Characterization and Vector Competence Studies of Chikungunya Virus Lacking Repetitive Motifs in the 3′ Untranslated Region of the Genome
Abstract
:1. Introduction
2. Materials and Methods
2.1. Mosquitoes
2.2. Rearing Mosquitoes
2.3. Cell Culture
2.4. Construction of CHIKV cDNA Clones
2.5. In Vitro Transcription and Recovery of Recombinant Virus
2.6. Growth Kinetic Studies in Cell Culture
2.7. Plaque Assay
2.8. Infection of Mosquitoes
2.9. Mosquito Processing
2.10. Nucleic Acid Extraction from Mosquitoes and Real-Time RT-PCR
2.11. Vector Competence Indices
2.12. Statistics
3. Results
3.1. Characterization of CHIKV Lacking DR Elements in the 3′ UTR in Cell Culture
3.2. Vector Competence of CHIKV-∆DR in Ae. aegypti and Ae. albopictus
3.3. Vector Competence of CHIKV-∆DR and CHIKV-WT in Ae. vexans and Cx. pipiens
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Weaver, S.C.; Barrett, A.D. Transmission cycles, host range, evolution and emergence of arboviral disease. Nat. Rev. Microbiol. 2004, 2, 789–801. [Google Scholar] [CrossRef]
- Pialoux, G.; Gaüzère, B.A.; Jauréguiberry, S.; Strobel, M. Chikungunya, an epidemic arbovirosis. Lancet Infect Dis. 2007, 7, 319–327. [Google Scholar] [CrossRef]
- Ross, R.W. The Newala epidemic. III. The virus: Isolation, pathogenic properties and relationship to the epidemic. J. Hyg. (Lond.) 1956, 54, 177–191. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pastorino, B.; Muyembe-Tamfum, J.J.; Bessaud, M.; Tock, F.; Tolou, H.; Durand, J.P.; Peyrefitte, C.N. Epidemic resurgence of Chikungunya virus in democratic Republic of the Congo: Identification of a new central African strain. J. Med. Virol. 2004, 74, 277–282. [Google Scholar] [CrossRef] [PubMed]
- Sergon, K.; Njuguna, C.; Kalani, R.; Ofula, V.; Onyango, C.; Konongoi, L.S.; Bedno, S.; Burke, H.; Dumilla, A.M.; Konde, J.; et al. Seroprevalence of Chikungunya virus (CHIKV) infection on Lamu Island, Kenya, October 2004. Am. J. Trop. Med. Hyg. 2008, 78, 333–337. [Google Scholar] [CrossRef] [PubMed]
- Sergon, K.; Yahaya, A.A.; Brown, J.; Bedja, S.A.; Mlindasse, M.; Agata, N.; Allaranger, Y.; Ball, M.D.; Powers, A.M.; Ofula, V.; et al. Seroprevalence of Chikungunya virus infection on Grande Comore Island, union of the Comoros, 2005. Am. J. Trop. Med. Hyg. 2007, 76, 1189–1193. [Google Scholar] [CrossRef] [PubMed]
- Renault, P.; Solet, J.L.; Sissoko, D.; Balleydier, E.; Larrieu, S.; Filleul, L.; Lassalle, C.; Thiria, J.; Rachou, E.; de Valk, H.; et al. A major epidemic of chikungunya virus infection on Reunion Island, France, 2005–2006. Am. J. Trop. Med. Hyg. 2007, 77, 727–731. [Google Scholar] [CrossRef]
- Chastel, C. Chikungunya virus: Its recent spread to the southern Indian Ocean and Reunion Island (2005–2006). Bull. Acad. Natl. Med. 2005, 189, 1827–1835. [Google Scholar] [PubMed]
- Lahariya, C.; Pradhan, S.K. Emergence of chikungunya virus in Indian subcontinent after 32 years: A review. J. Vector Borne Dis. 2006, 43, 151–160. [Google Scholar] [PubMed]
- Naresh Kumar, C.V.; Sai Gopal, D.V. Reemergence of Chikungunya virus in Indian Subcontinent. Indian J. Virol. 2010, 21, 8–17. [Google Scholar] [CrossRef] [Green Version]
- Tsetsarkin, K.A.; Vanlandingham, D.L.; McGee, C.E.; Higgs, S. A single mutation in chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog. 2007, 3, e201. [Google Scholar] [CrossRef] [PubMed]
