PROTOZOONLARIN VİRAL ENDOSİMBİYONTLARI
Year 2023,
Volume: 14 Issue: 1, 25 - 35, 06.05.2023
Ayşegül Damlapınar
,
Kader Yıldız
Abstract
Bazı parazitik protozoonlarda viral endosimbiyontlar ve virüs benzeri partiküller keşfedilmiştir. Bunların protozoonlara etkisi ve konaktaki şekillenen enfeksiyondaki rolü dikkati çekmektedir. Viral endosimbiyontların protozoonların konakta oluşturduğu patojeniteye katkısına dair bazı veriler mevcuttur. Bu derlemede; protozoonlarda bulunan viral endosimbiyontlar hakkında bilgi vermek amaçlanmıştır.
References
- Adaui, V., Lye, L. F., Akopyants, N. S., Zimic, M., Llanos-Cuentas, A., Garcia, L., Maes, I., Doncker, S., Dobson, D. E., Arevalo, J., Dujardin, J. C. & Beverley, S. M. (2016). Association of the Endobiont Double-Stranded RNA Virus LRV1 With Treatment Failure for Human Leishmaniasis Caused by Leishmania braziliensis in Peru and Bolivia. The Journal of Infectious Diseases, 213, 112-121.
- Alderete, J. F., Wendel, K. A., Rompalo, A. M., Erbelding, E. J., Benchimol, M. & Chang, T. H. (2003). Trichomonas vaginalis: evaluating capsid proteins of dsRNA viruses and the dsRNA virus within patients attending a sexually transmitted disease clinic. Experimental Parasitology, 103, 44-50.
- Arslan, M. Ö. & Sarı, B. (2015). Eimeriidae (Coccidiosis). N. Dumanlı ve Z. Karaer (Edt.), Veteriner Protozooloji (2.baskı), Ankara: Medisan Yayınevi, 77
- Atayde, A. V., Filho, A. S. L., Chaparro, V., Zimmermann, A., Martel, C., Jaramillo, M. & Olivier, M. (2019). Nature Microbiology, 4, 714-723.
- Becker, D. L., Santos, O., Frasson, A. P., Rigo, G. V., Macedo, A. J. & Tasca, T. (2015). High rates of Double-Stranded RNA Viruses and Mycoplasma hominis in Trichomonas vaginalis Clinical Isolates in South Brazil. Infection, Genetics and Evolution, 34, 181-187.
- Benchimol, M., Monteiro, S. P., Chang, T. H. & Alderete, J. F. (2002). Virus in Trichomonas—an ultrastructural study. Parasitology International, 51 (3), 293- 298.
- Berber, E., Şimşek, E., Çanakoğlu, N., Sürsal, N. & Gençay-Göksu, A. (2021). Newly identified Cryptosporidium parvum virus-1 from newborn calf diarrhoea in Turkey. Transboundary and Emerging Diseases, 68 (4), 2571-2580.
- Boratto, P. V. M., Oliveira, G. P., Machado, T. B., Andrade, A. C. S. P., Baudoin, J. P., Klose, T., Schulz, F., Azza, S., Decloquemen, P., Chabrière, E., Colson, P., Levasseur, A., Scola, B. L. & Abrahao, J. S. (2020). Yaravirus: Bulaşan yeni bir 80-nm virüs Acanthamoeba castellanii. Proceedings of the National Academy of Sciences, 117 (28), 16579-16586.
- Cacho, E., Gallego, M., Montes., C., Lopez-Bernad, F., Quilez, J. & Sanchez-Acedo, C. (2001). Eimeria necatrix virus: intracellular localisation of viral particles and proteins. International Journal for Parasitology, 31, 1269-1274.
- Cadd, T. L., Keenan, M. C. & Patterson, J. L. (1993). Detection of Leishmania RNA virus 1 proteins. Journal of Virology, 67 (9), 5647-5650.
- Castiglioni, P., Hartley, M. A., Rossi, M., Prevel, F., Desponds, C., Utzschneider, D. T., Eren, R. O., Zangger, H., Brunner, L., Collin, N., Zehn, D., Kuhlmann, F. M., Beverley, S. M., Fasel, N. & Ronet., C. (2017). Exacerbated Leishmaniasis Caused by a Viral Endosymbiont can be Prevented by Immunization with Its Viral Capsid. Plos Neglected Tropical Diseases, 11 (1), e0005240.
- Charon, J., Grigg, M J., Eden, J. S., Piera, K. A., Rana, H., William, T., Rose, K., Davenport, M. P., Anstey, N. M. & Holmes, E. C. (2019). Novel RNA viruses associated with Plasmodium vivax in human malaria and Leucocytozoon parasites in avian disease. PLOS Pathogens, 15 (12), e1008216.
- Diamond, L. S. & Mattern, C. F. T. (1976). Protozoal Viruses. Advances in Virus Research, 20, 87-112.
- El-Gayar, E. K., Mokhtar, A. B. & Hassan, W. A. (2016). Molecular characterization of double-stranded RNA virus in Trichomonas vaginalis Egyptian isolates and its association with pathogenicity. Parasitology Research, 115 (10), 4027-4036.
- Ellis, J. & Revets, H. (1990). Eimeria species which infect the chicken contain virus-like RNA molecules. Parasitology, 101 (2), 163.
- Eren, R. O., Reverte, M., Rossi, M., Hartley, M. A., Castiglioni, P., Prevel, F., Martin, R., Desponds, C., Lye, L. F., Drexler, S. K., Reith, W., Beverley, S. M., Ronet, C. & Fasel, N. (2016). Mammalian Innate Immune Response to a Leishmania-Resident RNA Virus Increases Macrophage Survival to Promote Parasite Persistence. Cell Host & Microbe, 20 (3), 318-328.
- Ertabaklar, H., Malatyalı, E., Özün-Özbay, E. P., Yıldız, İ., Sinecen, M., Ertuğ, S., Bozdoğan, B. & Güçlü, Ö. (2021). Microsatellite-Based Genotyping, Analysis of Population Structure, Presence of Trichomonas vaginalis Virus (TVV) and Mycoplasma hominis in T. vaginalis Isolates from Southwest of Turkey. Iranian Journal of Parasitology, 16 (1), 81-90.
- Fichorova, R. N., Lee, Y., Yamamoto, H. S., Takagi, Y., Hayes, G. R., Goodman, R.P., Chepa-Lotrea, X, Buck, O. R., Murray, R., Kula, T., Beach., D. H., Singh, B. N. & Nibert., M. L. (2012). Endobiont Viruses Sensed by the Human Host–Beyond Conventional Antiparasitic Therapy. Plos One, 7 (11), e48418.
