Evaluation of two artificial infection methods of live ticks as tools for studying interactions between tick-borne viruses and their tick vectors
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu hodnotící studie, časopisecké články, práce podpořená grantem
Grantová podpora
grant No. ANR-10-LABEX-62-IBEID
French Government's Investissement d'Avenir program, Laboratoire d'Excellence "Integrative Biology of Emerging Infectious Diseases"
No. 20-14325S
Czech Science Foundation project
PubMed
35017574
PubMed Central
PMC8752753
DOI
10.1038/s41598-021-04498-9
PII: 10.1038/s41598-021-04498-9
Knihovny.cz E-zdroje
- MeSH
- arachnida jako vektory fyziologie virologie MeSH
- interakce hostitele a patogenu MeSH
- klíště fyziologie virologie MeSH
- klíšťová encefalitida přenos virologie MeSH
- lidé MeSH
- myši inbrední BALB C MeSH
- myši MeSH
- Orbivirus fyziologie MeSH
- reovirové infekce přenos virologie MeSH
- virologie metody MeSH
- viry klíšťové encefalitidy fyziologie MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- hodnotící studie MeSH
- práce podpořená grantem MeSH
Up to 170 tick-borne viruses (TBVs) have been identified to date. However, there is a paucity of information regarding TBVs and their interaction with respective vectors, limiting the development of new effective and urgently needed control methods. To overcome this gap of knowledge, it is essential to reproduce transmission cycles under controlled laboratory conditions. In this study we assessed an artificial feeding system (AFS) and an immersion technique (IT) to infect Ixodes ricinus ticks with tick-borne encephalitis (TBE) and Kemerovo (KEM) virus, both known to be transmitted predominantly by ixodid ticks. Both methods permitted TBEV acquisition by ticks and we further confirmed virus trans-stadial transmission and onward transmission to a vertebrate host. However, only artificial feeding system allowed to demonstrate both acquisition by ticks and trans-stadial transmission for KEMV. Yet we did not observe transmission of KEMV to mice (IFNAR-/- or BALB/c). Artificial infection methods of ticks are important tools to study tick-virus interactions. When optimally used under laboratory settings, they provide important insights into tick-borne virus transmission cycles.
Zobrazit více v PubMed
Springer A, Glass A, Probst J, Strube C. Tick-borne zoonoses and commonly used diagnostic methods in human and veterinary medicine. Parasitol. Res. 2021 doi: 10.1007/s00436-020-07033-3. PubMed DOI PMC
Wikel SK. Ticks and tick-borne infections: Complex ecology, agents, and host interactions. Vet. Sci. 2018;5(2):60. PubMed PMC
Jongejan F, Uilenberg G. The global importance of ticks. Parasitology. 2004;129:3–14. PubMed
Labuda M, Nuttall PA. Tick-borne viruses. Parasitology. 2004;129:221–245. PubMed
Shi J, Hu Z, Deng F, Shen S. Tick-borne viruses. Virol. Sin. 2018;33(1):21–43. PubMed PMC
Bonnet S, Liu XY. Laboratory artificial infection of hard ticks: A tool for the analysis of tick-borne pathogen transmission. Acarologia. 2012;52(4):453–464.