- Vazeille, M.; Moutailler, S.; Coudrier, D.; Rousseaux, C.; Khun, H.; Huerre, M.; Thiria, J.; Dehecq, J.S.; Fontenille, D.; Schuffenecker, I.; et al. Two Chikungunya isolates from the outbreak of La Reunion (Indian Ocean) exhibit different patterns of infection in the mosquito, Aedes albopictus. PLoS ONE 2007, 2, e1168. [Google Scholar] [CrossRef] [PubMed]
- Rezza, G.; Nicoletti, L.; Angelini, R.; Romi, R.; Finarelli, A.C.; Panning, M.; Cordioli, P.; Fortuna, C.; Boros, S.; Magurano, F.; et al. Infection with chikungunya virus in Italy: An outbreak in a temperate region. Lancet 2007, 370, 1840–1846. [Google Scholar] [CrossRef]
- Calba, C.; Guerbois-Galla, M.; Franke, F.; Jeannin, C.; Auzet-Caillaud, M.; Grard, G.; Pigaglio, L.; Decoppet, A.; Weicherding, J.; Savaill, M.C.; et al. Preliminary report of an autochthonous chikungunya outbreak in France, July to September 2017. Euro Surveill. 2017, 22. [Google Scholar] [CrossRef] [Green Version]
- Leparc-Goffart, I.; Nougairede, A.; Cassadou, S.; Prat, C.; de Lamballerie, X. Chikungunya in the Americas. Lancet 2014, 383, 514. [Google Scholar] [CrossRef]
- Pan American Health Organization/World Health Organization (PAHO/WHO). Geographic Spread of Chikungunya in the Americas, December 2013–December 2017. Available online: https://ais.paho.org/phip/viz/ed_chikungunya_amro.asp (accessed on 25 January 2021).
- Lanciotti, R.S.; Valadere, A.M. Transcontinental movement of Asian genotype chikungunya virus. Emerg. Infect Dis. 2014, 20, 1400–1402. [Google Scholar] [CrossRef]
- Kuhn, R.J. Togaviridae. In Fields Virology, 6th ed.; Knipe, D.M., Howley, P.M., Eds.; Lippincott Williams & Wilkons: Philadelphia, PA, USA, 2013; Volume 1, pp. 629–650. [Google Scholar]
- Frolov, I.; Hardy, R.; Rice, C.M. Cis-acting RNA elements at the 5′ end of Sindbis virus genome RNA regulate minus- and plus-strand RNA synthesis. RNA 2001, 7, 1638–1651. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ou, J.H.; Trent, D.W.; Strauss, J.H. The 3′-non-coding regions of alphavirus RNAs contain repeating sequences. J. Mol. Biol. 1982, 156, 719–730. [Google Scholar] [CrossRef]
- Pfeffer, M.; Kinney, R.M.; Kaaden, O.R. The alphavirus 3′-nontranslated region: Size heterogeneity and arrangement of repeated sequence elements. Virology 1998, 240, 100–108. [Google Scholar] [CrossRef] [Green Version]
- Chen, R.; Wang, E.; Tsetsarkin, K.A.; Weaver, S.C. Chikungunya virus 3′ untranslated region: Adaptation to mosquitoes and a population bottleneck as major evolutionary forces. PLoS Pathog. 2013, 9, e1003591. [Google Scholar] [CrossRef] [Green Version]
- Volk, S.M.; Chen, R.; Tsetsarkin, K.A.; Adams, A.P.; Garcia, T.I.; Sall, A.A.; Nasar, F.; Schuh, A.J.; Holmes, E.C.; Higgs, S.; et al. Genome-scale phylogenetic analyses of chikungunya virus reveal independent emergences of recent epidemics and various evolutionary rates. J. Virol. 2010, 84, 6497–6504. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sahadeo, N.; Mohammed, H.; Allicock, O.M.; Auguste, A.J.; Widen, S.G.; Badal, K.; Pulchan, K.; Foster, J.E.; Weaver, S.C.; Carrington, C.V. Molecular Characterisation of Chikungunya Virus Infections in Trinidad and Comparison of Clinical and Laboratory Features with Dengue and Other Acute Febrile Cases. PLoS Negl. Trop. Dis. 2015, 9, e0004199. [Google Scholar]
