ksmaКубанский научный медицинский вестникKuban Scientific Medical Bulletin1608-62282541-9544Kuban State Medical University10.25207/1608-6228-2019-26-3-117-128ksma-1788Research ArticleОБЗОРЫREVIEWХАРАКТЕРИСТИКА ВИРУСА ЭНЦЕФАЛОМИОКАРДИТА И ЕГО ЗООНОЗНЫЙ ПОТЕНЦИАЛ (ОБЗОР ЛИТЕРАТУРЫ). ЧАСТЬ II. ПАТОГЕНЕЗ. КРУГ ВОСПРИИМЧИВЫХ ОРГАНИЗМОВTHE ENCEPHALOMYOCARDITIS VIRUS (EMCV) AND ITS ZOONOTIC POTENTIAL (A LITERATURE REVIEW). PART II. PATHOGENESIS. THE CIRCLE OF SUSCEPTIBLE ORGANISMSКалайджянА. А.KalajdzhjanAkop A.

аспирант лаборатории молекулярной биологии,

ул. Мира, д. 177, г. Сочи, 354376

PhD Researcher, Laboratory of Molecular Biology,

Mira str., 177, Sochi, 354376

КадеА. Х.KadeAzamat Kh.

доктор медицинских наук, профессор, заведующий кафедрой общей и клинической патологической физиологии,

ул. им. Митрофана Седина, д. 4, г. Краснодар, 350063

Dr. Sci. (Med.), Prof., Head of Department, Department of General and Clinical Pathological Physiology,

Mitrofanа Sedinа str., 4, Krasnodar, 350063

ПоляковП. П.PolyakovPavel P.

ассистент кафедры общей и клинической патологической физиологии,

ул. им. Митрофана Седина, д. 4, г. Краснодар, 350063;

тел.: +7 (861) 262-40-31

Research Assistant, Department of General and Clinical Pathological Physiology,

Mitrofanа Sedinа str., 4, Krasnodar, 350063;

tel.:+7 (861) 262-40-31

pal.pal.p@yandex.ruГудмановаА. И.GudmanovaAlla I.

врач-терапевт,

ул. Айвазовского, д. 97, г. Краснодар, 350040

Physician,

Aivazovskogo str., 97, Krasnodar, 350040

Федеральное государственное бюджетное научное учреждение «Научно-исследовательский институт медицинской приматологии»РоссияScientifc Research Institute of Medical PrimatologyRussian FederationФедеральное государственное бюджетное образовательное учреждение высшего образования «Кубанский государственный медицинский университет» Министерства здравоохранения Российской ФедерацииРоссияKuban State Medical University, Ministry of Healthcare of the Russian FederationRussian FederationГосударственное бюджетное учреждение здравоохранения «Городская клиническая больница № 3 города Краснодара» Министерства здравоохранения Краснодарского краяРоссияKrasnodar City Clinical Hospital No. 3, Ministry of Healthcare of Krasnodar KraiRussian Federation201906072019263117128Copyright © Калайджян А.А., Каде А.Х., Поляков П.П., Гудманова А.И., 20192019Калайджян А.А., Каде А.Х., Поляков П.П., Гудманова А.И.Kalajdzhjan A.A., Kade A.K., Polyakov P.P., Gudmanova A.I.This work is licensed under a Creative Commons Attribution 4.0 License.https://ksma.elpub.ru/jour/article/view/1788

Среди факторов вирулентности ЭМКВ в литературе выделяют как непосредственное действие вирусных белков (В2*, L, 2A), так и воспалительную реакцию организма. В зависимости от штамма ЭМКВ и вида инфицированного животного существуют особенности в выраженности и характере клинических проявлений заболевания. Также установлены различия патогенетических механизмов тканевых поражений в зависимости от величины инфицирующей дозы вируса, как, например, при развитии ЭМКВ-индуцированного диабета. Действие вируса in vivo изучалось на примерах свиней, грызунов и обезьян. Круг поражаемых животных весьма широк, а инфекция распространена практически повсеместно. В том числе немало работ описывает достаточно высокую иммунологическую прослойку среди людей, а также вспышки заболеваний среди населения. Таким образом, ЭМКВ представляет опасность не только для зоопарков и приматологических центров, но имеет явный зоонозный потенциал.

