Abstract
Murid herpesvirus 4 (MuHV 4) strain 68 (MHV-68) is a natural pathogen of murid rodents, which serves as hosts to Dermacentor reticulatus ticks. These ticks are known to transmit multiple pathogens, which can cause diseases in humans and animals. Recently, the detection of MHV-68 antibodies in the blood of animals living in the same biotope as virus-infected mice has suggested the role of ticks in pathogen circulation in nature. Herein, to identify MHV-68 in D. reticulatus ticks, DNA samples from 432 adults were collected at two sites in southwestern Slovakia from 2011 to 2014. Samples were examined by polymerase chain reaction (PCR), targeting ORF50 of MHV-68. Ignoring season and locality, we have found 25.9 % of the male and 44.9 % of the female ticks to be positive. Within ticks collected in Vojka, 40 % (125/312) became positive, at a rate of approximately 6.8 times higher in spring than in autumn (66 vs 9.7 %). In addition, in the spring, 1.4 times more females were positive than males. Within ticks collected in Gabčíkovo, 23.3 % (28/120) became positive, with positive females being twice as frequent. The infecting virus was identified by analyzing amplified products via sequencing and restriction fragment length polymorphism (RFLP) analyses. Using an explantation/co-cultivation procedure, we examined the salivary glands, intestines, and ovaries of five females for live MHV-68. In all organs of two ticks, we identified a virus capable of replication in mammalian cells. This is the first report of MHV-68 detection in D. reticulatus ticks and of a live virus in their organs. Findings encourage further study to determine whether this potential arbovirus, found in salivary glands, is transmissible. It further supports the hypothesis regarding the mediating role of ticks in MHV-68 circulation in nature.
Similar content being viewed by others
References
Blaškovič D, Stančeková M, Svobodová J, Mistríková J (1980) Isolation of five strains of herpesviruses from two species of free-living small rodents. Acta Virol 24:468
Rajčáni J, Kúdelová M (2007) Murid herpesvirus 4 (MHV-4): an animal model for human gammaherpesvirus research. In: Minarovits J, Gonczol E, Valyi-Nagy T (eds) Latency strategies of herpesviruses. Chapt V. Springer, Berlin, pp 102–136
Blasdell K, McCracken C, Morris A, Nash AA, Begon M, Bennett M, Stewart JP (2003) The wood mouse is a natural host for Murid herpesvirus 4. J Gen Virol 84:111–113
Ehlers B, Kuchler J, Yasmum N, Dural D, Voigt S, Schmidt-Chanasit J, Jäkel T, Matuschka FR, Richter D, Essbauer S, Hughes DJ, Summers C, Bennett M, Stewart JP, Ulrich RG (2007) Identification of novel rodent herpesviruses, including the first gammaherpesvirus of Mus musculus. J Virol 81:8091–8100
Hughes DJ, Kipar A, Milligan SG, Cunningham C, Sanders M, Quail MA, Rajandream M-A, Stewart JP (2010) Characterization of a novel wood mouse virus related to murid herpesvirus 4. J Gen Virol 9:867–879
Loh J, Zhao G, Nelson CA, Coder P, Droit L et al (2011) Identification and sequencing of a novel rodent gammaherpesvirus that establishes acute and latent infection in laboratory mice. J Virol 85(6):2642–2656
Nash AA, Dutia BM, Stewart JP, Davison AJ (2001) Natural history of murine gamma-herpesvirus infection. Philos Trans R Soc Lond B Biol Sci 356(1408):569–579
Rajčáni J, Blaškovič D, Svobodová J, Čiampor F, Hučková D, Staneková D (1985) Pathogenesis of acute and persistent murine herpesvirus infection in mice. Acta Virol 29:51–60
