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Entomological Review

, Volume 98, Issue 9, pp 1369–1378 | Cite as

The Ability of Ixodid Ticks (Acari: Ixodidae) to Support Reproduction of the Tick-Borne Encephalitis Virus

  • O. A. BelovaEmail author
  • I. S. Kholodilov
  • A. G. Litov
  • G. G. Karganova
Article
  • 9 Downloads

Abstract

Reproduction dynamics and phenotypic changes in the tick-borne encephalitis virus (TBEV) population during long-term infection, feeding of ixodid ticks, and at different temperatures were studied. The temperature significantly influenced the level of TBEV reproduction in ixodid ticks. However, more rapid and intensive TBEV reproduction was observed in feeding ticks as compared with infected ticks kept at elevated (32–37°C) and room temperatures. TBEV strains of the European and Siberian subtypes successfully replicated and formed long-term infection in ticks that are both primary (Ixodes ricinus, I. persulcatus) and secondary (Dermacentor reticulatus) virus vectors. The strain of the Siberian subtype reached its maximum titers in D. reticulatus, and the strain of the European subtype, in I. ricinus and D. reticulatus. Prolonged reproduction of the European and Siberian TBEV subtypes in both primary and secondary vectors increased heterogeneity of the virus population; however, virus variants retained high neuroinvasiveness characteristic of the virus adapted to mouse CNS cells. TBEV strains of different subtypes varied in the phenotypic population heterogeneity under different conditions. Unlike Absettarov (European subtype) strain, the population heterogeneity of EK-328 (Siberian subtype) strain by the plaque phenotype on PEK cell culture was significantly influenced by feeding of D. reticulatus ticks after long-term reproduction of the virus in them.