- Fraga, J., Rojas, L., Sariego, I. & Fernández-Calienes, A. (2012). Genetic characterization of three Cuban Trichomonas vaginalis virus. Phylogeny of Totiviridae family. Infection, Genetics and Evolution, 12 (1), 113-120.
- Fraga, J., Rojas, L., Sariego, I. & Fernández-Calienes, A. & Núñez, F. A, (2007). Double-Stranded RNA Viral Infection of Trichomonas vaginalis and Association with Clinical Presentation. Acta Parasitologica, 46, 93-98.
- Garnham, P. C. C., Bird, R. G. & Baker, J. R. (1962). Electron microscope studies of motile stages of malaria parasites: III. The ookinetes of Haemamoeba and Plasmodium. Trans R Soc Trop Med Hyg, 56 (2), 116-120.
- Gong, P., Li, X., Wu, W., Cao, L., Zhao, P., Li, X., Ren, B., Li, J. & Zhang, X. (2020). A novel microRNA from the translated region of the Giardiavirus rdrp gene governs virus copy number in Giardia duodenalis. Frontiers in Microbiology, 11, 569412.
- Guilbride, L., Myler, P. J. & Stuart, K. (1992). Distribution and sequence divergence of LRV1 viruses among different Leishmania species. Mol Biochem Parasitol, 54 (1), 101-104.
- Gündoğdu, A. & Ulu-Kılıç, A. (2018). Bakteriyofaj Terapisi: Unutulmuş Bir Şifa Kaynağı. Klimik Dergisi, 31 (2), 78-87.
- Hajjaran, H., Mahdi, M., Mohebali, M., Samimi-Rad, K., Ataei-Pirkooh, A., Kazemi-Rad, E., Naddaf, S. R. & Raoofian, R. (2016). Detection and molecular identification of Leishmania RNA virus (LRV) in Iranian Leishmania species. Archives of Virology, 161 (12), 3385-3390.
- Han, Q., Li, J., Gong, P., Gai, J., Li, S. & Zhang, X. (2011). Virus-like particles in Eimeria tenella are associated with multiple RNA segments. Experimental Parasitology, 127, 646-650.
- Hartley, M. A., Bourreau, E., Rossi, M., Castiglioni, P., Eren, R. O., Prevel, F., Couppié, P., Hickerson, S. M., Launois, P., Beverley, S. M., Ronet, C. & Fasel, F. (2016). Leishmaniavirus-DependentMetastatic LeishmaniasisIs Prevented by Blocking IL-17A. Plos Pathogens, 12 (9), e1005852.
- He, D., Pengtao, G., Ju, Y., Jianhua, L., He, L., Guocai, Z. & Xichen, Z. (2017). Differential Protein Expressions in Virus-Infected and Uninfected Trichomonas vaginalis. The Korean Journal of Parasitol, 55 (2), 121-128.
- Heidary, S., Bandehpour, M., Valadkhani, Z., Seyyed –Tabaee, S. J., Haghigh, A., Abadi, A. R. & Kazemi, B. (2013). Double-Stranded RNA Viral Infection in Tehran Trichomonas vaginalis Isolates. Iranian Journal of Parasitology, 8 (1), 60-64.
- Hillman, B. I. & Cohen A. B., (2021). Totiviruses (Totiviridae). Encyclopedia of Virology (4.baskı), Academic Press; Pp: 648-657.
- International Committee on Taxonomy of Viruses (2022). https://ictv.global/taxonomy/taxondetails?taxnode_id=202112530 (Erişim: 20.12.2022).
- Jenkins, M. C., Higgins, J., Abrahante, J. E., Kniel, K. E., O’Brien, C., Trout, J., Lancto, C. A., Abrahamsen, M. S. & Fayer, R. (2008). Fecundity of Cryptosporidium parvum is correlated with intracellular levels of the viral symbiont CPV. International Journal for Parasitology, 38, 1051-1055.
- Jenkins, M. C., O’Brien, C. N. & Fayer, R. (2015). Changes in the levels of Cryspovirus during in vitro development of Cryptosporidium parvum. Parasitology Research, 114, 2063-2068.
- Jonckheere, J. F. & Gordts, B. (1987). Occurrence and transfection of a Giardia virus. Molecular and Biochemical Parasitology, 23 (1), 85-89.
- Kar, S., Güven, E. & Karaer, Z. (2015). Hexamitidae. Genel Protozooloji. N. Dumanlı ve Z. Karaer (Edt.), Veteriner Protozooloji (2.baskı), 45-51. Ankara: Medisan Yayınevi.
- Karaer, Z. & Nalbantoğlu, S. (2015). Trypanosomatidae. N. Dumanlı ve Z. Karaer (Edt.), Veteriner Protozooloji (2.baskı), Ankara: Medisan Yayınevi; Pp: 35-42.
- Keen, E. C. (2013). Beyond phage therapy: Virotherapy of protozoal diseases. Future Microbiology, 8 (7), 821-823.
- Khanaliha, K., Masoumi-Asl, H., Bokharaei-Salim, F., Tabatabaei, A. & Naghdalipoor, M. (2017). Double-stranded RNA viral infection of Trichomonas vaginalis (TVV1) in Iranian isolates. Microbial Pathogenesis, 109, 56-60.
- Khoshnan, A. & Alderete, J. F. (1994). Trichomonas vaginalis with a double-stranded RNA virus has upregulated levels of phenotypically variable immunogen mRNA. Journal of Virology, 68 (6), 4035-4038.
- Khramtsov, N. V. & Upton, S. J. (2000). Association of RNA polymerase complexes of the parasitic protozoan Cryptosporidium parvum with virus-like particles: heterogeneous system. Journal of Virology, 74 (13), 5788-5795.
- Khramtsov, N. V., Woods, K. M., Nesterenko, M. V., Dykstra, C. C. & Upton, S. J. (1997). Virus-like, double-stranded RNAs in the parasitic protozoan Cryptosporidium parvum. Molecular Microbiology, 26 (2), 289-300.
- Kim, J. W., Chung, P. R., Hwang, M. K. & Choi, E. Y. (2007). Double-stranded RNA virus in Korean Isolate IH-2 of Trichomonas vaginalis. The Korean Journal of Parasitology, 45 (2), 87-94.
- King, A. M., Adams, M. J., Lefkowitz, E. J. & Carstens, E. B. (2012). Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Amsterdam: Elsevier.
- Kniel, K. E., Higgins, J. A., Trout, J. M., Fayer, R. & Jenkins, M. C. (2004). Characterization and potential use of a Cryptosporidium parvum virus (CPV) antigen for detecting C. parvum oocysts. Journal of Microbiological Methods, 58 (2), 189-195.