According to literature data, both the direct action of (B2 *, L, 2A) viral proteins and the inflammatory response of the body are distinguished among the Encephalomyocarditis virus (EMCV) virulence factors. Depending on the EMCV strain and the type of the infected animal, the severity and nature of the disease is shown to be characterized by specific clinical manifestations. Differences in the pathogenetic mechanisms of tissue lesions depending on the magnitude of the virus infectious dose are established, e.g., in the development of EMCV-induced diabetes. The EMCV action was studied in vivo on such experimental animals as pigs, rodents and monkeys. The range of affected animals is extremely wide, with the infection being common almost everywhere. Thus, numerous works describe a fairly high immunological stratum among people, as well as disease outbreaks among the population. It is concluded that EMCV is dangerous not only for zoos and primatological centres, but also has a clear zoonotic potential.

вирус энцефаломиокардитаЭМКВ-индуцированный диабетЭМКВиндуцированный миокардитфакторы вирулентности ЭМКВencephalomyocarditis virusEMCV-induced diabetesEMCV-induced myocarditisEMCV virulence factorsReferencesCarocci M., Bakkali-Kassimi L. The encephalomyocarditis virus. Virulence. 2012; 3 (4): 351–367. DOI: 10.4161/viru.20573Carocci M., Bakkali-Kassimi L. The encephalomyocarditis virus. Virulence. 2012; 3 (4): 351–367. DOI: 10.4161/viru.20573Loughran G., Firth A.E., Atkins J.F. Ribosomal frameshifting into an overlapping gene in the 2B-encoding region of the cardiovirus genome. Proc. Natl. Acad. Sci. USA. 2011; 108(46): E1111–E1119. DOI: 10.1073/pnas.1102932108Loughran G., Firth A.E., Atkins J.F. Ribosomal frameshifting into an overlapping gene in the 2B-encoding region of the cardiovirus genome. Proc. Natl. Acad. Sci. USA. 2011; 108(46): E1111–E1119. DOI: 10.1073/pnas.1102932108Balvay L., Soto Rifo R., Ricci E.P., Decimo D., Ohlmann T. Structural and functional diversity of viral IRESes. Biochim. Biophys. Acta. 2009; 1789(9-10): 542–557. DOI: 10.1016/j.bbagrm.2009.07.005Balvay L., Soto Rifo R., Ricci E.P., Decimo D., Ohlmann T. Structural and functional diversity of viral IRESes. Biochim. Biophys. Acta. 2009; 1789(9-10): 542–557. DOI: 10.1016/j.bbagrm.2009.07.005Papon L., Oteiza A., Imaizumi T., Kato H., Brocchi E., Lawson T.G., Akira S., Mechti N. The viral RNA recognition sensor RIG-I is degraded during encephalomyocarditis virus (EMCV) infection. Virology. 2009; 393(2): 311–318. DOI: 10.1016/j.virol.2009.08.009Papon L., Oteiza A., Imaizumi T., Kato H., Brocchi E., Lawson T.G., Akira S., Mechti N. The viral RNA recognition sensor RIG-I is degraded during encephalomyocarditis virus (EMCV) infection. Virology. 2009; 393(2): 311–318. DOI: 10.1016/j.virol.2009.08.009de Jong A.S., de Mattia F., Van Dommelen M.M., Lanke K., Melchers W.J., Willems P.H., van Kuppeveld F.J. Functional analysis of picornavirus 2B proteins: effects on calcium homeostasis and intracellular protein traffcking. J. Virol. 