Skip to main content
Log in

Historical Isolates of Semliki Forest and Chikungunya Viruses and Their Virological Characteristic, Whole-Genome Sequences, and Phylogeny

  • EXPERIMENTAL PAPERS
  • Published:
Molecular Genetics, Microbiology and Virology Aims and scope Submit manuscript

Abstract

The purpose of the study was to analyze alphavirus isolates collected in Uganda and Tanzania in the period preceding their global spread dating back to the middle of the last century. We supposed that analysis of their genomes could help to learn more about the specific features and the direction of molecular evolution of alphaviruses in the modern world. Archival samples of Chikungunya (CHIKV) and Semliki Forest (SFV) viruses were revived by cultivation in the Vero E6 cells. Isolates were identified by RT-PCR followed by sequencing. Whole genome sequences were obtained by NGS and used for phylogenetic analysis. The presence of two representatives of the Alphavirus genus, namely, CHIKV and SFV, was observed in the studied archival CHIKV sample. Only SFV was found in the archival sample from 1942. All isolates were capable of highly efficient replication in the C6/36, Vero E6, 293, and SPEV cell cultures showing the development of cytopathological effects and were able to produce pathomorphological changes typical of these alphaviruses in mice. Whole genome sequences have been obtained for these viruses and analyzed. Studied isolates clustered with the typical African CHIKV and SFV strains. These isolates may be attributed to the oldest known SFV and CHIKV strains dating back to 1942 and 1953 preserved in laboratory collections. The archival CHIKV isolate was genotyped as an ECSA variant, the modern representatives of which are associated with the global spread of CHIKV in recent decades. Semliki Forest and Chikungunya virus isolates were revived from archival laboratory samples presumably dating back to 1942 and 1953, and their virological characterization was carried out, followed by genotyping and phylogenetic analysis of their whole-genome sequences.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.

REFERENCES

  1. Chen, R., Mukhopadhyay, S., Merits, A., Bolling, B., Nasar, F., Coffey, L.L., Powers, A., and Weaver, S.C., ICTV report consortium ICTV virus taxonomy profile: Togaviridae, J. Gen. Virol., 2018, vol. 99, no. 6, pp. 761–762. https://doi.org/10.1099/jgv.0.001072

    Article  CAS  PubMed  Google Scholar 

  2. Cui, J., Gao, M., and Ren, X., Phylogeny and homologous recombination in Chikungunya viruses, Infect., Genet. Evol., 2011, vol. 11, no. 8, pp. 1957–1963. https://doi.org/10.1016/j.meegid.2011.08.026

    Article  CAS  PubMed  Google Scholar 

  3. Khongwichit, S., Chansaenroj, J., Chirathaworn, C., and Poovorawan Y.J., Chikungunya virus infection: Molecular biology, clinical characteristics, and epidemiology in Asian countries, Biomed. Sci., 2021, vol. 28, no. 1, p. 84. https://doi.org/10.1186/s12929-021-00778-8

    Article  Google Scholar 

  4. Robinson, M.C., An epidemic of virus disease in Southern Province, Tanganyika territory, in 1952–1953. I. Clinical Features, Trans. R. Soc. Trop. Med. Hyg., 1955, vol. 49, no. 1, pp. 28–32. https://doi.org/10.1016/0035-9203(55)90080-8

    Article  CAS  PubMed  Google Scholar 

  5. Mason, P.J. and Haddow, A.J., An epidemic of virus disease in Southern Province, Tanganyika Territory, in 1952–1953: An additional note on Chikungunya virus isolations and serum antibodies, Trans. R. Soc. Trop. Med. Hyg., 1957, vol. 51, no. 3, pp. 238–240. https://doi.org/10.1016/0035-9203(57)90022-6

    Article  CAS  PubMed  Google Scholar 

  6. Ross, R.W., The Newala epidemic. III. The virus: Isolation, pathogenic properties and relationship to the epidemic, J. Hyg., 1956, vol. 54, no. 2, pp. 177–191. https://doi.org/10.1017/s0022172400044442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Schlesinger, R.W., New opportunities in biological research offered by arthropod cell cultures. I. Some speculations on the possible role of arthropods in the evolution of arboviruses, Curr. Top. Microbiol. Immunol., 1971, vol. 55, pp. 241–245. https://doi.org/10.1007/978-3-642-65224-0_40

    Article  CAS  PubMed  Google Scholar 

  8. Vancini, R., Hernandez, R., and Brown, D., Alphavirus entry into host cells, Prog. Mol. Biol. Transl. Sci., 2015, vol. 129, pp. 33–62. https://doi.org/10.1016/bs.pmbts.2014.10.002

    Article  PubMed  Google Scholar 

  9. Calisher, C.H. and Karabatsos, N., Arbovirus Serogroups: Definition and Geographic Distribution, Boca Raton, FL: CRC Press, 1988, pp. 19–57.