- Kniel, K. E. & Jenkins, M. C. (2005). Detection of Cryptosporidium parvum Oocysts on Fresh Vegetables and Herbs Using Antibodies Specific for a Cryptosporidium parvum Viral Antigen. Journal of Food Protection, 68 (5), 1093-1096.
- 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. Proceedings of the National Academy of Sciences, 114 (5), E811-E819.
- Lee, S., Fernando, M. A. & Nagy, E. (1996). dsRNA associated with virus-like particles in Eimeria spp. of the domestic fowl. Parasitology research, 82, 518-523.
- Leoni, F., Gallimore, C. I., Green, J. & McLauchlin, J. (2006). Characterisation of small double stranded RNA molecule in Cryptosporidium hominis, Cryptosporidium felis and Cryptosporidium meleagridis. Parasitology International, 55 (4), 299-306.
- Levin, I. I. & Parker, P. G. (2012). Haemosporidian Parasites: Impacts on Avian Hosts. R. E. Miller & M. E. Fowler (Edt.), Fowler’s Zoo and Wild Animal Medicine Current Therapy (7.baskı). Elsevier Saunders; Pp: 356.
- Lewis, D. (2014). Trichomoniasis. Medicine, 42 (7), 369-371.
- Mahmud, R., Lim, Y. A. L. & Amir, A. (2017). Hemoflagellates. Medical Parasitology. Cham: Springer; Pp: 32-38.
- Malla, N., Kaul, P., Sehgal, R. & Gupta, I. (2011). The presence of dsRNA virus in Trichomonas vaginalis isolates from symptomatic and asymptomatic Indian women and its correlation with in vitro metronidazole sensitivity. Indian Journal of Medical Microbiology, 29 (2), 152-157.
- Margulis, L. & Chapman, M. J. (2010). Kingdoms and Domains: An Illustrated Guide to the Phyla of Life on Earth. Academic Press, 493.
- Marucci, G., Zullino, I., Bertuccini, L., Camerini, S., Cecchetti, S., Pietrantoni, A., Casella, M., Vatta, P., Greenwood, A. D., Fiorillo, A. & Lalle, M. (2021). Re-Discovery of Giardiavirus: Genomic and Functional Analysis of Viruses from Giardia duodenalis Isolates. Biomedicines, 9 (6), 654.
- Masha, S. C., Cools, P., Crucitti, T., Sanders, E. J. & Vaneechoutte, M. (2017). Molecular typing of Trichomonas vaginalis isolates by actin gene sequence analysis and carriage of T. vaginalis viruses. Parasites & Vectors, 10 (1), 537.
- Monis, P. T., Caccio, S. M. & Andrew Thompson, R. C. (2009). Variation in Giardia: towards a taxonomic revision of the genus. Trends in Parasitology, 25 (2), 93-100.
- Nalçacı, M., Karakuş, M., Yılmaz, B., Demir, S., Özbilgin A., Özbel, Y. & Töz, S. (2019). Detection of Leishmania RNA virus 2 in Leishmania species from Turkey. Trans R Soc Trop Med Hyg, 113, 410-417.
- Nibert, M. L., Woods, K. M., Upton, S. J. & Ghabrial, S. A. (2009). Cryspovirus: a new genus of protozoan viruses in the family Partitiviridae. Archives of Virology, 154, 1959-1965.
- Provenzano, D., Khoshnan, A. & Alderete, J. F. (1997). Involvement of dsRNA virus in the protein composition and growth kinetics of host Trichomonas vaginalis. Archives of Virology, 142, 939-952.
- Pu, X., Li, X., Cao, L., Yue, K., Zhao, P., Wang, X., Li, J., Zhang, X., Zhang, N., Zhao, Z., Liang, M. & Gong, P. (2021). Giardia duodenalis Induces Proinflammatory Cytokine Production in Mouse Macrophages via TLR9-Mediated p38 and ERK Signaling Pathways. Frontiers in Cell and Developmental Biology, 1-12.
- Rahmanipour, M., Mohebali, M., Koosha, M., Kazemirad, E., Yasami-Khiabani, S., Mirjalali, H. & Hajjaran, H. (2022). Effect of Leishmania RNA virus 2 on virulence factors and cytokines gene expression in a human macrophage infected with Leishmania major: A preliminary study. Experimental Parasitology, 108459.
- Revets, H., Dekegel, D., Deleersnijder, W., De Jonckheere, J., Peeters, J., Leysen, E. & Hamers, R. (1989). Identification of virus-like particles in Eimeria stiedae. Molecular and Biochemical Parasitology, 36 (3), 209-215.
- Ro, Y. T., Scheffter, S. M. & Patterson, J. L. (1997). Hygromycin B resistance mediates elimination of Leishmania virus from persistently infected parasites. Journal of Virology, 71 (12), 8991-8998.
- Roditi, I., Wyler, T., Smith, N. & Braun, R. (1994). Virus-like particles in Eimeria nieschulzi are associated with multiple RNA segments. Molecular and Biochemical Parasitology, 63 (2), 275-282.
- Rodrigues, J. R., Roy, S. W. & Sehgal, R. N. (2022). Novel RNA viruses associated with avian haemosporidian parasites. Plos one, 17 (6), e0269881.
- Rodriguez, A. E., Estévez, J. O., Nevot, M. C., Barrios, A. & Florin-Christensen, M. (2018). M. Florin-Christensen ve L. Schnittger (Edt.), Parasitic Protozoa of Farm Animals and Pets, Cham: Springer; Pp: 287-307.
- Rivera, W. L., Justo, C. A. C., Diego, M. A. C. V. & Loyola, L. M. (2015). Detection and molecular characterization of double-stranded RNA viruses in Philippine Trichomonas vaginalis isolates. Journal of Microbiology Immunology and Infection, 50 (5), 669-676.
- Salman, T. & Dinçkal, Ç. (2022). Kanser ve İmmünoterapi. H. Koçdor, A. Pabuççuoğlu, F. Zihnioğlu ve F. Sağın (Edt.), Sağlık Biyoteknolojisi, (1.Baskı). Ankara. Pp: 78-84.
- Saura, A., Zakharova, A., Klocek, D., Gerasimov, E. S., Butenko, A., Macedo, D. H., Servienė, E., Zagirova, D., Meshcheryakova, A., Rogozin, I. B., Serva, S., Kostygov, A. Y. & Yurchenko, V. (2022). Elimination of LRVs elicits different responses in Leishmania spp. Msphere, 7 (4), e00335-22.
- Sepp, T., Wang, A. L. & Wang, C. C. (1993). Giardiavirus-Resistant Giardia lamblia Lacks a Virus Receptor on the Cell Membrane Surface. Journal of Virology, 68 (3), 1426-1431.