Burri C, Schumann O, Schumann C, Gern L (2014) Are Apodemus spp. mice and Myodes glareolus reservoirs for Borrelia miyamotoi, Candidatus Neoehrlichia mikurensis, Rickettsia helvetica, R. monacensis and Anaplasma phagocytophilum? Ticks Tick-Borne Dis 5:245–251
Dantas-Torres F, Chomel BB, Otranto D (2012) Ticks and tick-borne diseases: a One Health perspective. Trends Parasitol 26(10):437–446
Nuttall PA (2009) Molecular characterization of tick-virus interactions. Front Biosci 14:2466–2483
Jori F, Vial L, Penrith ML, Pérez-Sánchez R, Etter E, Albina E, Michaud V, Roger F (2013) Review of the sylvatic cycle of African swine fever in sub-Saharan Africa and the Indian ocean. Virus Res 173(1):212–227
Labuda M, Nuttall P (2004) Tick-borne viruses. Parasitology 129:S221–S245
de la Fuente J, Estrada-Pena A, Venzal JM, Kocan KM, Sonenshine DE (2008) Overview: ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci 13:6938–6946
Estrada-Peña A, Jongejan F (1999) Ticks feeding on humans: a review ofrecords on human-biting Ixodoidea with special reference to pathogentransmission. Exp Appl Acarol 23(9):685–715
Martello E, Selmi M, Ragagli C, Ambrogi C, Stella MC, Mannelli A, Tomassone L (2013) Rickettsia slovaca in immature Dermacentor marginatus and tissues from Apodemus spp. in the northern Apennines, Italy. Ticks Ticks-Borne Dis 4:518–521
Reye AL, Stegniy V, Mishaeva NP, Velhin S, Hubschen JM, Ignatyev G, Muller CP et al (2013) Prevalence of Tick-Borne Pathogens in Ixodes ricinus and Dermacentor reticulatus ticks from different geographical locations in Belarus. PLoS ONE 8(1):e54476
Hubálek Z, Sixl W, Halouzka J (1998) Francisella tularensis in Dermacentor reticulatus ticks from the Czech Republic and Austria. Wien Klin Wochenschr 110(24):909–910
Nosek J (1972) The ecology and public health importance of Dermacentor marginatus and D. reticulatus ticks in Central Europe. Folia Parasitol 19:93–102
Špitalská E, Kocianová E (2003) Detection of Coxiella burnetii in tickscollected in Slovakia and Hungary. Eur J Epidemiol 18(3):263–266
Švehlová A, Berthová L, Sallay B, Boldiš V, Olivier A, Sparagano E, Špitalská E (2014) Sympatric occurrence of Ixodes ricinus, Dermacentor reticulatus and Haemaphysalis concinna ticks and their pathogens Rickettsia and Babesia species in Slovakia. Ticks Tick-Borne Dis 5(5):600–605
Wójcik-Fatla A, Bartosik K, Buczek A, Dutkiewicz J (2012) Babesia microti in adult Dermacentor reticulatus ticks from Eastern Poland. Vector Borne Zoonotic Dis 12(10):841–843
Wójcik-Fatla A, Cisak E, Zając V, Zwoliński J, Dutkiewicz J (2011) Prevalenceof tick-borne encephalitis virus in Ixodes ricinus and Dermacentor reticulatus ticks collected from the Lublin region (eastern Poland). Ticks Tick Borne Dis 2(1):16–19
Buczek A, Bartosik K, Wiśniowski Ł, Tomasiewicz K (2013) Changes in population abundance of adult Dermacentor reticulatus (Acari: Amblyommidae) in long-term investigations in eastern Poland. Ann Agric Environ Med 20(2):269–272
Bullová E, Lukan M, Stanko M, Pet’ko B (2009) Spatial distribution of Dermacentor reticulatus tick in Slovakia in the beginning of the 21st century. Vet Parazit 165(3–4):357–360
Dautel H, Dippel C, Oehme R, Hartelt K, Schettler E (2006) Evidence for an increased geographical distribution of Dermacentor reticulatus in Germany and detection of Rickettsia sp. RpA4. Inter J Med Microbiol 296(Suppl 40):149–156
Hubálek Z, Rudolf I (2012) Tick-borne viruses in Europe. Parasitol Res 111:9–36
Wielinga PR, Gaasenbeek C, Fonville M, de Boer A, de Vries A, Dimmers W, Akkerhuis OP, Jagers G, Schouls LM, Borgsteede F, van der Giessen JW (2006) Longitudinal analysis of tick densities and Borrelia, Anaplasma, and Ehrlichia infections of Ixodes ricinus ticks in different habitat areas in The Netherlands. Appl Environ Microbiol 72:7594–7601