2008; 82(7): 3782–3790. DOI: 10.1128/JVI.02076-07de Jong A.S., de Mattia F., Van Dommelen M.M., Lanke K., Melchers W.J., Willems P.H., van Kuppeveld F.J. Functional analysis of picornavirus 2B proteins: effects on calcium homeostasis and intracellular protein traffcking. J. Virol. 2008; 82(7): 3782–3790. DOI: 10.1128/JVI.02076-07Choe S.S., Dodd D.A., Kirkegaard K. Inhibition of cellular protein secretion by picornaviral 3A proteins. Virology. 2005; 337(1): 18–29. DOI: 10.1016/j.virol.2005.03.036Choe S.S., Dodd D.A., Kirkegaard K. Inhibition of cellular protein secretion by picornaviral 3A proteins. Virology. 2005; 337(1): 18–29. DOI: 10.1016/j.virol.2005.03.036Moffat K., Knox C., Howell G., Clark S.J., Yang H., Belsham G.J., Ryan М., Wileman Т. Inhibition of the secretory pathway by foot-and-mouth disease virus 2BC protein is reproduced by coexpression of 2B with 2C, and the site of inhibition is determined by the subcellular location of 2C. J. Virol. 2007; 81(3): 1129–1139. DOI: 10.1128/JVI.00393-06Moffat K., Knox C., Howell G., Clark S.J., Yang H., Belsham G.J., Ryan М., Wileman Т. Inhibition of the secretory pathway by foot-and-mouth disease virus 2BC protein is reproduced by coexpression of 2B with 2C, and the site of inhibition is determined by the subcellular location of 2C. J. Virol. 2007; 81(3): 1129–1139. DOI: 10.1128/JVI.00393-06Canelli E., Luppi A., Lavazza A., Lelli D., Sozzi E., Martin A.M., Gelmetti D., Pascotto E., Sandri C., Magnone W., Cordioli P. Encephalomyocarditis virus infection in an Italian zoo. Virol. J. 2010; 7: 64. DOI: 10.1186/1743-422X-7-64Canelli E., Luppi A., Lavazza A., Lelli D., Sozzi E., Martin A.M., Gelmetti D., Pascotto E., Sandri C., Magnone W., Cordioli P. Encephalomyocarditis virus infection in an Italian zoo. Virol. J. 2010; 7: 64. DOI: 10.1186/1743-422X-7-64Czechowicz J., Huaman J.L., Forshey B.M., Morrison A.C., Castillo R., Huaman A., Caceda R., Eza D., Rocha C., Blair P.J., Olson J.G., Kochel T.J. Prevalence and risk factors for encephalomyocarditis virus infection in Peru. Vector. Borne. Zoonotic. Dis. 2011; 11(4): 367–374. DOI: 10.1089/vbz.2010.0029Czechowicz J., Huaman J.L., Forshey B.M., Morrison A.C., Castillo R., Huaman A., Caceda R., Eza D., Rocha C., Blair P.J., Olson J.G., Kochel T.J. Prevalence and risk factors for encephalomyocarditis virus infection in Peru. Vector. Borne. Zoonotic. Dis. 2011; 11(4): 367–374. DOI: 10.1089/vbz.2010.0029Oberste M.S., Gotuzzo E., Blair P., Nix W.A., Ksiazek T.G., Comer J.A., Rollin Р., Goldsmith С.S., Olson J., Koche T.J. Human febrile illness caused by encephalomyocarditis virus infection, Peru. Emerg. Infect. Dis. 2009; 15(4): 640–646. DOI: 10.3201/eid1504.081428Oberste M.S., Gotuzzo E., Blair P., Nix W.A., Ksiazek T.G., Comer J.A., Rollin Р., Goldsmith С.S., Olson J., Koche T.J. Human febrile illness caused by encephalomyocarditis virus infection, Peru. Emerg. Infect. Dis. 2009; 15(4): 640–646. DOI: 10.3201/eid1504.081428An D.