- Hyde, J.L.; Chen, R.; Trobaugh, D.W.; Diamond, M.S.; Weaver, S.C.; Klimstra, W.B.; Wilusz, J. The 5′ and 3′ ends of alphavirus RNAs—Non-coding is not non-functional. Virus Res. 2015, 206, 99–107. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Filomatori, C.V.; Bardossy, E.S.; Merwaiss, F.; Suzuki, Y.; Henrion, A.; Saleh, M.C.; Alvarez, D.E. RNA recombination at Chikungunya virus 3’UTR as an evolutionary mechanism that provides adaptability. PLoS Pathog. 2019, 15, e1007706. [Google Scholar] [CrossRef] [PubMed]
- Merwaiss, F.; Filomatori, C.V.; Susuki, Y.; Bardossy, E.S.; Alvarez, D.E.; Saleh, M.C. Chikungunya virus replication rate determines the capacity of crossing tissue barriers in mosquitoes. J. Virol. 2021. [Google Scholar] [CrossRef]
- Filomatori, C.V.; Merwaiss, F.; Bardossy, E.S.; Alvarez, D.E. Impact of alphavirus 3’UTR plasticity on mosquito transmission. Semin. Cell Dev. Biol. 2020, 111, 148–155. [Google Scholar] [CrossRef]
- Arias-Goeta, C.; Mousson, L.; Rougeon, F.; Failloux, A.B. Dissemination and transmission of the E1-226V variant of chikungunya virus in Aedes albopictus are controlled at the midgut barrier level. PLoS ONE 2013, 8, e57548. [Google Scholar] [CrossRef]
- Roiz, D.; Neteler, M.; Castellani, C.; Arnoldi, D.; Rizzoli, A. Climatic factors driving invasion of the tiger mosquito (Aedes albopictus) into new areas of Trentino, northern Italy. PLoS ONE 2011, 6, e14800. [Google Scholar] [CrossRef] [Green Version]
- Medlock, J.M.; Hansford, K.M.; Schaffner, F.; Versteirt, V.; Hendrickx, G.; Zeller, H.; Van Bortel, W. A review of the invasive mosquitoes in Europe: Ecology, public health risks, and control options. Vector Borne Zoonotic. Dis. 2012, 12, 435–447. [Google Scholar] [CrossRef] [Green Version]
- Sherpa, S.; Blum, M.G.B.; Capblancq, T.; Cumer, T.; Rioux, D.; Després, L. Unravelling the invasion history of the Asian tiger mosquito in Europe. Mol. Ecol. 2019, 28, 2360–2377. [Google Scholar] [CrossRef]
- Goiri, F.; González, M.A.; Goikolea, J.; Oribe, M.; Castro, V.; Delacour, S.; Lucientes, J.; Ortega-Araiztegi, I.; Barandika, J.F.; García-Pérez, A.L. Progressive Invasion of Aedes albopictus in Northern Spain in The Period 2013-2018 and A Possible Association with the Increase in Insect Bites. Int. J. Environ. Res. Public Health 2020, 17, 1678. [Google Scholar] [CrossRef] [Green Version]
- ECDC. Mosquito Maps. 2020. Available online: https://ecdc.europa.eu/en/disease-vectors/surveillance-and-disease-data/mosquito-maps (accessed on 25 January 2021).
- Pluskota, B.; Jöst, A.; Augsten, X.; Stelzner, L.; Ferstl, I.; Becker, N. Successful overwintering of Aedes albopictus in Germany. Parasitol. Res. 2016, 115, 3245–3247. [Google Scholar] [CrossRef]
- Modlmaier, M.; Kuhn, R.; Kaaden, O.R.; Pfeffer, M. Transmission studies of a European Sindbis virus in the floodwater mosquito Aedes vexans (Diptera: Culicidae). Int. J. Med. Microbiol. 2002, 291 (Suppl. 33), 164–170. [Google Scholar] [CrossRef]
- Kümmerer, B.M.; Grywna, K.; Gläsker, S.; Wieseler, J.; Drosten, C. Construction of an infectious Chikungunya virus cDNA clone and stable insertion of mCherry reporter genes at two different sites. J. Gen. Virol. 2012, 93 Pt 9, 1991–1995. [Google Scholar] [CrossRef]
- Voßmann, S.; Wieseler, J.; Kerber, R.; Kümmerer, B.M. A basic cluster in the N terminus of yellow fever virus NS2A contributes to infectious particle production. J. Virol. 2015, 89, 4951–4965. [Google Scholar] [CrossRef] [Green Version]