Nuttall PA, Jones LD, Labuda M, Kaufman WR. Adaptations of arboviruses to ticks. J. Med. Entomol. 1994;31(1):1–9. PubMed
Jones LD, Hodgson E, Nuttall PA. Enhancement of virus transmission by tick salivary glands. J. Gen. Virol. 1989;70(7):1895–1898. PubMed
de la Fuente J, et al. Tick–pathogen interactions and vector competence: Identification of molecular drivers for tick-borne diseases. Front. Cell. Infect. Microbiol. 2017;7(April):1–13. PubMed PMC
Belova OA, et al. Properties of the tick-borne encephalitis virus population during persistent infection of ixodid ticks and tick cell lines. Ticks Tick Borne Dis. 2017;8(6):895–906. PubMed
Slovák M, et al. Survival dynamics of tick-borne encephalitis virus in Ixodes ricinus ticks. Ticks Tick Borne Dis. 2014;5(6):962–969. PubMed
Hurlbut H, Thomas J. The experimental host range of the arthropod-borne animal viruses in arthropods. Virology. 1960;12:391–407. PubMed
Talactac MR, et al. Vector competence of Haemaphysalis longicornis ticks for a Japanese isolate of the Thogoto virus. Sci. Rep. 2018;8(1):1–8. PubMed PMC
Bonnet S, et al. Transstadial and transovarial persistence of Babesia divergens DNA in Ixodes ricinus ticks fed on infected blood in a new skin-feeding technique. Parasitology. 2007;134(2):197–207. PubMed
Policastro PF, Schwan TG. Experimental infection of Ixodes scapularis Larvae (Acari: Ixodidae) by immersion in low passage cultures of Borrelia burgdorferi. J. Med. Entomol. 2003;40(3):364–370. PubMed
Bonnet S, Brisseau N, Hermouet A, Jouglin M, Chauvin A. Experimental in vitro transmission of Babesia sp. (EU1) by Ixodes ricinus. Vet. Res. 2009;40(3):1–8. PubMed PMC
Cotté V, et al. Transmission of Bartonella henselae by Ixodes ricinus. Emerg. Infect. Dis. 2008;14(7):1074–1080. PubMed PMC
Wechtaisong W, Bonnet SI, Lien YY, Te Chuang S, Tsai YL. Transmission of bartonella henselae within rhipicephalus sanguineus: Data on the potential vector role of the tick. PLoS Negl. Trop. Dis. 2020;14(10):1–14. PubMed PMC
Liu XY, Cote M, Paul REL, Bonnet SI. Impact of feeding system and infection status of the blood meal on Ixodes ricinus feeding. Ticks Tick Borne Dis. 2014;5(3):323–328. PubMed
Reis C, et al. Vector competence of the tick Ixodes ricinus for transmission of Bartonella birtlesii. PLoS Negl. Trop. Dis. 2011;5(5):1–6. PubMed PMC
Mitlzel DN, Wolfinbarger JB, Long DR, Masnick M, Best SM, Bloom ME. Tick-borne flavivirus infection in Ixodes scapularis larvae: Development of a novel method for synchronous viral infection of ticks. Virology. 2007;365(2):410–418. PubMed PMC
Labuda M, et al. An antivector vaccine protects against a lethal vector-borne pathogen. PLoS Pathog. 2006;2(4):251–259. PubMed PMC
Labuda M, et al. Non-viraemic transmission of tick-borne encephalitis virus: A mechanism for arbovirus survival in nature. Experientia. 1993;49(9):802–805. PubMed
Labuda M, et al. Importance of localized skin infection in tick-borne encephalitis virus transmission. Virology. 1996;219(2):357–366. PubMed
Rizzoli A, et al. Ixodes ricinus and its transmitted pathogens in urban and peri-urban areas in Europe: New hazards and relevance for public health. Front. Public Health. 2014;2:1–26. PubMed PMC
Valarcher JF, Hägglund S, Juremalm M, Blomqvist G. Tick-borne encephalitis. Rev. Sci. Tech. Off. Int. Epiz. 2015;34(2):453–466. PubMed
Chumakov M. Report on the isolation from Ixodes persulcatus ticks and from patients in western Siberia of a virus differing from the agent of tick-borne encephalitis. Acta Virol. 1963;7:82–83. PubMed
Tkachev S, Panov V, Dobler G, Tikunova N. First detection of Kemerovo virus in Ixodes pavlovskyi and Ixodes persulcatus ticks collected in Novosibirsk region, Russia. Ticks Tick Borne Dis. 2014;5(5):494–496. PubMed
Dedkov VG, et al. Prevalence of Kemerovo virus in ixodid ticks from the Russian Federation. Ticks Tick Borne Dis. 2014;5(6):651–655. PubMed
Chihota CM, Rennie LF, Kitching RP, Mellor PS. Mechanical transmission of lumpy skin disease virus by Aedes. Epidemiol. Infect. 2001;126:317–321. PubMed PMC