-J., Jeong W., Jeoung H.-Y., Yoon S.H., Kim H.J., Choi C.U., Park B.K. Encephalomyocarditis in Korea: serological survey in pigs and phylogenetic analysis of two historical isolates. Vet. Microbiol. 2009; 137(1–2): 37–44. DOI: 10.1016/j.vetmic.2009.01.005An D.-J., Jeong W., Jeoung H.-Y., Yoon S.H., Kim H.J., Choi C.U., Park B.K. Encephalomyocarditis in Korea: serological survey in pigs and phylogenetic analysis of two historical isolates. Vet. Microbiol. 2009; 137(1–2): 37–44. DOI: 10.1016/j.vetmic.2009.01.005Ge X., Zhao D., Liu C., Wang F., Guo X, Yang H. Seroprevalence of encephalomyocarditis virus in intensive pig farms in China. Vet. Rec. 2010; 166(5): 145–146. DOI: 10.1136/vr.b4766Ge X., Zhao D., Liu C., Wang F., Guo X, Yang H. Seroprevalence of encephalomyocarditis virus in intensive pig farms in China. Vet. Rec. 2010; 166(5): 145–146. DOI: 10.1136/vr.b4766Billinis C. Encephalomyocarditis virus infection in wildlife species in Greece. J. Wildl. Dis. 2009; 45(2): 522–526.Billinis C. Encephalomyocarditis virus infection in wildlife species in Greece. J. Wildl. Dis. 2009; 45(2): 522–526.Psalla D., Psychas V., Spyrou V., Billinis C., Papaioannou N., Vlemmas I. Pathogenesis of experimental encephalomyocarditis: a histopathological, immunohistochemical and virological study in rats. J. Comp. Pathol. 2006; 134(1): 30–39. DOI: 10.1016/j.jcpa.2005.06.008Psalla D., Psychas V., Spyrou V., Billinis C., Papaioannou N., Vlemmas I. Pathogenesis of experimental encephalomyocarditis: a histopathological, immunohistochemical and virological study in rats. J. Comp. Pathol. 2006; 134(1): 30–39. DOI: 10.1016/j.jcpa.2005.06.008Spyrou V., Maurice H., Billinis C., Papanastassopoulou M., Psalla D., Nielen M. Transmission and pathogenicity of encephalomyocarditis virus (EMCV) among rats. Vet. Res. 2004; 35(1): 113–122. DOI: 10.1051/vetres:2003044Spyrou V., Maurice H., Billinis C., Papanastassopoulou M., Psalla D., Nielen M. Transmission and pathogenicity of encephalomyocarditis virus (EMCV) among rats. Vet. Res. 2004; 35(1): 113–122. DOI: 10.1051/vetres:2003044Kluivers M., Maurice H., Vyt P., Koenen F., Nielen M. Transmission of encephalomyocarditis virus in pigs estimated from feld data in Belgium by means of R0. Vet Res. 2006; 37(6): 757–766. DOI: 10.1051/vetres:2006035Kluivers M., Maurice H., Vyt P., Koenen F., Nielen M. Transmission of encephalomyocarditis virus in pigs estimated from feld data in Belgium by means of R0. Vet Res. 2006; 37(6): 757–766. DOI: 10.1051/vetres:2006035Koenen F. Chapter 17: Encephalomyocarditis Virus. In: Straw B.E., D’Allaire S., Zimmerman J.J., Taylor D.J, editors. Disease of the Swine. 9th ed. Boston: Blackwell Science; 2006.Koenen F. Chapter 17: Encephalomyocarditis Virus. In: Straw B.E., D’Allaire S., Zimmerman J.J., Taylor D.J, editors. Disease of the Swine. 