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

. 2022 ; 13 () : 893692. [epub] 20220504

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid35602021

Trichomonas vaginalis is a parasitic protist that infects the human urogenital tract. During the infection, trichomonads adhere to the host mucosa, acquire nutrients from the vaginal/prostate environment, and release small extracellular vesicles (sEVs) that contribute to the trichomonad adherence and modulate the host-parasite communication. Approximately 40-70% of T. vaginalis strains harbor a double-stranded RNA virus called Trichomonasvirus (TVV). Naked TVV particles have the potential to stimulate a proinflammatory response in human cells, however, the mode of TVV release from trichomonads to the environment is not clear. In this report, we showed for the first time that TVV particles are released from T. vaginalis cells within sEVs. The sEVs loaded with TVV stimulated a higher proinflammatory response of human HaCaT cells in comparison to sEVs from TVV negative parasites. Moreover, a comparison of T. vaginalis isogenic TVV plus and TVV minus clones revealed a significant impact of TVV infection on the sEV proteome and RNA cargo. Small EVs from TVV positive trichomonads contained 12 enriched and 8 unique proteins including membrane-associated BspA adhesine, and about a 2.5-fold increase in the content of small regulatory tsRNA. As T. vaginalis isolates are frequently infected with TVV, the release of TVV via sEVs to the environment represents an important factor with the potential to enhance inflammation-related pathogenesis during trichomoniasis.

Zobrazit více v PubMed

Abramowicz A., Story M. D. (2020). The long and short of it: the emerging roles of non-coding RNA in small extracellular vesicles. Cancers 12:1445. 10.3390/cancers12061445 PubMed DOI PMC

Ahsan N. A., Sampey G. C., Lepene B., Akpamagbo Y., Barclay R. A., Iordanskiy S., et al. (2016). Presence of viral RNA and proteins in exosomes from cellular clones resistant to Rift Valley fever virus infection. Front. Microbiol. 7:139. 10.3389/fmicb.2016.00139 PubMed DOI PMC

Alderete J. F. (1999). Iron modulates phenotypic variation and phosphorylation of P270 in double-stranded RNA virus-infected Trichomonas vaginalis. Infect. Immun. 67 4298–4302. 10.1128/IAI.67.8.4298-4302.1999 PubMed DOI PMC

Amos B., Aurrecoechea C., Barba M., Barreto A., Basenko E. Y., Bażant W., et al. (2022). VEuPathDB: the eukaryotic pathogen, vector and host bioinformatics resource center. Nucleic Acids Res. 50 D898–D911. 10.1093/nar/gkab929 PubMed DOI PMC

Artuyants A., Campos T. L., Rai A. K., Johnson P. J., Dauros-Singorenko P., Phillips A., et al. (2020). Extracellular vesicles produced by the protozoan parasite Trichomonas vaginalis contain a preferential cargo of tRNA-derived small RNAs. Int. J. Parasitol. 50 1145–1155. 10.1016/J.IJPARA.2020.07.003 PubMed DOI

Atayde V. D., da Silva Lira Filho A., Chaparro V., Zimmermann A., Martel C., Jaramillo M., et al. (2019). Exploitation of the Leishmania exosomal pathway by Leishmania RNA virus 1. Nat. Microbiol. 4 714–723. 10.1038/S41564-018-0352-Y PubMed DOI

Bayer-Santos E., Lima F. M., Ruiz J. C., Almeida I. C., Da Silveira J. F. (2014). Characterization of the small RNA content of Trypanosoma cruzi extracellular vesicles. Mol. Biochem. Parasitol. 193 71–74. 10.1016/J.MOLBIOPARA.2014.02.004 PubMed DOI PMC

Belfort I. K. P., Cunha A. P. A., Mendes F. P. B., Galvão-Moreira L. V., Lemos R. G., de Lima Costa L. H., et al. (2021). Trichomonas vaginalis as a risk factor for human papillomavirus: a study with women undergoing cervical cancer screening in a northeast region of Brazil. BMC Womens Health 21:174. 10.1186/s12905-021-01320-6 PubMed DOI PMC

Benchimol M., Monteiro S. P., Chang T. H., Alderete J. F. (2002). Virus in Trichomonas - an ultrastructural study. Parasitol. Int. 51 293–298. 10.1016/S1383-5769(02)00016-8 PubMed DOI