- Sevinç, F. & Dik, B. (2015). Cryptosporidiidae. N. Dumanlı ve Z. Karaer (Edt.), Veteriner Protozooloji (2.baskı). Ankara: Medisan Yayınevi; Pp: 125-126.
- Scheffter, S. M., Ro, Y. T., Chung, I. K. & Patterson, J. L. (1995). The complete sequence of Leishmania RNA virus LRV2-1, a virus of an Old World parasite strain. Virology, 212 (1), 84-90.
- Schurer, J. M., Mosites, E., Li, C., Meschke, S. & Rabinowitz, P. (2016). Community-based surveillance of zoonotic parasites in a ‘One Health’world: a systematic review. One Health, 2, 166-174.
- Shita, E. Y., Semegn, E. N., Wubetu, G. Y., Abitew, A. M., Andualem, B. G. & Alemneh, M. G. (2022). Prevalence of Leishmania RNA virus in Leishmania parasites in patients with tegumentary leishmaniasis: A systematic review and meta-analysis. PLOS Neglected Tropical Diseases, 16 (6), e0010427.
- Snipes, L. J., Gamard, P. M., Narcisi, E. M., Beard, C. B., Lehmann, T. & Secor, W. E. (2000). Molecular Epidemiology of Metronidazole Resistance in a Population of Trichomonas vaginalis Clinical Isolates. Journal of Clinical Microbiology, 38 (8), 3004-3009.
- Tai, J. H., Chang, S. C., Chou, C. F. & Ong, S. J. (1996). Separation and characterization of two related Giardiaviruses in the parasitic protozoan Giardia lamblia. Virology, 216 (1), 124-132.
- Tai, J. H. & Ip, C. F. (1995). The cDNA Sequence of Trichomonas vaginalis Virus-T1 Double-Stranded RNA. Virology, 206 (1), 773-776.
- Tai, L., Li, J., Yin, J., Zhang, N., Yang, J., Li, H., Yang, Z., Gong, P. & Zhang, X. (2019). A novel detection method of Cryptosporidium parvum infection in cattle based on Cryptosporidium parvum virus 1. Acta Biochim Biophys Sin, 51 (1), 104-111.
- Tai, J. H., Ong, S. J., Chang, S. C. & Su, H. M. (1993). Giardiavirus enters Giardia lamblia WB trophozoite via endocytosis. Experimental Parasitology, 76 (2), 165-174.
- Tarr, P. I., Aline, R. F., Smiley, B. L., Scholler, J. & Keithly, J. (1988). LR1: A candidate RNA virus of Leishmania. Proceedings of the National Academy of Sciences, 83, 9572-9575.
- Thu, T. T. T., Margarita, V., Cocco, A. R., Marongiu, Dessì, D., Rappelli, P. & Fiori, P. L., (2018). Trichomonas vaginalis Transports Virulent Mycoplasma hominis and Transmits the Infection to Human Cells after Metronidazole Treatment: A Potential Role in Bacterial Invasion of Fetal Membranes and Amniotic Fluid. Journal of Pregnancy.
- Valencia, B. M., Lau, R., Kariyawasam, R., Jara, M., Ramos, A. P., Chantry, M., Lana, J. T., Boggild, A. K. & Llanos-Cuentas, A. (2022). Leishmania RNA virus-1 is similarly detected among metastatic and non-metastatic phenotypes in a prospective cohort of American tegumentary leishmaniasis. PLOS Neglected Tropical Diseases, 16 (1), e0010162.
- Vong, M., Ludington, J. G., Ward, H. D. & Nibert, M. L. (2017). Complete cryspovirus genome sequences from Cryptosporidium parvum isolate Iowa. Archives of Virology, 162, 2875-2879.
- Wang, A. L., Miller, R. L. & Wang, C. C. (1988). Antibodies to the Giardia lamblia double-stranded RNA virus major protein can block the viral infection. Molecular and Biochemical Parasitology, 30 (3), 225-232.
- Wang, A. L. & Wang, C. C. (1985). A Linear Double-stranded RNA in Trichomonas vaginalis. The Journal of Biologycal Chemistry, 260 (6), 3697-3702.
- Wang, A. L. & Wang, C. C. (1986). Discovery of a specific double-stranded RNA virus in Giardia lamblia. Molecular and Biochemical Parasitology, 21, 269-276.
- Weber, B., Mapeka, T. M., Maahlo, M. A. & Hoosen, A. A. (2003). Double stranded RNA virus in South African Trichomonas vaginalis isolates. Journal of Clinical Pathology, 56 (7), 542-543.
- Wendel, K. A., Rompalo, A. M., Erbelding, E. J., Chang, T. H. & Alderete, J. F. (2002). Double-Stranded RNA Viral Infection of Trichomonas vaginalis Infecting Patients Attending a Sexually Transmitted Diseases Clinic. The Journal of Infectious Diseases, 186 (4), 558-561.
- Widmer, G. & Dooley, S. (1995). Phylogenetic analysis of Leishmania RNA virus and Leishmania suggests ancient virus-parasite association. Nucleic Acids Research, 23 (12), 2300-2304.
- Wu, B., Zhang, X., Gong, P., Li, M., Ding, H., Xin, C., Zhao, N. & Li, J. (2016). Eimeria tenella: A novel dsRNA virus in E. tenella and its complete genome sequence analysis. Virus Genes, 52, 244-252.
- Xin, C., Wu, B., Li, J., Gong, P., Yang, J., Li, H., Cai, X. & Zhang, X. (2016). Complete genome sequence and evolution analysis of Eimeria stiedai RNA virus 1, a novel member of the family Totiviridae. Arch Virol, 161, 3571-3576.
- Yaman, M. (2015). Phlebotominae (Kum Sinekleri). Z. Karaer ve N. Dumanlı (Edt.), Arthropodoloji. Ankara: Medisan Yayınevi; Pp:187.
- Yeşilbağ, K. (2010). Genel Viroloji. Malayta: Medipres Matbaacılık; Pp: 3-24.
- Yukarı, B. A. (2015). Entamoebidae, Hartmannellidae, Vahlkampfiidae. N. Dumanlı ve Z. Karaer (Edt.), Veteriner Protozooloji (2.baskı). Ankara: Medisan Yayınevi; Pp: 73.
- Zangger, H., Hailu, A., Desponds, C., Lye, L. F., Akopyants, N. S., Dobson, D. E., Ronet, C., Ghalib, H., Beverley, S. M. & Fasel, N. (2014). Leishmania aethiopica field isolates bearing an endosymbiontic dsRNA virus induce pro-inflammatory cytokine response. PLoS Neglected Tropical Diseases, 8 (4), e2836.