9th ed. Boston: Blackwell Science; 2006.Juncker-Voss M., Prosl H., Lussy H., Enzenberg U., Auer H., Lassnig H., Müller M., Nowotny N. Screening for antibodies against zoonotic agents among employees of the Zoological Garden of Vienna, Schönbrunn, Austria. Berl. Munch. Tierarztl. Wochenschr. 2004; 117(9–10): 404–409.Juncker-Voss M., Prosl H., Lussy H., Enzenberg U., Auer H., Lassnig H., Müller M., Nowotny N. Screening for antibodies against zoonotic agents among employees of the Zoological Garden of Vienna, Schönbrunn, Austria. Berl. Munch. Tierarztl. Wochenschr. 2004; 117(9–10): 404–409.Masek-Hammerman K., Miller A.D., Lin K.C., MacKey J., Weissenböck H., Gierbolini L., Burgos A., Perez H., Mansfeld K.G. Epizootic myocarditis associated with encephalomyocarditis virus in a group of rhesus macaques (Macaca mulatta). Vet. Pathol. 2012; 49(2): 386–392. DOI: 10.1177/0300985811409254Masek-Hammerman K., Miller A.D., Lin K.C., MacKey J., Weissenböck H., Gierbolini L., Burgos A., Perez H., Mansfeld K.G. Epizootic myocarditis associated with encephalomyocarditis virus in a group of rhesus macaques (Macaca mulatta). Vet. Pathol. 2012; 49(2): 386–392. DOI: 10.1177/0300985811409254Gelmetti D., Meroni A., Brocchi E., Koenen F., Cammarata G. Pathogenesis of encephalomyocarditis experimental infection in young piglets: a potential animal model to study viral myocarditis. Vet Res. 2006; 37(1): 15–23. DOI: 10.1051/vetres:2005041Gelmetti D., Meroni A., Brocchi E., Koenen F., Cammarata G. Pathogenesis of encephalomyocarditis experimental infection in young piglets: a potential animal model to study viral myocarditis. Vet Res. 2006; 37(1): 15–23. DOI: 10.1051/vetres:2005041Psalla D., Psychas V., Spyrou V., Billinis C., Papaioannou N., Vlemmas I. Pathogenesis of experimental encephalomyocarditis: a histopathological, immunohistochemical and virological study in mice. J. Comp. Pathol. 2006; 135(2–3): 142–145. DOI: 10.1016/j.jcpa.2006.04.003Psalla D., Psychas V., Spyrou V., Billinis C., Papaioannou N., Vlemmas I. Pathogenesis of experimental encephalomyocarditis: a histopathological, immunohistochemical and virological study in mice. J. Comp. Pathol. 2006; 135(2–3): 142–145. DOI: 10.1016/j.jcpa.2006.04.003Yoon J.-W., Jun H.-S. Viruses cause type 1 diabetes in animals. Ann. NY Acad. Sci. 2006; 1079(1): 138–146. DOI: 10.1196/annals.1375.021Yoon J.-W., Jun H.-S. Viruses cause type 1 diabetes in animals. Ann. NY Acad. Sci. 2006; 1079(1): 138–146. DOI: 10.1196/annals.1375.021Nakayama Y., Su W., Ohguchi A., Nakayama H., Doi K. Experimental encephalomyocarditis virus infection in pregnant mice. Exp. Mol. Pathol. 2004; 77(2): 133–137. DOI: 10.1016/j.yexmp.2004.02.003Nakayama Y., Su W., Ohguchi A., Nakayama H., Doi K. Experimental encephalomyocarditis virus infection in pregnant mice. Exp. Mol. Pathol. 2004; 77(2): 133–137. DOI: 10.1016/j.yexmp.2004.02.003Yamanouchi-Ueno A., Nakayama Y., Doi K. Characteristics of testicular lesions in mice infected with a low dose of encephalomyocarditis (EMC) virus. Exp. Mol. Pathol. 