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References

  1. 1.
    Balashov, Yu.S., Ixodid Ticks as Parasites and Infection Vectors (Nauka, St. Petersburg, 1998) [in Russian].Google Scholar
  2. 2.
    Belova, O.A., Burenkova, L.A., and Karganova, G.G., “Different Tick-Borne Encephalitis Virus (TBEV) Prevalences in Unfed versus Partially Engorged Ixodid Ticks–Evidence of Virus Replication and Changes in Tick Behavior,” Ticks and Tick-Borne Diseases 3, 240–246 (2012).CrossRefGoogle Scholar
  3. 3.
    Belova, O.A., Kholodilov, I.S., and Karganova, G.G., “Neuroinvasiveness of Tick-Borne Encephalitis Virus Variants Adapted to Ixodid Ticks,” Sovremennye Problemy Nauki i Obrazovaniya 5: 21883 (2015). https://doi.org/www.science-education.ru/128-21883.Google Scholar
  4. 4.
    Belova, O.A., Litov, A.G., Kholodilov, I.S., Kozlovskaya, L.I., Bell-Sakyi, L., Romanova, L.Iu., and Karganova, G.G., “Properties of the Tick-Borne Encephalitis Virus Population during Persistent Infection of Ixodid Ticks and Tick Cell Lines,” Ticks and Tick-Borne Diseases 8 (6), 895–906 (2017).CrossRefGoogle Scholar
  5. 5.
    Benda, R., “The Common Tick Ixodes ricinus as Reserve Host and Vector of Tick-Borne Encephalitis Virus. II. Experimental Transition of Encephalitis to Laboratory Animals by Different Stages of Ticks,” Zhurnal Gigieny, Epidemiologii, Mikrobiologii i Immunologii (Prague) 2, 467–480 (1958).Google Scholar
  6. 6.
    Chunikhin, S.P. and Kurenkov, V.B., “Reproduction Dynamics of the Tick-Borne Encephalitis Virus in Hyalomma plumbeum Ticks,” Meditsinskaya Parazitologiya i Parazitarnye Bolezni 49 (2), 25–27 (1980).Google Scholar
  7. 7.
    Chunikhin, S.P., Kurenkov, V.B., Dzhivanian, T.I., and Ryltseva, E.V., “Characteristics of Transphasic and Transmissive Passage of Tick-Borne Encephalitis Virus Strains with Varying Degree of Pathogenicity for Mice,” Meditsinskaya Parazitologiya i Parazitarnye Bolezni 48 (2), 61–65 (1979).Google Scholar
  8. 8.
    Chunikhin, S.P., Alekseev, A.N., and Reshetnikov, I.A., “Determining the Tick-Borne Encephalitis Virus Titer in the Saliva of Unfed Ixodid Ticks,” Meditsinskaya Parazitologiya i Parazitarnye Bolezni, No. 3, 89–91 (1988).Google Scholar
  9. 9.
    Dzhivanian, T.I., Chunikhin, S.P., Lisak, V.M., Kashtanova, G.M., and Korolev, M.B., “Immunochemical Characteristics of Antigenes from Tick-Borne Encephalitis Virus Variants Adapted to Hyalomma plumbeum Ticks,” Voprosy Virusologii, No. 1, 92–96 (1986).Google Scholar
  10. 10.
    Dzhivanian, T.I., Korolev, M.B., Karganova, G.G., Lisak, V.M., Kashtanova, G.M., and Chuprinskaya, M.V., “Changes in Host-Related Characteristics of the Tick-Borne Encephalitis Virus during Its Adaptation to Ixodid Ticks and Subsequent Readaptation to White Mice,” Voprosy Virusologii, No. 5, 589–595 (1988).Google Scholar
  11. 11.
    Dzhivanian, T.I., Karganova, G.G., Sobolev, S.G., Korolev, M.B., Kashtanova, G.M., Chuprinskaya, M.V., and Lashkevich, V.A., “Properties of Particles Formed during in vitro Reproduction of Tick-Borne Encephalitis Virus Adapted to H. plumbeum Ticks,” Voprosy Virusologii, No. 4, 297–300 (1991).Google Scholar
  12. 12.
    Khasnatinov, M.A., Ustanikova, K., Frolova, T.V., Pogodina, V.V., Bochkova, N.G., Levina, L.S., Slovak, M., Kazimirova, M., Labuda, M., Klempa, B., Eleckova, E., Gould, E.A., and Gritsun, T.S., “Non-Hemagglutinating Flaviviruses: Molecular Mechanisms for the Emergence of New Strains via Adaptation to European Ticks,” PLoS One 4 (10): e7295 (2009).Google Scholar
  13. 13.
    Korenberg, E.I. and Pchelkina, A.A., “Tick-Borne Encephalitis Virus Titers in Engorged Adult Ixodes persulcatus Ticks,” Parazitologiya 28 (2), 123–127 (1984).Google Scholar
  14. 14.
    Kozlovskaya, L.I., Osolodkin, D.I., Shevtsova, A.S., Romanova, L.Iu., Rogova, Y.V., Dzhivanian, T.I., Lyapustin, V.N., Pivanova, G.P., Gmyl, A.P., Palyulin, V.A., and Karganova, G.G., “GAG-Binding Variants of Tick-Borne Encephalitis Virus,” Virology 398 (2), 262–272 (2010).CrossRefGoogle Scholar
  15. 15.
    Kožuch, O. and Nosek, J., “Experimental Transmission of Tick-Borne Encephalitis (TBE) Virus by Haemaphysalis concinna Ticks,” Acta Virologica 24 (5), 377 (1980).Google Scholar