    Google Scholar 

  10. Ferguson, M.C., Saul, S., Fragkoudis, R., Weisheit, S., Cox, J., Patabendige, A., et al., Ability of the encephalitic arbovirus Semliki forest virus to cross the blood–brain barrier is determined by the charge of the E2 glycoprotein, J. Virol., 2015, vol. 89, pp. 7536–7549. https://doi.org/10.1128/JVI.03645-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Das, T., Hoarau, J.J., Bandjee, M.C.J., Maquart, M., and Gasque, P., Multifaceted innate immune responses engaged by astrocytes, microglia and resident dendritic cells against chikungunya neuroinfection, J. Gen. Virol., 2015, vol. 96, pp. 294–310. https://doi.org/10.1099/vir.0.071175-0

    Article  CAS  PubMed  Google Scholar 

  12. Meshram, C.D., Lukash, T., Philips, A.T., Akhrymuk, I., Frolova, E.I., and Frolov, I., Lack of nsP2-specific nuclear functions attenuates chikungunya virus replication both in vitro and in vivo, Virology, 2019, vol. 534, pp. 14–24. https://doi.org/10.1016/j.virol.2019.05.016

    Article  CAS  PubMed  Google Scholar 

  13. Burt, F.J., Rolph, M.S., Rulli, N.E., Mahalingam, S., and Heise, M.T., Chikungunya: A re-emerging virus, Lancet, 2012, vol. 379, no. 9816, pp. 662–671. https://doi.org/10.1016/S0140-6736(11)60281-X

    Article  PubMed  Google Scholar 

  14. Weaver, S.C. and Lecuit, M., Chikungunya virus and the global spread of a mosquito-borne disease, N. Engl. J. Med., 2015, vol. 372, pp. 1231–1239. https://doi.org/10.1016/S0140-6736(11)60281-X

    Article  CAS  PubMed  Google Scholar 

  15. Khongwichit, S., Chansaenroj, J., Thongmee, T., Benjamanukul, S., Wanlapakorn, N., Chirathaworn, C., and Poovorawan, Y., Large-scale outbreak of Chikungunya virus infection in Thailand, 2018–2019, PLoS One, 2021, vol. 16, no. 3, p. e0247314. https://doi.org/10.1371/journal.pone.0247314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Arankalle, V.A., Shrivastava, S., Cherian, S., Gunjikar, R.S., Walimbe, A.M., Jadhav, S.M., et al., Genetic divergence of Chikungunya viruses in India (1963–2006) with special reference to the 2005–2006 explosive epidemic, J. Gen. Virol., 2007, vol. 88, part 7, pp. 1967–1976. https://doi.org/10.1099/vir.0.82714-0

    Article  CAS  PubMed  Google Scholar 

  17. Patterson, J., Sammon, M., and Garg, M., Dengue, Zika and Chikungunya: Emerging arboviruses in the New World, West J. Emerg. Med., 2016, vol. 17, no. 6, pp. 671–679. https://doi.org/10.5811/westjem.2016.9.30904

    Article  PubMed  PubMed Central  Google Scholar 

  18. Smithburn, K.C., Semliki Forest virus; propagation of the virus in developing chick embryos, J. Immunol., 1946, vol. 52, pp. 309–314.

    Article  CAS  PubMed  Google Scholar 

  19. Smithburn, K.C., Haddow, A.J., and Mahaffy, A.F., A neurotropic virus isolated from aedes mosquitoes caught in the Semliki Forest, Am. J. Trop. Med. Hyg., 1946, vol. 26, pp. 189–208. https://doi.org/10.4269/ajtmh.1946.s1-26.189

    Article  CAS  PubMed  Google Scholar 

  20. Dick, G.W., Epidemiological notes on some viruses isolated in Uganda (Yellow fever, Rift Valley fever, Bwamba fever, West Nile, Mengo, Semliki Forest, Bunyamwera, Ntaya, Uganda S and Zika viruses), Trans. R. Soc. Trop. Med. Hyg., 1953, vol. 47, no. 1, pp. 13–48. https://doi.org/10.1016/0035-9203(53)90021-2