VIRAL ENDOSYMBIONTS OF PROTOZOA
Year 2023,
Volume: 14 Issue: 1, 25 - 35, 06.05.2023
Ayşegül Damlapınar
,
Kader Yıldız
Abstract
Viral endosymbionts and virus-like particles have been detected in some parasitic protozoans. The effect of them on protozoa and their role in the infection in the host is remarkable. There are some data on the contribution of viral endosymbionts to the pathogenicity of protozoa in the host. It is aimed to give information about viral endosymbionts in protozoa in the review.
References
- Adaui, V., Lye, L. F., Akopyants, N. S., Zimic, M., Llanos-Cuentas, A., Garcia, L., Maes, I., Doncker, S., Dobson, D. E., Arevalo, J., Dujardin, J. C. & Beverley, S. M. (2016). Association of the Endobiont Double-Stranded RNA Virus LRV1 With Treatment Failure for Human Leishmaniasis Caused by Leishmania braziliensis in Peru and Bolivia. The Journal of Infectious Diseases, 213, 112-121.
- Alderete, J. F., Wendel, K. A., Rompalo, A. M., Erbelding, E. J., Benchimol, M. & Chang, T. H. (2003). Trichomonas vaginalis: evaluating capsid proteins of dsRNA viruses and the dsRNA virus within patients attending a sexually transmitted disease clinic. Experimental Parasitology, 103, 44-50.
- Arslan, M. Ö. & Sarı, B. (2015). Eimeriidae (Coccidiosis). N. Dumanlı ve Z. Karaer (Edt.), Veteriner Protozooloji (2.baskı), Ankara: Medisan Yayınevi, 77
- Atayde, A. V., Filho, A. S. L., Chaparro, V., Zimmermann, A., Martel, C., Jaramillo, M. & Olivier, M. (2019). Nature Microbiology, 4, 714-723.
- Becker, D. L., Santos, O., Frasson, A. P., Rigo, G. V., Macedo, A. J. & Tasca, T. (2015). High rates of Double-Stranded RNA Viruses and Mycoplasma hominis in Trichomonas vaginalis Clinical Isolates in South Brazil. Infection, Genetics and Evolution, 34, 181-187.
- Benchimol, M., Monteiro, S. P., Chang, T. H. & Alderete, J. F. (2002). Virus in Trichomonas—an ultrastructural study. Parasitology International, 51 (3), 293- 298.
- Berber, E., Şimşek, E., Çanakoğlu, N., Sürsal, N. & Gençay-Göksu, A. (2021). Newly identified Cryptosporidium parvum virus-1 from newborn calf diarrhoea in Turkey. Transboundary and Emerging Diseases, 68 (4), 2571-2580.
- Boratto, P. V. M., Oliveira, G. P., Machado, T. B., Andrade, A. C. S. P., Baudoin, J. P., Klose, T., Schulz, F., Azza, S., Decloquemen, P., Chabrière, E., Colson, P., Levasseur, A., Scola, B. L. & Abrahao, J. S. (2020). Yaravirus: Bulaşan yeni bir 80-nm virüs Acanthamoeba castellanii. Proceedings of the National Academy of Sciences, 117 (28), 16579-16586.
- Cacho, E., Gallego, M., Montes., C., Lopez-Bernad, F., Quilez, J. & Sanchez-Acedo, C. (2001). Eimeria necatrix virus: intracellular localisation of viral particles and proteins. International Journal for Parasitology, 31, 1269-1274.
- Cadd, T. L., Keenan, M. C. & Patterson, J. L. (1993). Detection of Leishmania RNA virus 1 proteins. Journal of Virology, 67 (9), 5647-5650.
- Castiglioni, P., Hartley, M. A., Rossi, M., Prevel, F., Desponds, C., Utzschneider, D. T., Eren, R. O., Zangger, H., Brunner, L., Collin, N., Zehn, D., Kuhlmann, F. M., Beverley, S. M., Fasel, N. & Ronet., C. (2017). Exacerbated Leishmaniasis Caused by a Viral Endosymbiont can be Prevented by Immunization with Its Viral Capsid. Plos Neglected Tropical Diseases, 11 (1), e0005240.
- Charon, J., Grigg, M J., Eden, J. S., Piera, K. A., Rana, H., William, T., Rose, K., Davenport, M. P., Anstey, N. M. & Holmes, E. C. (2019). Novel RNA viruses associated with Plasmodium vivax in human malaria and Leucocytozoon parasites in avian disease. PLOS Pathogens, 15 (12), e1008216.
- Diamond, L. S. & Mattern, C. F. T. (1976). Protozoal Viruses. Advances in Virus Research, 20, 87-112.
- El-Gayar, E. K., Mokhtar, A. B. & Hassan, W. A. (2016). Molecular characterization of double-stranded RNA virus in Trichomonas vaginalis Egyptian isolates and its association with pathogenicity. Parasitology Research, 115 (10), 4027-4036.
- Ellis, J. & Revets, H. (1990). Eimeria species which infect the chicken contain virus-like RNA molecules. Parasitology, 101 (2), 163.
- Eren, R. O., Reverte, M., Rossi, M., Hartley, M. A., Castiglioni, P., Prevel, F., Martin, R., Desponds, C., Lye, L. F., Drexler, S. K., Reith, W., Beverley, S. M., Ronet, C. & Fasel, N. (2016). Mammalian Innate Immune Response to a Leishmania-Resident RNA Virus Increases Macrophage Survival to Promote Parasite Persistence. Cell Host & Microbe, 20 (3), 318-328.
- Ertabaklar, H., Malatyalı, E., Özün-Özbay, E. P., Yıldız, İ., Sinecen, M., Ertuğ, S., Bozdoğan, B. & Güçlü, Ö. (2021). Microsatellite-Based Genotyping, Analysis of Population Structure, Presence of Trichomonas vaginalis Virus (TVV) and Mycoplasma hominis in T. vaginalis Isolates from Southwest of Turkey. Iranian Journal of Parasitology, 16 (1), 81-90.
- Fichorova, R. N., Lee, Y., Yamamoto, H. S., Takagi, Y., Hayes, G. R., Goodman, R.P., Chepa-Lotrea, X, Buck, O. R., Murray, R., Kula, T., Beach., D. H., Singh, B. N. & Nibert., M. L. (2012). Endobiont Viruses Sensed by the Human Host–Beyond Conventional Antiparasitic Therapy. Plos One, 7 (11), e48418.