Bessarab I. N., Nakajima R., Liu H. W., Tai J. H. (2011). Identification and characterization of a type III Trichomonas vaginalis virus in the protozoan pathogen Trichomonas vaginalis. Arch. Virol. 156 285–294. 10.1007/s00705-010-0858-y PubMed DOI

Bienkowska-Haba M., Luszczek W., Keiffer T. R., Guion L. G. M., DiGiuseppe S., Scott R. S., et al. (2017). Incoming human papillomavirus 16 genome is lost in PML protein-deficient HaCaT keratinocytes. Cell. Microbiol. 19:e12708. 10.1111/CMI.12708 PubMed DOI PMC

Boukamp P., Petrussevska R. T., Breitkreutz D., Hornung J., Markham A., Fusenig N. E. (1988). Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106 761–771. 10.1083/JCB.106.3.761 PubMed DOI PMC

Cantalapiedra C. P., Hernández-Plaza A., Letunic I., Bork P., Huerta-Cepas J. (2021). eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol. Biol. Evol. 38 5825–5829. 10.1093/MOLBEV/MSAB293 PubMed DOI PMC

Corrado C., Barreca M. M., Zichittella C., Alessandro R., Conigliaro A. (2021). Molecular mediators of rna loading into extracellular vesicles. Cells 10:3355. 10.3390/cells10123355 PubMed DOI PMC

Cox J., Hein M. Y., Luber C. A., Paron I., Nagaraj N., Mann M. (2014). Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol. Cell. Proteomics 13 2513–2526. 10.1074/MCP.M113.031591 PubMed DOI PMC

Crenshaw B. J., Gu L., Sims B., Matthews Q. L. (2018). Exosome biogenesis and biological function in response to viral infections. Open Virol. J. 12 134–148. 10.2174/1874357901812010134 PubMed DOI PMC

De Miguel N., Lustig G., Twu O., Chattopadhyay A., Wohlschlegel J. A., Johnson P. J. (2010). Proteome analysis of the surface of Trichomonas vaginalis reveals novel proteins and strain-dependent differential expression. Mol. Cell. Proteomics 9 1554–1566. 10.1074/mcp.M000022-MCP201 PubMed DOI PMC

Diamond L. S. (1957). The establishment of various trichomonads of animals and man in axenic cultures. J. Parasitol. 43 488–490. 10.2307/3274682 PubMed DOI

Dias-Guerreiro T., Palma-Marques J., Mourata-Gonçalves P., Alexandre-Pires G., Valério-Bolas A., Gabriel Á., et al. (2021). African trypanosomiasis: extracellular vesicles shed by Trypanosoma brucei brucei manipulate host mononuclear cells. Biomedicines 9:1056. 10.3390/biomedicines9081056 PubMed DOI PMC

Dong G., Filho A. L., Olivier M. (2019). Modulation of host-pathogen communication by extracellular vesicles (EVs) of the protozoan parasite Leishmania. Front. Cell. Infect. Microbiol. 9:100. 10.3389/fcimb.2019.00100 PubMed DOI PMC

Dou S., Wang Y., Lu J. (2019). Metazoan tsRNAs: biogenesis, evolution and regulatory functions. Noncoding RNA 5:18. 10.3390/ncrna5010018 PubMed DOI PMC

Emanuelsson O., Brunak S., von Heijne G., Nielsen H. (2007). Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2 953–971. 10.1038/nprot.2007.131 PubMed DOI

Fichorova R. N., Lee Y., Yamamoto H. S., Takagi Y., Hayes G. R., Goodman R. P., et al. (2012). Endobiont viruses sensed by the human host - beyond conventional antiparasitic therapy. PLoS One 7:e48418. 10.1371/JOURNAL.PONE.0048418 PubMed DOI PMC

Fichorova R. N., Rheinwald J. G., Anderson D. J. (1997). Generation of papillomavirus-immortalized cell lines from normal human ectocervical, endocervical, and vaginal epithelium that maintain expression of tissue-specific differentiation proteins. Biol. Reprod. 57 847–855. 10.1095/BIOLREPROD57.4.847 PubMed DOI

Flegr J., Čerkasov J., Kulda J., Tachezy J., Štokrová J. (1987). The dsRNA of Trichomonas vaginalis is associated with virus-like particles and does not correlate with metronidazole resistance. Folia Microbiol. 32 345–348. 10.1007/BF02877224 PubMed DOI

Fraga J., Rojas L., Sariego I., Fernández-Calienes A., Nuñez F. A. (2012). Species typing of Cuban Trichomonas vaginalis virus by RT-PCR, and association of TVV-2 with high parasite adhesion levels and high pathogenicity in patients. Arch. Virol. 157 1789–1795. 10.1007/S00705-012-1353-4 PubMed DOI