Ficová M, Betáková T, Pančík P, Václav R, Prokop P, Halásová Z, Kúdelová M (2011) Molecular detection of murine herpesvirus 68 in ticks feeding on free-living reptiles. Microb Ecol 62(1):862–867
Mistríková J, Kožuch O, Klempa B, Kontseková E, Labuda M, Mrmusová M (2000) New findings on the ecology and epidemiology of murine herpes virus isolated in Slovakia. Bratisl Lek Listy 101(3):157–162
Hricová M, Mistríková J (2007) Murine gammaherpesvirus 68 serum antibodies in general human population. Acta Virol 51(4):283–287
Rijpkema SGT, Herbes RG, Verbeek-de Kruif N, Schellekens JFP (1996) Detection of four species of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected from roe deer (Capreolus capreolus) in the Netherlands. Epidemiol Infect 117:563–566
Margolis TP, Elfman FL, Leib D, Pakpour N, Apakupakul K, Imai Y, Voyte C (2007) Spontaneous reactivation of herpes simplex virus type 1 in latently infected murine sensory ganglia. J Virol 80(20):11069–11074
Rajčáni J, Čiampor F, Sabo A (1975) Experimental latent herpesvirus infection in rabbits, mice and hamsters: ultrastructure of virus activation in the explanted Gasserian ganglion. Acta Virol 19:19–28
Belvončíková P, Kráľová A, Kúdelová M, Hajnická V, Režuchová I, Vančová I (2008) Chemokine-binding activities of M3 protein encoded by murine gammaherpesvirus 72. Acta Virol 52:91–97
Weck KE, Kim SS, Virgin HW, Speck SH (1999) B cells regulate murine gammaherpesvirus 68 latency. J Virol 73:4651–4661
Virgin HW IV, Latreille P, Wamsley P, Hallsworth K, Weck KE, Dal Canto AJ, Speck SH (1997) Complete sequence and genomic analysis of Murine gammaherpesvirus 68. J Virol 71:5894–5904
Mačáková K, Matis J, Režuchová I, Kúdela O, Rašlová H, Kúdelová M (2003) Murine gammaherpesvirus M7 gene encoding gp 150: difference in the sequence between 72 and 68 strains. Virus Genes 26:89–95
Adler H, Messerle M, Wagner M, Koszinowski UH (2000) Cloning and mutagenesis of the murine gammaherpesvirus 68 genome as an infectious bacterial artificial chromosome. J Virol 74:6964–6974
Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9
Frey S, Essbauer S, Zoeller G, Klempa B, Dobler G, Pfeffer M (2014) Full genome sequences and preliminary molecular characterization of three tick-borne encephalitis virus strains isolated from ticks and a bank vole in Slovak Republic. Virus Genes 48(1):184–188
Rašlová H, Berebbi M, Rajčáni J, Sarasin A, Matis J, Kúdelová M (2001) Susceptibility of mouse mammary glands to Murine gammaherpesvirus 72 (MHV-72) infection: evidence of MHV-72 transmission via breast milk. Microb Pathog 31:47–58
Stančeková M, Golais F, Leššo J (1992) Some physicochemical properties of murine herpesvirus. Acta Virol 36(2):201–203
Estrada-Peña A, Gray JS, Kahl O, Lane RS, Nijhof AM (2013) Research on the ecology of ticks and tick-borne pathogens—methodological principles and caveats. Front Cell Inf Microbiol 3:29
Acknowledgment
This work was supported by the joint grant agency of the Slovak Ministry of Education and Slovak Academy of Sciences VEGA (#2/091/13) and by the Slovak Research and Development Agency (#APVV-0621-12).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kúdelová, M., Belvončíková, P., Vrbová, M. et al. Detection of Murine Herpesvirus 68 (MHV-68) in Dermacentor reticulatus Ticks. Microb Ecol 70, 785–794 (2015). https://doi.org/10.1007/s00248-015-0622-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-015-0622-7