Brault V, Uzest M, Monsion B, Jacquot E, Blanc S. Aphids as transport devices for plant viruses. Comptes Rendus Biol. 2010;333(6–7):524–538. PubMed
Gritsun TS, Nuttall PA, Gould EA. Tick-borne flaviviruses. Adv. Virus Res. 2003;61:317–371. PubMed
Steele GM, Nuttall PA. Difference in vector competence of two species of sympatric ticks, Amblyomma variegatum and Rhipicephalus appendiculatus, for Dugbe virus (Nairovirus, Bunyaviridae) Virus Res. 1989;14(1):73–84. PubMed
Mandl CW. Steps of the tick-borne encephalitis virus replication cycle that affect neuropathogenesis. Virus Res. 2005;111(2):161–174. PubMed
Laureti M, Narayanan D, Rodriguez-Andres J, Fazakerley JK, Kedzierski L. Flavivirus receptors: Diversity, identity, and cell entry. Front. Immunol. 2018;9:2180. PubMed PMC
Hassan SH, Roy P. Expression and functional characterization of Bluetongue Virus VP2 protein: Role in cell entry. J. Virol. 1999;73(12):9832–9842. PubMed PMC
Patel A, Roy P. The molecular biology of Bluetongue virus replication. Virus Res. 2014;182:5–20. PubMed PMC
Mertens PPC, et al. Enhanced infectivity of modified bluetongue virus particles for two insect cell lines and for two Culicoides vector species. Virology. 1996;217(2):582–593. PubMed
Tan B-H, Nason E, Staeuber N, Jiang W, Monastryrskaya K, Roy P. RGD tripeptide of Bluetongue Virus VP7 protein is responsible for core attachment to culicoides cells. J. Virol. 2001;75(8):3937–3947. PubMed PMC
Šimo L, Kazimirova M, Richardson J, Bonnet SI. The essential role of tick salivary glands and saliva in tick feeding and pathogen transmission. Front. Cell. Infect. Microbiol. 2017;7:1–23. PubMed PMC
Libikova H, Rehacek J, Somogyiavo J. Viruses related to the Kemerovo virus in Ixodes ricinus ticks in Czechoslovakia. Acta Virol. 1965;9:76–82. PubMed
Kingsolver MB, Huang Z, Hardy RW. Insect antiviral innate immunity: Pathways, effectors, and connections. J. Mol. Biol. 2013;425(24):4921–4936. PubMed PMC
Schnettler E, et al. Induction and suppression of tick cell antiviral RNAi responses by tick-borne flaviviruses. Nucleic Acids Res. 2014;42(14):9436–9446. PubMed PMC
Hornok S, Horváth G, Jongejan F, Farkas R. Ixodid ticks on ruminants, with on-host initiated moulting (apolysis) of Ixodes, Haemaphysalis and Dermacentor larvae. Vet. Parasitol. 2012;187(1–2):350–353. PubMed
Liebig K, et al. Tick populations from endemic and non-endemic areas in Germany show differential susceptibility to TBEV. Sci. Rep. 2020 doi: 10.1038/s41598-020-71920-z. PubMed DOI PMC
Ciota AT, et al. Effects of Zika virus strain and Aedes mosquito species on vector competence. Emerg. Infect. Dis. 2017;23(7):1110–1117. PubMed PMC
Zouache K, et al. Three-way interactions between mosquito population, viral strain and temperature underlying chikungunya virus transmission potential. Proc. R. Soc. B Biol. Sci. 2014;281(1792):20141078. PubMed PMC
Paslaru AI, Mathis A, Torgerson P, Veronesi E. Vector competence of pre-alpine Culicoides (Diptera: Ceratopogonidae) for bluetongue virus serotypes 1, 4 and 8. Parasit. Vectors. 2018;11(1):1–12. PubMed PMC
Moutailler S, Krida G, Schaffner F, Vazeille M, Failloux AB. Potential vectors of Rift Valley fever virus in the Mediterranean region. Vector-Borne Zoonotic Dis. 2008;8(6):749–754. PubMed
Vega-Rua A, Zouache K, Girod R, Failloux A-B, Lourenco-de-Oliveira R. High level of vector competence of Aedes aegypti and Aedes albopictus from ten American countries as a crucial factor in the spread of Chikungunya Virus. J. Virol. 2014;88(11):6294–6306. PubMed PMC
Veronesi E, et al. Measurement of the infection and dissemination of Bluetongue Virus in culicoides biting midges using a semi-quantitative RT-PCR assay and isolation of infectious virus. PLoS ONE. 2013;8(8):1–8. PubMed PMC
Wallner G, et al. Characterization and complete genome sequences of high- and low-virulence variants of tick-borne encephalitis virus. J. Gen. Virol. 1996;77(5):1035–1042. PubMed
Yasumura Y, Kawakita Y. Studies on SV40 in tissue culture-preliminary step for cancer research in vitro. Nihon Rinsho. 1963;21:1201–1212.