Galperin M. Y., Wolf Y. I., Makarova K. S., Alvarez R. V., Landsman D., Koonin E. V. (2021). COG database update: focus on microbial diversity, model organisms, and widespread pathogens. Nucleic Acids Res. 49 D274–D281. 10.1093/NAR/GKAA1018 PubMed DOI PMC

Goodman R. P., Ghabrial S. A., Fichorova R. N., Nibert M. L. (2011). Trichomonasvirus: a new genus of protozoan viruses in the family Totiviridae. Arch. Virol. 156 171–179. 10.1007/S00705-010-0832-8 PubMed DOI PMC

Govender Y., Chan T., Yamamoto H. S., Budnik B., Fichorova R. N. (2020). The role of small extracellular vesicles in viral-protozoan symbiosis: lessons from Trichomonasvirus in an isogenic host parasite model. Front. Cell. Infect. Microbiol. 10:591172. 10.3389/FCIMB.2020.591172 PubMed DOI PMC

Graves K. J., Ghosh A. P., Schmidt N., Augostini P., Evan Secor W., Schwebke J. R., et al. (2019). Trichomonas vaginalis virus among women with trichomoniasis and associations with demographics, clinical outcomes, and metronidazole resistance. Clin. Infect. Dis. 69 2170–2176. 10.1093/cid/ciz146 PubMed DOI PMC

Guduric-Fuchs J., O’Connor A., Camp B., O’Neill C. L., Medina R. J., Simpson D. A. (2012). Selective extracellular vesicle-mediated export of an overlapping set of microRNAs from multiple cell types. BMC Genomics 13:357. 10.1186/1471-2164-13-357 PubMed DOI PMC

Handrich M. R., Garg S. G., Sommerville E. W., Hirt R. P., Gould S. B. (2019). Characterization of the BspA and Pmp protein family of trichomonads. Parasit. Vectors 12:406. 10.1186/S13071-019-3660-Z PubMed DOI PMC

Hirt R. P., Sherrard J. (2015). Trichomonas vaginalis origins, molecular pathobiology and clinical considerations. Curr. Opin. Infect. Dis. 28 72–79. 10.1097/QCO.0000000000000128 PubMed DOI

Hrdy I., Hirt R. P., Dolezal P., Bardonová L., Foster P. G., Tachezy J., et al. (2004). Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432 618–622. 10.1038/NATURE03149 PubMed DOI

Iša P., Pérez-Delgado A., Quevedo I. R., López S., Arias C. F. (2020). Rotaviruses associate with distinct types of extracellular vesicles. Viruses 12:763. 10.3390/V12070763 PubMed DOI PMC

Ives A., Ronet C., Prevel F., Ruzzante G., Fuertes-Marraco S., Schutz F., et al. (2011). Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science 331 775–778. 10.1126/SCIENCE.1199326 PubMed DOI PMC

Ju Y., Bai H., Ren L., Zhang L. (2021). The role of exosome and the ESCRT pathway on enveloped virus infection. Int. J. Mol. Sci. 22:9060. 10.3390/IJMS22169060 PubMed DOI PMC

Kissinger P., Adamski A. (2013). Trichomoniasis and HIV interactions: a review. Sex. Transm. Infect. 89 426–433. 10.1136/SEXTRANS-2012-051005 PubMed DOI PMC

Kowal J., Arras G., Colombo M., Jouve M., Morath J. P., Primdal-Bengtson B., et al. (2016). Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc. Natl. Acad. Sci. U.S.A. 113 E968–E977. 10.1073/PNAS.1521230113 PubMed DOI PMC

Krogh A., Larsson B., Von Heijne G., Sonnhammer E. L. L. (2001). Predicting transmembrane protein topology with a hidden markov model: application to complete genomes. J. Mol. Biol. 305 567–580. 10.1006/JMBI.2000.4315 PubMed DOI

Kuhlmann F. M., Robinson J. I., Bluemling G. R., Ronet C., Fasel N., Beverley S. M. (2017). Antiviral screening identifies adenosine analogs targeting the endogenous dsRNA Leishmania RNA virus 1 (LRV1) pathogenicity factor. Proc. Natl. Acad. Sci. U.S.A. 114 E811–E819. 10.1073/pnas.1619114114 PubMed DOI PMC