- Fraga, J., Rojas, L., Sariego, I. & Fernández-Calienes, A. (2012). Genetic characterization of three Cuban Trichomonas vaginalis virus. Phylogeny of Totiviridae family. Infection, Genetics and Evolution, 12 (1), 113-120.
- Fraga, J., Rojas, L., Sariego, I. & Fernández-Calienes, A. & Núñez, F. A, (2007). Double-Stranded RNA Viral Infection of Trichomonas vaginalis and Association with Clinical Presentation. Acta Parasitologica, 46, 93-98.
- Garnham, P. C. C., Bird, R. G. & Baker, J. R. (1962). Electron microscope studies of motile stages of malaria parasites: III. The ookinetes of Haemamoeba and Plasmodium. Trans R Soc Trop Med Hyg, 56 (2), 116-120.
- Gong, P., Li, X., Wu, W., Cao, L., Zhao, P., Li, X., Ren, B., Li, J. & Zhang, X. (2020). A novel microRNA from the translated region of the Giardiavirus rdrp gene governs virus copy number in Giardia duodenalis. Frontiers in Microbiology, 11, 569412.
- Guilbride, L., Myler, P. J. & Stuart, K. (1992). Distribution and sequence divergence of LRV1 viruses among different Leishmania species. Mol Biochem Parasitol, 54 (1), 101-104.
- Gündoğdu, A. & Ulu-Kılıç, A. (2018). Bakteriyofaj Terapisi: Unutulmuş Bir Şifa Kaynağı. Klimik Dergisi, 31 (2), 78-87.
- Hajjaran, H., Mahdi, M., Mohebali, M., Samimi-Rad, K., Ataei-Pirkooh, A., Kazemi-Rad, E., Naddaf, S. R. & Raoofian, R. (2016). Detection and molecular identification of Leishmania RNA virus (LRV) in Iranian Leishmania species. Archives of Virology, 161 (12), 3385-3390.
- Han, Q., Li, J., Gong, P., Gai, J., Li, S. & Zhang, X. (2011). Virus-like particles in Eimeria tenella are associated with multiple RNA segments. Experimental Parasitology, 127, 646-650.
- Hartley, M. A., Bourreau, E., Rossi, M., Castiglioni, P., Eren, R. O., Prevel, F., Couppié, P., Hickerson, S. M., Launois, P., Beverley, S. M., Ronet, C. & Fasel, F. (2016). Leishmaniavirus-DependentMetastatic LeishmaniasisIs Prevented by Blocking IL-17A. Plos Pathogens, 12 (9), e1005852.
- He, D., Pengtao, G., Ju, Y., Jianhua, L., He, L., Guocai, Z. & Xichen, Z. (2017). Differential Protein Expressions in Virus-Infected and Uninfected Trichomonas vaginalis. The Korean Journal of Parasitol, 55 (2), 121-128.
- Heidary, S., Bandehpour, M., Valadkhani, Z., Seyyed –Tabaee, S. J., Haghigh, A., Abadi, A. R. & Kazemi, B. (2013). Double-Stranded RNA Viral Infection in Tehran Trichomonas vaginalis Isolates. Iranian Journal of Parasitology, 8 (1), 60-64.
- Hillman, B. I. & Cohen A. B., (2021). Totiviruses (Totiviridae). Encyclopedia of Virology (4.baskı), Academic Press; Pp: 648-657.
- International Committee on Taxonomy of Viruses (2022). https://ictv.global/taxonomy/taxondetails?taxnode_id=202112530 (Erişim: 20.12.2022).
- Jenkins, M. C., Higgins, J., Abrahante, J. E., Kniel, K. E., O’Brien, C., Trout, J., Lancto, C. A., Abrahamsen, M. S. & Fayer, R. (2008). Fecundity of Cryptosporidium parvum is correlated with intracellular levels of the viral symbiont CPV. International Journal for Parasitology, 38, 1051-1055.
- Jenkins, M. C., O’Brien, C. N. & Fayer, R. (2015). Changes in the levels of Cryspovirus during in vitro development of Cryptosporidium parvum. Parasitology Research, 114, 2063-2068.
- Jonckheere, J. F. & Gordts, B. (1987). Occurrence and transfection of a Giardia virus. Molecular and Biochemical Parasitology, 23 (1), 85-89.
- Kar, S., Güven, E. & Karaer, Z. (2015). Hexamitidae. Genel Protozooloji. N. Dumanlı ve Z. Karaer (Edt.), Veteriner Protozooloji (2.baskı), 45-51. Ankara: Medisan Yayınevi.
- Karaer, Z. & Nalbantoğlu, S. (2015). Trypanosomatidae. N. Dumanlı ve Z. Karaer (Edt.), Veteriner Protozooloji (2.baskı), Ankara: Medisan Yayınevi; Pp: 35-42.
- Keen, E. C. (2013). Beyond phage therapy: Virotherapy of protozoal diseases. Future Microbiology, 8 (7), 821-823.
- Khanaliha, K., Masoumi-Asl, H., Bokharaei-Salim, F., Tabatabaei, A. & Naghdalipoor, M. (2017). Double-stranded RNA viral infection of Trichomonas vaginalis (TVV1) in Iranian isolates. Microbial Pathogenesis, 109, 56-60.
- Khoshnan, A. & Alderete, J. F. (1994). Trichomonas vaginalis with a double-stranded RNA virus has upregulated levels of phenotypically variable immunogen mRNA. Journal of Virology, 68 (6), 4035-4038.
- Khramtsov, N. V. & Upton, S. J. (2000). Association of RNA polymerase complexes of the parasitic protozoan Cryptosporidium parvum with virus-like particles: heterogeneous system. Journal of Virology, 74 (13), 5788-5795.
- Khramtsov, N. V., Woods, K. M., Nesterenko, M. V., Dykstra, C. C. & Upton, S. J. (1997). Virus-like, double-stranded RNAs in the parasitic protozoan Cryptosporidium parvum. Molecular Microbiology, 26 (2), 289-300.
- Kim, J. W., Chung, P. R., Hwang, M. K. & Choi, E. Y. (2007). Double-stranded RNA virus in Korean Isolate IH-2 of Trichomonas vaginalis. The Korean Journal of Parasitology, 45 (2), 87-94.
- King, A. M., Adams, M. J., Lefkowitz, E. J. & Carstens, E. B. (2012). Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Amsterdam: Elsevier.
- Kniel, K. E., Higgins, J. A., Trout, J. M., Fayer, R. & Jenkins, M. C. (2004). Characterization and potential use of a Cryptosporidium parvum virus (CPV) antigen for detecting C. parvum oocysts. Journal of Microbiological Methods, 58 (2), 189-195.