Sato M, Maeda N, Yoshida H, Urade M, Saito S. Plaque formation of herpes virus hominis type 2 and rubella virus in variants isolated from the colonies of BHK21/WI-2 cells formed in soft agar. Arch. Virol. 1977;53(3):269–273. PubMed
Mohd Jaafar F, et al. Immunisation with bacterial expressed VP2 and VP5 of bluetongue virus (BTV) protect α/β interferon-receptor knock-out (IFNAR-/-) mice from homologous lethal challenge. Vaccine. 2014;32(32):4059–4067. PubMed
Mohd Jaafar F, Attoui H, Mertens PPC, De Micco P, De Lamballerie X. Structural organization of an encephalitic human isolate of Banna virus (genus Seadornavirus, family Reoviridae ) Printed in Great Britain. J. Gen. Virol. 2005;86:1147–1157. PubMed
Helmová R, Hönig V, Tykalová H, Palus M, Bell-Sakyi L, Grubho L. Tick-borne encephalitis virus adaptation in different host environments and existence of quasispecies. Viruses. 2020;12(8):1–17. PubMed PMC
Huang S, et al. Immune response in mice that lack the interferon-gamma receptor (see comments) Science. 1993;259:1742–1745. PubMed
Müller U, et al. Functional role of type I and type II interferons in antiviral defense. Science. 1994;264:1918–1921. PubMed
Weber E, et al. Type I interferon protects mice from fatal neurotropic infection with Langat virus by systemic and local antiviral responses. J. Virol. 2014;88(21):12202–12212. PubMed PMC
Karabatsos N. International Catalogue of Arboviruses, Including Certain Other Viruses of Vertebrates. 3. American Society of Tropical Medicine and Hygiene for The Subcommittee on Information Exchange of the American Committee on Arthropod-borne Viruses; 1985.
Calvo-Pinilla E, Rodríguez-Calvo T, Anguita J, Sevilla N, Ortego J. Establishment of a bluetongue virus infection model in mice that are deficient in the alpha/beta interferon receptor. PLoS ONE. 2009;4(4):e5171. PubMed PMC
Haviernik J, et al. An E460D substitution in the NS5 protein of tick-borne encephalitis virus confers resistance to the inhibitor Galidesivir (BCX4430) and also attenuates the virus in mice. Proceedings. 2020;50(1):12. PubMed PMC
Radda A, Hofmann H, Pretzmann G. Threshold of viraemia in Apodemus flavicollis for infection of Ixodes ricinus with tick-borne encephalitis virus. Acta Virol. 1969;13(1):74–77. PubMed
Chunikhin SP, Kurenkov V. Viraemia in Clethrionomys glareolus—A new ecological marker of tick-borne encephalitis virus. Acta Virol. 1979;23(3):257–260. PubMed
Mateos Hernandez L. A capsule-based model for immature hard tick stages infestation on laboratory mice. JoVE. 2020 doi: 10.3791/61430. PubMed DOI
Attoui H, Billoir F, Cantaloube JF, Biagini P, De Micco P, De Lamballerie X. Strategies for the sequence determination of viral dsRNA genomes. J. Virol. Methods. 2000;89(1–2):147–158. PubMed
Gondard M, et al. Prevalence of tick-borne viruses in Ixodes ricinus assessed by high-throughput real-time PCR. Pathog. Dis. 2018;76(8):1–13. PubMed
Schwaiger M, Cassinotti P. Development of a quantitative real-time RT-PCR assay with internal control for the laboratory detection of tick borne encephalitis virus (TBEV) RNA. J. Clin. Virol. 2003;27:136–145. PubMed