  16. 16.
    Lawrie, C.H., Uzcátegui, N.Y., Armesto, M., Bell-Sakyi, L., and Gould, E.A., “Susceptibility of Mosquito and Tick Cell Lines to Infection with Various Flaviviruses,” Medical and Veterinary Entomology 18 (3), 268–274 (2004).CrossRefGoogle Scholar
  17. 17.
    Lorenz, R.J. and Bogel, K., “Methods of Calculation,” in Laboratory Techniques in Rabies, 3rd Edition, Ed. by Kaplan, M.M. and Koprowski, H. (World Health Organization, Geneva, 1973), pp. 321–335.Google Scholar
  18. 18.
    Mishaeva, N.P. and Erofeeva, N.I., “Effect of Diapause of the Ticks Ixodes ricinus (Ixodidae) on Reproduction of the Tick-Borne Encephalitis Virus,” Parazitologiya 13 (3), 218–222 (1979).Google Scholar
  19. 19.
    Mishaeva, N.P. and Votyakov, V.I., “The Reproduction Balance of the Tick-Borne Encephalitis Virus in Ixodid Ticks and Vertebrates under the Conditions of Immunological Adaptation of the Host Organism to Arthropod Salivary Antigens,” in Ecology of Viruses (Moscow, 1982), pp. 40–45 [in Russian].Google Scholar
  20. 20.
    Nelzina, E.N., The Tropical Rat Mite (Moscow, 1950) [in Russian].Google Scholar
  21. 21.
    Nosek, J. and Kožuch, O., “Replication of Tick-Borne Encephalitis (TBE) Virus in Ticks Dermacentor marginatus,” Angewandte Parasitologie 26 (2), 97–101 (1985).Google Scholar
  22. 22.
    Nosek, J., Chunikhin, S.P., Gresíková, M., Korolev, M., Kožuch, O., Stefutkina, L.F., and Ivannikova, T.I., “Peculiarities of Tick-Borne Encephalitis Virus Reproduction in Haemaphysalis inermis Ticks and Their Explants,” Acta Virologica 30 (5), 396–401 (1986).Google Scholar
  23. 23.
    Nuttall, P.A., Jones, L.D., Labuda, M., and Kaufman, W., “Adaptations of Arboviruses to Ticks,” Journal of Medical Entomology 31 (1), 1–9 (1994).CrossRefGoogle Scholar
  24. 24.
    Rajcáni, J., Nosek, J., Kožuch, O., and Waltinger, H., “Reaction of the Host to the Tick-Bite. II. Distribution of Tick Borne Encephalitis Virus in Sucking Ticks,” Zentralblatt für Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene. 1. Abt. Medizinisch-Hygienische Bakteriologie, Virusforschung und Parasitologie. Originale 236 (1), 1–9 (1976).Google Scholar
  25. 25.
    Romanova, L.Iu., Gmyl, A.P., Dzhivanian, T.I., Bakhmutov, D.V., Lukashev, A.N., Gmyl, L.V., Rumyantsev, A.A., Burenkova, L.A., Lashkevich, V.A., and Karganova, G.G., “Microevolution of Tick-Borne Encephalitis Virus in Course of Host Alternation,” Virology 36 (2), 75–84 (2007).CrossRefGoogle Scholar
  26. 26.
    Růzek, D., Bell-Sakyi, L., Kopecký, J., and Grubhoffer, L., “Growth of Tick-Borne Encephalitis Virus (European Subtype) in Cell Lines from Vector and Non-Vector Ticks,” Virus Research 137 (1), 142–146 (2008).CrossRefGoogle Scholar
  27. 27.
    Šenigl, F., Kopecký, J., and Grubhoffer, L., “Distribution of E and NS1 Proteins of TBE Virus in Mammalian and Tick Cells,” Folia Microbiologica 49, 213–216 (2004).CrossRefGoogle Scholar
  28. 28.
    Šenigl, F., Grubhoffer, L., and Kopecký, J., “Differences in Maturation of Tick-Borne Encephalitis Virus in Mammalian and Tick Cell Line,” Intervirology 49 (4), 239–248 (2006).CrossRefGoogle Scholar
  29. 29.
    Slovák, M., Kazimírová, M., Siebenstichová, M., Ustaníková, K., Klempa, B., Gritsun, T., Gould, E.A., and Nuttall, P.A., “Survival Dynamics of Tick-Borne Encephalitis Virus in Ixodes ricinus Ticks,” Ticks and Tick-Borne Diseases 5 (6), 962–969 (2014).CrossRefGoogle Scholar
  30. 30.
    Stefutkina, L.F., Candidate’s Dissertation in Medical Sciences (Moscow, 1989).Google Scholar

Copyright information

© Pleiades Publishing, Inc. 2018

Authors and Affiliations

  • O. A. Belova
    • 1
    • 2
    Email author
  • I. S. Kholodilov
    • 1
  • A. G. Litov
    • 1
    • 3
  • G. G. Karganova
    • 1
    • 4
  1. 1.Chumakov Federal Scientific Center for Research and Development of Immunobiological ProductsRussian Academy of SciencesMoscowRussia
  2. 2.Martsinovsky Institute of Medical Parasitology, Tropical and Vector-Borne DiseasesSechenov Moscow State Medical UniversityMoscowRussia
  3. 3.Faculty of BiologyLomonosov Moscow State UniversityMoscowRussia
  4. 4.Sechenov Moscow State Medical UniversityMoscowRussia

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