    Article  CAS  PubMed  Google Scholar 

  21. Willems, W.R., Kaluza, G., Boschek, G.B., and Bauer, H., Semliki Forest virus: cause of a fatal case of human encephalitis, Science, 1979, vol. 203, no. 4385, pp. 1127–1129. https://doi.org/10.1126/science.424742

    Article  CAS  PubMed  Google Scholar 

  22. Svyatchenko, V.A., Nikonov, S.D., Mayorov, A.P., Gelfond, M.L., and Loktev, VB., Antiviral photodynamic therapy: Inactivation and inhibition of SARS-CoV-2 in vitro using methylene blue and Radachlorin, Photodiagn. Photodyn. Ther., 2021, vol. 33, p. 102112. https://doi.org/10.1016/j.pdpdt.2020.102112

    Article  CAS  Google Scholar 

  23. Tamura, K., Dudley, J., Nei, M., and Kumar, S., MEG-A7: Molecular Evolutionary Genetics Analysis (MEGA) software version 7.0, Mol. Biol. Evol., 2016, vol. 33, no. 7, pp. 1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Svyatchenko, V.A., Ternovoi, V.A., Lutkovskiy, R.Y., Protopopova, E.V., Gudymo, A.S., Danilchenko, N.V., et al., Human adenovirus and influenza A virus exacerbate SARS-CoV-2 infection in animal models, Microorganisms, 2023, vol. 11, p. 180. https://doi.org/10.3390/microorganisms11010180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Volk, S.M., Chen, R., Tsetsarkin, K.A., Adams, A.P., Garcia, T.I., Sall, A.A., et al., Genome-scale phylogenetic analyses of chikungunya virus reveal independent emergences of recent epidemics and various evolutionary rates, J. Virol., 2010, vol. 84, no. 13, pp. 6497–6504. https://doi.org/10.1128/JVI.01603-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Khan, A.H., Morita, K., Parquet, M.D.C., Hasebe, F., Mathenge, E.G.M., and Igarashi, A., Complete nucleotide sequence of chikungunya virus and evidence for an internal polyadenylation site, J. Gen. Virol., 2002, vol. 83, part 12, pp. 3075–3084. https://doi.org/10.1099/0022-1317-83-12-3075

    Article  CAS  PubMed  Google Scholar 

  27. Hakim, M.S., Annisa, L., Gazali, F.M., and Aman, A.T., The origin and continuing adaptive evolution of chikungunya virus, Arch. Virol., 2022, vol. 167, pp. 2443–2455. https://doi.org/10.1007/s00705-022-05570-z

    Article  CAS  PubMed  Google Scholar 

  28. Charrel, R.N., Leparc-Goffart, I., Gallian, P., and de Lamballerie, X., Globalization of Chikungunya: 10 years to invade the world, Clin. Microbiol. Infect., 2014, vol. 20, no. 7, pp. 662–663. https://doi.org/10.1111/1469-0691.12694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Rahman, M., Yamagishi, J., Rahim, R., Hasan, A., and Sobhan, A., East/Central/ South African genotype in a Chikungunya outbreak, Dhaka, Bangladesh, 2017, Emerging Infect. Dis., 2019, vol. 25, no. 2, p. 370. https://doi.org/10.3201/eid2502.180188

    Article  Google Scholar 

Download references

Funding

The work was supported by a state order to the State Research Center of Virology and Biotechnology “VECTOR” of the Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. B. Loktev.

Ethics declarations

CONFLICT OF INTEREST

The authors of this work declare that they have no conflicts of interest.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

All experimentation with animals was performed using general anesthesia in accordance with the decision of the Bioethics Committee of the State Research Center of Virology and Biotechnology “VECTOR,” protocol no. 02-05 dated May 15, 2020. All studies were performed in compliance with the biosafety rules outlined in Sanitary Regulation and Norms no. 3.3686-21.

Additional information

Translated by E. Martynova

Publisher’s Note.

Allerton Press remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mikryukova, T.P., Protopopova, E.V., Mezhevalova, A.S. et al. Historical Isolates of Semliki Forest and Chikungunya Viruses and Their Virological Characteristic, Whole-Genome Sequences, and Phylogeny. Mol. Genet. Microbiol. Virol. 38, 249–255 (2023). https://doi.org/10.3103/S0891416823040055

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0891416823040055

Keywords:

Navigation