Kushwaha B., Devi A., Maikhuri J. P., Rajender S., Gupta G. (2021). Inflammation driven tumor-like signaling in prostatic epithelial cells by sexually transmitted Trichomonas vaginalis. Int. J. Urol. 28 225–240. 10.1111/IJU.14431/FORMAT/PDF PubMed DOI

Lambertz U., Oviedo Ovando M. E., Vasconcelos E. J. R., Unrau P. J., Myler P. J., Reiner N. E. (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 16:151. 10.1186/S12864-015-1260-7 PubMed DOI PMC

Langmead B., Salzberg S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nat. Methods 94 357–359. 10.1038/nmeth.1923 PubMed DOI PMC

Li S., Xu Z., Sheng J. (2018). tRNA-derived small RNA: a novel regulatory small non-coding RNA. Genes 9:246. 10.3390/genes9050246 PubMed DOI PMC

Liu H. W., Chu Y. D., Tai J. H. (1998). Characterization of Trichomonas vaginalis virus proteins in the pathogenic protozoan T. vaginalis. Arch. Virol. 143 963–970. 10.1007/s007050050345 PubMed DOI

Longatti A., Boyd B., Chisari F. V. (2015). Virion-independent transfer of replication-competent hepatitis C virus RNA between permissive cells. J. Virol. 89 2956–2961. 10.1128/JVI.02721-14 PubMed DOI PMC

Meckes D. G., Shair K. H. Y., Marquitz A. R., Kung C. P., Edwards R. H., Raab-Traub N. (2010). Human tumor virus utilizes exosomes for intercellular communication. Proc. Natl. Acad. Sci. U.S.A. 107 20370–20375. 10.1073/PNAS.1014194107 PubMed DOI PMC

Mitteregger D., Aberle S. W., Makristathis A., Walochnik J., Brozek W., Marberger M., et al. (2012). High detection rate of Trichomonas vaginalis in benign hyperplastic prostatic tissue. Med. Microbiol. Immunol. 201 113–116. 10.1007/S00430-011-0205-2 PubMed DOI

Morris-Love J., Gee G. V., O’Hara B. A., Assetta B., Atkinson A. L., Dugan A. S., et al. (2019). JC polyomavirus uses extracellular vesicles to infect target cells. mBio 10:e00379-19. 10.1128/mBio.00379-19 PubMed DOI PMC

Narayanasamy R. K., Rada P., Zdrha A., van Ranst M., Neyts J., Tachezy J. (2021). Cytidine nucleoside analog is an effective antiviral drug against Trichomonasvirus. J. Microbiol. Immunol. Infect. 55 191–198. 10.1016/j.jmii.2021.08.008 PubMed DOI

Nievas Y. R., Coceres V. M., Midlej V., de Souza W., Benchimol M., Pereira-Neves A., et al. (2018). Membrane-shed vesicles from the parasite Trichomonas vaginalis: characterization and their association with cell interaction. Cell. Mol. Life Sci. 75 2211–2226. 10.1007/s00018-017-2726-3 PubMed DOI PMC

Nobre L. S., Meloni D., Teixeira M., Viscogliosi E., Saraiva L. M. (2016). Trichomonas vaginalis repair of iron centres proteins: the different role of two paralogs. Protist 167 222–233. 10.1016/j.protis.2016.03.001 PubMed DOI

Noël C. J., Diaz N., Sicheritz-Ponten T., Safarikova L., Tachezy J., Tang P., et al. (2010). Trichomonas vaginalis vast BspA-like gene family: evidence for functional diversity from structural organisation and transcriptomics. BMC Genomics 11:99. 10.1186/1471-2164-11-99 PubMed DOI PMC

Olmos-Ortiz L. M., Barajas-Mendiola M. A., Barrios-Rodiles M., Castellano L. E., Arias-Negrete S., Avila E. E., et al. (2017). Trichomonas vaginalis exosome-like vesicles modify the cytokine profile and reduce inflammation in parasite-infected mice. Parasite Immunol. 39:e12426. 10.1111/PIM.12426 PubMed DOI

Opadokun T., Rohrbach P. (2021). Extracellular vesicles in malaria: an agglomeration of two decades of research. Malar. J. 20:442. 10.1186/S12936-021-03969-8 PubMed DOI PMC

Parent K. N., Takagi Y., Cardone G., Olson N. H., Ericsson M., Yang M., et al. (2013). Structure of a protozoan virus from the human genitourinary parasite Trichomonas vaginalis. mBio 4:e00056-13. 10.1128/MBIO.00056-13 PubMed DOI PMC