- Heitmann, A.; Jansen, S.; Lühken, R.; Leggewie, M.; Schmidt-Chanasit, J.; Tannich, E. Forced Salivation as a Method to Analyze Vector Competence of Mosquitoes. J. Vis. Exp. 2018. [Google Scholar] [CrossRef]
- Riswari, S.F.; Ma’roef, C.N.; Djauhari, H.; Kosasih, H.; Perkasa, A.; Yudhaputri, F.A.; Artika, I.M.; Williams, M.; van der Ven, A.; Myint, K.S.; et al. Study of viremic profile in febrile specimens of chikungunya in Bandung, Indonesia. J. Clin. Virol. 2016, 74, 61–65. [Google Scholar] [CrossRef] [Green Version]
- Waggoner, J.J.; Gresh, L.; Vargas, M.J.; Ballesteros, G.; Tellez, Y.; Soda, K.J.; Sahoo, M.K.; Nuñez, A.; Balmaseda, A.; Harris, E.; et al. Viremia and Clinical Presentation in Nicaraguan Patients Infected With Zika Virus, Chikungunya Virus, and Dengue Virus. Clin. Infect Dis. 2016, 63, 1584–1590. [Google Scholar] [CrossRef]
- Rosen, L.; Gubler, D. The use of mosquitoes to detect and propagate dengue viruses. Am. J. Trop. Med. Hyg. 1974, 23, 1153–1160. [Google Scholar] [CrossRef]
- Boorman, J. Induction of salivation in biting midges and mosquitoes, and demonstration of virus in the saliva of infected insects. Med. Vet. Entomol. 1987, 1, 211–214. [Google Scholar] [CrossRef]
- Kraemer, M.U.G.; Reiner, R.C., Jr.; Brady, O.J.; Messina, J.P.; Gilbert, M.; Pigott, D.M.; Yi, D.; Johnson, K.; Earl, L.; Marczak, L.B.; et al. Past and future spread of the arbovirus vectors Aedes aegypti and Aedes albopictus. Nat. Microbiol. 2019, 4, 854–863. [Google Scholar] [CrossRef]
- Strauss, J.H.; Strauss, E.G. The alphaviruses: Gene expression, replication, and evolution. Microbiol. Rev. 1994, 58, 491–562. [Google Scholar] [CrossRef]
- Faragher, S.G.; Dalgarno, L. Regions of conservation and divergence in the 3’ untranslated sequences of genomic RNA from Ross River virus isolates. J. Mol. Biol. 1986, 190, 141–148. [Google Scholar] [CrossRef]
- Kuhn, R.J.; Hong, Z.; Strauss, J.H. Mutagenesis of the 3’ nontranslated region of Sindbis virus RNA. J. Virol. 1990, 64, 1465–1476. [Google Scholar] [CrossRef] [Green Version]
- Morley, V.J.; Noval, M.G.; Chen, R.; Weaver, S.C.; Vignuzzi, M.; Stapleford, K.A.; Turner, P.E. Chikungunya virus evolution following a large 3’UTR deletion results in host-specific molecular changes in protein-coding regions. Virus Evol. 2018, 4, vey012. [Google Scholar] [CrossRef] [Green Version]
- Roberts, G.C.; Zothner, C.; Remenyi, R.; Merits, A.; Stonehouse, N.J.; Harris, M. Evaluation of a range of mammalian and mosquito cell lines for use in Chikungunya virus research. Sci. Rep. 2017, 7, 14641. [Google Scholar] [CrossRef] [Green Version]
- Zhang, X.; Huang, Y.; Wang, M.; Yang, F.; Wu, C.; Huang, D.; Xiong, L.; Wan, C.; Cheng, J.; Zhang, R. Differences in genome characters and cell tropisms between two chikungunya isolates of Asian lineage and Indian Ocean lineage. Virol. J. 2018, 15, 130. [Google Scholar] [CrossRef]
- Garcia-Moreno, M.; Sanz, M.A.; Carrasco, L. A Viral mRNA Motif at the 3’-Untranslated Region that Confers Translatability in a Cell-Specific Manner. Implications for Virus Evolution. Sci. Rep. 2016, 6, 19217. [Google Scholar] [CrossRef]
- Vazeille, M.; Jeannin, C.; Martin, E.; Schaffner, F.; Failloux, A.B. Chikungunya: A risk for Mediterranean countries? Acta Trop. 2008, 105, 200–202. [Google Scholar] [CrossRef]
