMC

Shayman J.A., Tesmer J.J.G. Lysosomal phospholipase A2. Biochim. Biophys. Acta Mol. Cell Biol. Lipids. 2019;1864:932–940. PubMed PMC

Harwig S.S.L., Tan L., Qu X.D., Cho Y., Eisenhauer P.B., Lehrer R.I. Bactericidal properties of murine intestinal phospholipase A2. J. Clin. Invest. 1995;95:603–610. PubMed PMC

Fenard D., Lambeau G., Valentin E., Lefebvre J.C., Lazdunski M., Doglio A. Secreted phospholipases A2, a new class of HIV inhibitors that block virus entry into host cells. J. Clin. Invest. 1999;104:611–618. PubMed PMC

Sanon A., Tournaire-Arellano C., Younes El Hage S., Bories C., Caujolle R., Loiseau P.M. N-acetyl-β-d-hexosaminidase from Trichomonas vaginalis: Substrate specificity and activity of inhibitors. Biomed. Pharmacother. 2005;59:245–248. PubMed

Rivero M.R., Miras S.L., Feliziani C., Zamponi N., Quiroga R., Hayes S.F., Rópolo A.S., Touz M.C. Vacuolar protein sorting receptor in Giardia lamblia. PLoS One. 2012;7 PubMed PMC

Sloves P.J., Delhaye S., Mouveaux T., Werkmeister E., Slomianny C., Hovasse A., Dilezitoko Alayi T., Callebaut I., Gaji R.Y., Schaeffer-Reiss C., Van Dorsselear A., Carruthers V.B., Tomavo S. Toxoplasma sortilin-like receptor regulates protein transport and is essential for apical secretory organelle biogenesis and host infection. Cell Host Microbe. 2012;11:515–527. PubMed

Dennes A., Cromme C., Suresh K., Kumar N.S., Eble J.A., Hahnenkamp A., Pohlmann R. The novel Drosophila lysosomal enzyme receptor protein mediates lysosomal sorting in mammalian cells and binds mammalian and Drosophila GGA adaptors. J. Biol. Chem. 2005;280:12849–12857. PubMed

Samuelson J., Banerjee S., Magnelli P., Cui J., Kelleher D.J., Gilmore R., Robbins P.W. The diversity of dolichol-linked precursors to Asn-linked glycans likely results from secondary loss of sets glycosyltranferases. Proc. Natl. Acad. Sci. U. S. A. 2005;102:1548–1553. PubMed PMC

Lee J., Ye Y. The roles of endo-lysosomes in unconventional protein secretion. Cells. 2018;7:198. PubMed PMC

Perez-Riverol Y., Csordas A., Bai J., Bernal-Llinares M., Hewapathirana S., Kundu D., Inuganti A., Griss J., Mayer G., Eisenacher M., Al E. The PRIDE database and related tools and resources in 2019: Improving support for quantification data. Nucleic Acids Res. 2019;47:D442–D450. PubMed PMC

The retromer and retriever systems are conserved and differentially expanded in parabasalids

Double-Stranded RNA Viruses Are Released From Trichomonas vaginalis Inside Small Extracellular Vesicles and Modulate the Exosomal Cargo