Perez-Riverol Y., Csordas A., Bai J., Bernal-Llinares M., Hewapathirana S., Kundu D. J., et al. (2019). The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 47 D442–D450. 10.1093/NAR/GKY1106 PubMed DOI PMC

Poeck H., Bscheider M., Gross O., Finger K., Roth S., Rebsamen M., et al. (2010). Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1 beta production. Nat. Immunol. 11 63–69. 10.1038/NI.1824 PubMed DOI

Rabouille C. (2017). Pathways of unconventional protein secretion. Trends Cell Biol. 27 230–240. 10.1016/J.TCB.2016.11.007 PubMed DOI

Rada P., Kellerová P., Verner Z., Tachezy J. (2019). Investigation of the secretory pathway in Trichomonas vaginalis argues against a moonlighting function of hydrogenosomal enzymes. J. Eukaryot. Microbiol. 66 899–910. 10.1111/jeu.12741 PubMed DOI

Rada P., Makki A. R., Zimorski V., Garg S., Hampl V., Hrdý I., et al. (2015). N-terminal presequence-independent import of phosphofructokinase into hydrogenosomes of Trichomonas vaginalis. Eukaryot. Cell 14 1264–1275. 10.1128/EC.00104-15 PubMed DOI PMC

Rai A. K., Johnson P. J. (2019). Trichomonas vaginalis extracellular vesicles are internalized by host cells using proteoglycans and caveolin-dependent endocytosis. Proc. Natl. Acad. Sci. U.S.A. 116 21354–21360. 10.1073/pnas.1912356116 PubMed DOI PMC

Reyes-Ruiz J. M., Osuna-Ramos J. F., de Jesús-González L. A., Palacios-Rápalo S. N., Cordero-Rivera C. D., Farfan-Morales C. N., et al. (2020). The regulation of flavivirus infection by hijacking exosome-mediated cell-cell communication: new insights on virus-host interactions. Viruses 12:765. 10.3390/v12070765 PubMed DOI PMC

Saad M. H., Badierah R., Redwan E. M., El-Fakharany E. M. (2021). A comprehensive insight into the role of exosomes in viral infection: dual faces bearing different functions. Pharmaceutics 13:1405. 10.3390/pharmaceutics13091405 PubMed DOI PMC

Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9 676–682. 10.1038/NMETH.2019 PubMed DOI PMC

Silver B. J., Guy R. J., Kaldor J. M., Jamil M. S., Rumbold A. R. (2014). Trichomonas vaginalis as a cause of perinatal morbidity: a systematic review and meta-analysis. Sex. Transm. Dis. 41 369–376. 10.1097/OLQ.0000000000000134 PubMed DOI

Sokol C. L., Luster A. D. (2015). The chemokine system in innate immunity. Cold Spring Harb. Perspect. Biol. 7:a016303. 10.1101/CSHPERSPECT.A016303 PubMed DOI PMC

Stáfková J., Rada P., Meloni D., Zárský V., Smutná T., Zimmann N., et al. (2018). Dynamic secretome of Trichomonas vaginalis: case study of β-amylases. Mol. Cell. Proteomics 17 304–320. 10.1074/MCP.RA117.000434 PubMed DOI PMC

Steinegger M., Meier M., Mirdita M., Vöhringer H., Haunsberger S. J., Söding J. (2019). HH-suite3 for fast remote homology detection and deep protein annotation. BMC Bioinformatics 20:473. 10.1186/S12859-019-3019-7 PubMed DOI PMC

Stepkowski S., Honigberg B. M. (1972). Antigenic analysis of virulent and avirulent strains of Trichomonas gallinae by gel diffusion methods. J. Protozool. 19 306–315. 10.1111/j.1550-7408.1972.tb03465.x PubMed DOI

Stevens A., Muratore K., Cui Y., Johnson P. J., Zhou Z. H. (2021). Atomic structure of the Trichomonas vaginalis double-stranded RNA virus 2. mBio 12:e02924-20. 10.1128/mBio.02924-20 PubMed DOI PMC

Strober W. (2015). Trypan blue exclusion test of cell viability. Curr. Protoc. Immunol. 111 A3.B.1–A3.B.3. 10.1002/0471142735.IMA03BS111 PubMed DOI PMC

Studier F. W. (2005). Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41 207–234. 10.1016/J.PEP.2005.01.016 PubMed DOI