- Talbalaghi, A.; Moutailler, S.; Vazeille, M.; Failloux, A.B. Are Aedes albopictus or other mosquito species from northern Italy competent to sustain new arboviral outbreaks? Med. Vet. Entomol. 2010, 24, 83–87. [Google Scholar] [CrossRef]
- Prudhomme, J.; Fontaine, A.; Lacour, G.; Gantier, J.C.; Diancourt, L.; Velo, E.; Bino, S.; Reiter, P.; Mercier, A. The native European Aedes geniculatus mosquito species can transmit chikungunya virus. Emerg. Microbes Infect 2019, 8, 962–972. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ribeiro Cruz, A.C.; Pinto Nunes Neto, J.; Patroca da Silva, S.; Vieira Pinto da Silva, E.; Juscely Galvão Pereira, G.; Maia Santos, M.; Antônio de Oliveira Monteiro, H.; Barreto Dos Santos, F.; José de Paula Souza, E.G.R.; Fortes Aragão, C.; et al. Chikungunya virus Detection in Aedes aegypti and Culex quinquefasciatus during an Outbreak in the Amazon Region. Viruses 2020, 12, 853. [Google Scholar] [CrossRef]
Mosquito Taxon | Origin/Collection Site | Year of Collection | Year (Generation) Colony Established in Leipzig | Generations Used for Experiments |
---|---|---|---|---|
Aedes aegypti | Geigy, Switzerland 1 | 1950 | 2017 (F1) 2 | F2–F5 |
Aedes albopictus | Cesena, Italy | 2016 | 2016 (F2) | F11–F13 |
Aedes vexans ‘TAMU’ | Texas, USA | 2002 | 2013 (F35) | F45–F53 |
Culex pipiens biotype molestus | Hesse, Germany | 2000 | 2013 (F1) 2 | F55–F85 |
Mosquito Species | Virus | Days Post Infection (%) | Infection Rate (%) | Dissemination Rate (%) | Transmission Rate (%) | Transmission Efficiency (%) |
---|---|---|---|---|---|---|
Aedes aegypti | ∆DR | 7 | 11/11 | 10/11 | 4/10 | 4/11 |
100% | 90.9% | 40% | 36.4% | |||
14 | 10/10 | 9/10 | 3/9 | 3/10 | ||
100% | 90% | 33.3% | 30% | |||
Aedes albopictus | ∆DR | 7 | 7/7 | 6/7 | 3/6 | 3/7 |
100% | 85.7% | 50% | 42.9% | |||
14 | 9/9 | 9/9 | 6/9 | 6/9 | ||
100% | 100% | 66.6% | 66.7% |
Mosquito Species | Virus | Days Post Infection (%) | Infection Rate (%) | Dissemination Rate (%) | Transmission Rate (%) | Transmission Efficiency (%) |
---|---|---|---|---|---|---|
Aedes vexans | WT | 7 | 10/12 | 2/10 | 1/2 | 1/12 |
83.3% | 20% | 50% | 8.3% | |||
14 | 13/20 | 4/13 | 3/4 | 3/20 | ||
65% | 30.8% | 75% | 15% | |||
∆DR | 7 | 8/10 | 0/8 | 0/0 | 0/10 | |
80% | 0% | n.a. | 0% | |||
14 | 11/23 | 4/11 | 1/4 | 1/23 | ||
47.8% | 36.4% | 25% | 4.3% | |||
Culex pipiens | WT | 7 | 0/9 | 0/0 | 0/0 | 0/9 |
0% | n.a. | n.a. | 0% | |||
14 | 6/20 | 3/6 | 1/3 | 1/20 | ||
30% | 50% | 33.9% | 5% | |||
∆DR | 7 | 6/8 | 1/6 | 1/1 | 1/8 | |
75% | 16.6% | 100% | 12.5% | |||
14 | 4/14 | 0/4 | 0/0 | 0/14 | ||
28.5% | 0% | n.a. | 0% |
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Karliuk, Y.; vom Hemdt, A.; Wieseler, J.; Pfeffer, M.; Kümmerer, B.M. Characterization and Vector Competence Studies of Chikungunya Virus Lacking Repetitive Motifs in the 3′ Untranslated Region of the Genome. Viruses 2021, 13, 403. https://doi.org/10.3390/v13030403
Karliuk Y, vom Hemdt A, Wieseler J, Pfeffer M, Kümmerer BM. Characterization and Vector Competence Studies of Chikungunya Virus Lacking Repetitive Motifs in the 3′ Untranslated Region of the Genome. Viruses. 2021; 13(3):403. https://doi.org/10.3390/v13030403
Chicago/Turabian StyleKarliuk, Yauhen, Anja vom Hemdt, Janett Wieseler, Martin Pfeffer, and Beate M. Kümmerer. 2021. "Characterization and Vector Competence Studies of Chikungunya Virus Lacking Repetitive Motifs in the 3′ Untranslated Region of the Genome" Viruses 13, no. 3: 403. https://doi.org/10.3390/v13030403