- Kniel, K. E. & Jenkins, M. C. (2005). Detection of Cryptosporidium parvum Oocysts on Fresh Vegetables and Herbs Using Antibodies Specific for a Cryptosporidium parvum Viral Antigen. Journal of Food Protection, 68 (5), 1093-1096.
- 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. Proceedings of the National Academy of Sciences, 114 (5), E811-E819.
- Lee, S., Fernando, M. A. & Nagy, E. (1996). dsRNA associated with virus-like particles in Eimeria spp. of the domestic fowl. Parasitology research, 82, 518-523.
- Leoni, F., Gallimore, C. I., Green, J. & McLauchlin, J. (2006). Characterisation of small double stranded RNA molecule in Cryptosporidium hominis, Cryptosporidium felis and Cryptosporidium meleagridis. Parasitology International, 55 (4), 299-306.
- Levin, I. I. & Parker, P. G. (2012). Haemosporidian Parasites: Impacts on Avian Hosts. R. E. Miller & M. E. Fowler (Edt.), Fowler’s Zoo and Wild Animal Medicine Current Therapy (7.baskı). Elsevier Saunders; Pp: 356.
- Lewis, D. (2014). Trichomoniasis. Medicine, 42 (7), 369-371.
- Mahmud, R., Lim, Y. A. L. & Amir, A. (2017). Hemoflagellates. Medical Parasitology. Cham: Springer; Pp: 32-38.
- Malla, N., Kaul, P., Sehgal, R. & Gupta, I. (2011). The presence of dsRNA virus in Trichomonas vaginalis isolates from symptomatic and asymptomatic Indian women and its correlation with in vitro metronidazole sensitivity. Indian Journal of Medical Microbiology, 29 (2), 152-157.
- Margulis, L. & Chapman, M. J. (2010). Kingdoms and Domains: An Illustrated Guide to the Phyla of Life on Earth. Academic Press, 493.
- Marucci, G., Zullino, I., Bertuccini, L., Camerini, S., Cecchetti, S., Pietrantoni, A., Casella, M., Vatta, P., Greenwood, A. D., Fiorillo, A. & Lalle, M. (2021). Re-Discovery of Giardiavirus: Genomic and Functional Analysis of Viruses from Giardia duodenalis Isolates. Biomedicines, 9 (6), 654.
- Masha, S. C., Cools, P., Crucitti, T., Sanders, E. J. & Vaneechoutte, M. (2017). Molecular typing of Trichomonas vaginalis isolates by actin gene sequence analysis and carriage of T. vaginalis viruses. Parasites & Vectors, 10 (1), 537.
- Monis, P. T., Caccio, S. M. & Andrew Thompson, R. C. (2009). Variation in Giardia: towards a taxonomic revision of the genus. Trends in Parasitology, 25 (2), 93-100.
- Nalçacı, M., Karakuş, M., Yılmaz, B., Demir, S., Özbilgin A., Özbel, Y. & Töz, S. (2019). Detection of Leishmania RNA virus 2 in Leishmania species from Turkey. Trans R Soc Trop Med Hyg, 113, 410-417.
- Nibert, M. L., Woods, K. M., Upton, S. J. & Ghabrial, S. A. (2009). Cryspovirus: a new genus of protozoan viruses in the family Partitiviridae. Archives of Virology, 154, 1959-1965.
- Provenzano, D., Khoshnan, A. & Alderete, J. F. (1997). Involvement of dsRNA virus in the protein composition and growth kinetics of host Trichomonas vaginalis. Archives of Virology, 142, 939-952.
- Pu, X., Li, X., Cao, L., Yue, K., Zhao, P., Wang, X., Li, J., Zhang, X., Zhang, N., Zhao, Z., Liang, M. & Gong, P. (2021). Giardia duodenalis Induces Proinflammatory Cytokine Production in Mouse Macrophages via TLR9-Mediated p38 and ERK Signaling Pathways. Frontiers in Cell and Developmental Biology, 1-12.
- Rahmanipour, M., Mohebali, M., Koosha, M., Kazemirad, E., Yasami-Khiabani, S., Mirjalali, H. & Hajjaran, H. (2022). Effect of Leishmania RNA virus 2 on virulence factors and cytokines gene expression in a human macrophage infected with Leishmania major: A preliminary study. Experimental Parasitology, 108459.
- Revets, H., Dekegel, D., Deleersnijder, W., De Jonckheere, J., Peeters, J., Leysen, E. & Hamers, R. (1989). Identification of virus-like particles in Eimeria stiedae. Molecular and Biochemical Parasitology, 36 (3), 209-215.
- Ro, Y. T., Scheffter, S. M. & Patterson, J. L. (1997). Hygromycin B resistance mediates elimination of Leishmania virus from persistently infected parasites. Journal of Virology, 71 (12), 8991-8998.
- Roditi, I., Wyler, T., Smith, N. & Braun, R. (1994). Virus-like particles in Eimeria nieschulzi are associated with multiple RNA segments. Molecular and Biochemical Parasitology, 63 (2), 275-282.
- Rodrigues, J. R., Roy, S. W. & Sehgal, R. N. (2022). Novel RNA viruses associated with avian haemosporidian parasites. Plos one, 17 (6), e0269881.
- Rodriguez, A. E., Estévez, J. O., Nevot, M. C., Barrios, A. & Florin-Christensen, M. (2018). M. Florin-Christensen ve L. Schnittger (Edt.), Parasitic Protozoa of Farm Animals and Pets, Cham: Springer; Pp: 287-307.
- Rivera, W. L., Justo, C. A. C., Diego, M. A. C. V. & Loyola, L. M. (2015). Detection and molecular characterization of double-stranded RNA viruses in Philippine Trichomonas vaginalis isolates. Journal of Microbiology Immunology and Infection, 50 (5), 669-676.
- Salman, T. & Dinçkal, Ç. (2022). Kanser ve İmmünoterapi. H. Koçdor, A. Pabuççuoğlu, F. Zihnioğlu ve F. Sağın (Edt.), Sağlık Biyoteknolojisi, (1.Baskı). Ankara. Pp: 78-84.
- Saura, A., Zakharova, A., Klocek, D., Gerasimov, E. S., Butenko, A., Macedo, D. H., Servienė, E., Zagirova, D., Meshcheryakova, A., Rogozin, I. B., Serva, S., Kostygov, A. Y. & Yurchenko, V. (2022). Elimination of LRVs elicits different responses in Leishmania spp. Msphere, 7 (4), e00335-22.
- Sepp, T., Wang, A. L. & Wang, C. C. (1993). Giardiavirus-Resistant Giardia lamblia Lacks a Virus Receptor on the Cell Membrane Surface. Journal of Virology, 68 (3), 1426-1431.