Sutton M., Sternberg M., Koumans E. H., McQuillan G., Berman S., Markowitz L. (2007). The prevalence of Trichomonas vaginalis infection among reproductive-age women in the United States, 2001-2004. Clin. Infect. Dis. 45 1319–1326. 10.1086/522532 PubMed DOI

Todd K. V., Tripp R. A. (2020). Exosome-mediated human norovirus infection. PLoS One 15:e0237044. 10.1371/JOURNAL.PONE.0237044 PubMed DOI PMC

Twu O., de Miguel N., Lustig G., Stevens G. C., Vashisht A. A., Wohlschlegel J. A., et al. (2013). Trichomonas vaginalis exosomes deliver cargo to host cells and mediate host:parasite interactions. PLoS Pathog. 9:e1003482. 10.1371/journal.ppat.1003482 PubMed DOI PMC

Twu O., Dessí D., Vu A., Mercer F., Stevens G. C., De Miguel N., et al. (2014). Trichomonas vaginalis homolog of macrophage migration inhibitory factor induces prostate cell growth, invasiveness, and inflammatory responses. Proc. Natl. Acad. Sci. U.S.A. 111 8179–8184. 10.1073/pnas.1321884111 PubMed DOI PMC

Van Gerwen O. T., Camino A. F., Sharma J., Kissinger P. J., Muzny C. A. (2021). Epidemiology, natural history, diagnosis, and treatment of Trichomonas vaginalis in men. Clin. Infect. Dis. 73 1119–1124. 10.1093/cid/ciab514 PubMed DOI PMC

Van Kuppeveld F. J. M., Johansson K. E., Galama J. M. D., Kissing J., Bolske G., Van der Logt J. T. M., et al. (1994). Detection of mycoplasma contamination in cell cultures by a mycoplasma group-specific PCR. Appl. Environ. Microbiol. 60 149–152. 10.1128/AEM.60.1.149-152.1994 PubMed DOI PMC

Vonka V., Petrovska P., Borecky L., Roth Z. (1995). Increased effects of topically applied interferon on herpes simplex virus-induced lesions by caffeine. Acta Virol. 39 125–130. PubMed

Wang A., Wang C. C., Alderete J. F. (1987). Trichomonas Vaginalis phenotypic variation occurs only among trichomonads infected with the double-stranded RNA virus. J. Exp. Med. 166 142–150. 10.1084/jem.166.1.142 PubMed DOI PMC

Wang A. L., Wang C. C. (1986). The double-stranded RNA in Trichomonas vaginalis may originate from virus-like particles. Proc. Natl. Acad. Sci. U.S.A. 83 7956–7960. 10.1073/PNAS.83.20.7956 PubMed DOI PMC

Wang T., Fang L., Zhao F., Wang D., Xiao S. (2018). Exosomes mediate intercellular transmission of porcine reproductive and respiratory syndrome virus. J. Virol. 92:e01734-17. 10.1128/jvi.01734-17 PubMed DOI PMC

Wang Z. S., Zhou H. C., Wei C. Y., Wang Z. H., Hao X., Zhang L. H., et al. (2021). Global survey of miRNAs and tRNA-derived small RNAs from the human parasitic protist Trichomonas vaginalis. Parasit. Vectors 14:87. 10.1186/S13071-020-04570-9 PubMed DOI PMC

World Health Organization [WHO] (2018). Report on Global Sexually Transmitted Infection Surveillance. Available Online at: https://www.who.int/publications/i/item/9789241565691

Xu X., Zhang D., Ding W., Wang W., Jin N., Ding Z. (2021). NDV related exosomes enhance NDV replication through exporting NLRX1 mRNA. Vet. Microbiol. 260:109167. 10.1016/j.vetmic.2021.109167 PubMed DOI

Yagur Y., Weitzner O., Barchilon Tiosano L., Paitan Y., Katzir M., Schonman R., et al. (2021). Characteristics of pelvic inflammatory disease caused by sexually transmitted disease - an epidemiologic study. J. Gynecol. Obstet. Hum. Reprod. 50:102176. 10.1016/J.JOGOH.2021.102176 PubMed DOI

Zimmann N., Rada P., Žárský V., Smutná T., Záhonová K., Dacks J., et al. (2021). Proteomic analysis of Trichomonas vaginalis phagolysosome, lysosomal targeting, and unconventional secretion of cysteine peptidases. Mol. Cell. Proteomics 21:100174. 10.1016/J.MCPRO.2021.100174 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...