- Sevinç, F. & Dik, B. (2015). Cryptosporidiidae. N. Dumanlı ve Z. Karaer (Edt.), Veteriner Protozooloji (2.baskı). Ankara: Medisan Yayınevi; Pp: 125-126.
- Scheffter, S. M., Ro, Y. T., Chung, I. K. & Patterson, J. L. (1995). The complete sequence of Leishmania RNA virus LRV2-1, a virus of an Old World parasite strain. Virology, 212 (1), 84-90.
- Schurer, J. M., Mosites, E., Li, C., Meschke, S. & Rabinowitz, P. (2016). Community-based surveillance of zoonotic parasites in a ‘One Health’world: a systematic review. One Health, 2, 166-174.
- Shita, E. Y., Semegn, E. N., Wubetu, G. Y., Abitew, A. M., Andualem, B. G. & Alemneh, M. G. (2022). Prevalence of Leishmania RNA virus in Leishmania parasites in patients with tegumentary leishmaniasis: A systematic review and meta-analysis. PLOS Neglected Tropical Diseases, 16 (6), e0010427.
- Snipes, L. J., Gamard, P. M., Narcisi, E. M., Beard, C. B., Lehmann, T. & Secor, W. E. (2000). Molecular Epidemiology of Metronidazole Resistance in a Population of Trichomonas vaginalis Clinical Isolates. Journal of Clinical Microbiology, 38 (8), 3004-3009.
- Tai, J. H., Chang, S. C., Chou, C. F. & Ong, S. J. (1996). Separation and characterization of two related Giardiaviruses in the parasitic protozoan Giardia lamblia. Virology, 216 (1), 124-132.
- Tai, J. H. & Ip, C. F. (1995). The cDNA Sequence of Trichomonas vaginalis Virus-T1 Double-Stranded RNA. Virology, 206 (1), 773-776.
- Tai, L., Li, J., Yin, J., Zhang, N., Yang, J., Li, H., Yang, Z., Gong, P. & Zhang, X. (2019). A novel detection method of Cryptosporidium parvum infection in cattle based on Cryptosporidium parvum virus 1. Acta Biochim Biophys Sin, 51 (1), 104-111.
- Tai, J. H., Ong, S. J., Chang, S. C. & Su, H. M. (1993). Giardiavirus enters Giardia lamblia WB trophozoite via endocytosis. Experimental Parasitology, 76 (2), 165-174.
- Tarr, P. I., Aline, R. F., Smiley, B. L., Scholler, J. & Keithly, J. (1988). LR1: A candidate RNA virus of Leishmania. Proceedings of the National Academy of Sciences, 83, 9572-9575.
- Thu, T. T. T., Margarita, V., Cocco, A. R., Marongiu, Dessì, D., Rappelli, P. & Fiori, P. L., (2018). Trichomonas vaginalis Transports Virulent Mycoplasma hominis and Transmits the Infection to Human Cells after Metronidazole Treatment: A Potential Role in Bacterial Invasion of Fetal Membranes and Amniotic Fluid. Journal of Pregnancy.
- Valencia, B. M., Lau, R., Kariyawasam, R., Jara, M., Ramos, A. P., Chantry, M., Lana, J. T., Boggild, A. K. & Llanos-Cuentas, A. (2022). Leishmania RNA virus-1 is similarly detected among metastatic and non-metastatic phenotypes in a prospective cohort of American tegumentary leishmaniasis. PLOS Neglected Tropical Diseases, 16 (1), e0010162.
- Vong, M., Ludington, J. G., Ward, H. D. & Nibert, M. L. (2017). Complete cryspovirus genome sequences from Cryptosporidium parvum isolate Iowa. Archives of Virology, 162, 2875-2879.
- Wang, A. L., Miller, R. L. & Wang, C. C. (1988). Antibodies to the Giardia lamblia double-stranded RNA virus major protein can block the viral infection. Molecular and Biochemical Parasitology, 30 (3), 225-232.
- Wang, A. L. & Wang, C. C. (1985). A Linear Double-stranded RNA in Trichomonas vaginalis. The Journal of Biologycal Chemistry, 260 (6), 3697-3702.
- Wang, A. L. & Wang, C. C. (1986). Discovery of a specific double-stranded RNA virus in Giardia lamblia. Molecular and Biochemical Parasitology, 21, 269-276.
- Weber, B., Mapeka, T. M., Maahlo, M. A. & Hoosen, A. A. (2003). Double stranded RNA virus in South African Trichomonas vaginalis isolates. Journal of Clinical Pathology, 56 (7), 542-543.
- Wendel, K. A., Rompalo, A. M., Erbelding, E. J., Chang, T. H. & Alderete, J. F. (2002). Double-Stranded RNA Viral Infection of Trichomonas vaginalis Infecting Patients Attending a Sexually Transmitted Diseases Clinic. The Journal of Infectious Diseases, 186 (4), 558-561.
- Widmer, G. & Dooley, S. (1995). Phylogenetic analysis of Leishmania RNA virus and Leishmania suggests ancient virus-parasite association. Nucleic Acids Research, 23 (12), 2300-2304.
- Wu, B., Zhang, X., Gong, P., Li, M., Ding, H., Xin, C., Zhao, N. & Li, J. (2016). Eimeria tenella: A novel dsRNA virus in E. tenella and its complete genome sequence analysis. Virus Genes, 52, 244-252.
- Xin, C., Wu, B., Li, J., Gong, P., Yang, J., Li, H., Cai, X. & Zhang, X. (2016). Complete genome sequence and evolution analysis of Eimeria stiedai RNA virus 1, a novel member of the family Totiviridae. Arch Virol, 161, 3571-3576.
- Yaman, M. (2015). Phlebotominae (Kum Sinekleri). Z. Karaer ve N. Dumanlı (Edt.), Arthropodoloji. Ankara: Medisan Yayınevi; Pp:187.
- Yeşilbağ, K. (2010). Genel Viroloji. Malayta: Medipres Matbaacılık; Pp: 3-24.
- Yukarı, B. A. (2015). Entamoebidae, Hartmannellidae, Vahlkampfiidae. N. Dumanlı ve Z. Karaer (Edt.), Veteriner Protozooloji (2.baskı). Ankara: Medisan Yayınevi; Pp: 73.
- Zangger, H., Hailu, A., Desponds, C., Lye, L. F., Akopyants, N. S., Dobson, D. E., Ronet, C., Ghalib, H., Beverley, S. M. & Fasel, N. (2014). Leishmania aethiopica field isolates bearing an endosymbiontic dsRNA virus induce pro-inflammatory cytokine response. PLoS Neglected Tropical Diseases, 8 (4), e2836.