2004; 77(2): 72–76. DOi: 10.1016/j.yexmp.2003.12.008Yamanouchi-Ueno A., Nakayama Y., Doi K. Characteristics of testicular lesions in mice infected with a low dose of encephalomyocarditis (EMC) virus. Exp. Mol. Pathol. 2004; 77(2): 72–76. DOi: 10.1016/j.yexmp.2003.12.008Doi K. Experimental encephalomyocarditis virus infection in small laboratory rodents. J. Comp. Pathol. 2011; 144(1): 25–40. DOI: 10.1016/j.jcpa.2010.05.001Doi K. Experimental encephalomyocarditis virus infection in small laboratory rodents. J. Comp. Pathol. 2011; 144(1): 25–40. DOI: 10.1016/j.jcpa.2010.05.001Matsumori A., Yamamoto K., Shimada M. Cetirizine a histamine H1 receptor antagonist improves viral myocarditis. J. Inflamm. (Lond). 2010; 7: 39. DOI: 10.1186/1476-9255-7-39Matsumori A., Yamamoto K., Shimada M. Cetirizine a histamine H1 receptor antagonist improves viral myocarditis. J. Inflamm. (Lond). 2010; 7: 39. DOI: 10.1186/1476-9255-7-39Wang J.-F., Meissner A., Malek S., Chen Y., Ke Q., Zhang J., Chu V., Hampton T.G., Crumpacker C.S., Abelmann W.H., Amende I., Morgan J.P. Propranolol ameliorates and epinephrine exacerbates progression of acute and chronic viral myocarditis. Am. J. Physiol. Heart Circ. Physiol. 2005; 289(4): H1577–1583. DOI: 10.1152/ajpheart.00258.2005Wang J.-F., Meissner A., Malek S., Chen Y., Ke Q., Zhang J., Chu V., Hampton T.G., Crumpacker C.S., Abelmann W.H., Amende I., Morgan J.P. Propranolol ameliorates and epinephrine exacerbates progression of acute and chronic viral myocarditis. Am. J. Physiol. Heart Circ. Physiol. 2005; 289(4): H1577–1583. DOI: 10.1152/ajpheart.00258.2005Matsumori A., Nunokawa Y., Yamaki A., Yamamoto K., Hwang M.W., Miyamoto T., Hara M., Nishio R., Kitaura-Inenaga K., Ono K. Suppression of cytokines and nitric oxide production, and protection against lethal endotoxemia and viral myocarditis by a new NF-kappaB inhibitor. Eur. J. Heart. Fail. 2004; 6(2): 137–144. DOI: 10.1016/j.ejheart.2003.10.007Matsumori A., Nunokawa Y., Yamaki A., Yamamoto K., Hwang M.W., Miyamoto T., Hara M., Nishio R., Kitaura-Inenaga K., Ono K. Suppression of cytokines and nitric oxide production, and protection against lethal endotoxemia and viral myocarditis by a new NF-kappaB inhibitor. Eur. J. Heart. Fail. 2004; 6(2): 137–144. DOI: 10.1016/j.ejheart.2003.10.007Nasu-Nishimura Y., Taniuchi Y., Nishimura T., Sakudo A., Nakajima K., Ano Y., Sugiura K., Sakaguchi S., Itohara S., Onodera T. Cellular prion protein prevents brain damage after encephalomyocarditis virus infection in mice. Arch. Virol. 2008; 153(6): 1007–1012. DOI: 10.1007/s00705-008-0086-xNasu-Nishimura Y., Taniuchi Y., Nishimura T., Sakudo A., Nakajima K., Ano Y., Sugiura K., Sakaguchi S., Itohara S., Onodera T. Cellular prion protein prevents brain damage after encephalomyocarditis virus infection in mice. Arch. Virol. 2008; 153(6): 1007–1012. DOI: 10.1007/s00705-008-0086-xTakeda M., Ohtsuka R., Nakayama Y., Doi K. The role of CD4(+) T cells in biphasic hind limb paralysis induced by the D variant of encephalomyocarditis virus (EMC-D) in DBA/2 mice. Exp. Anim. 2004; 53(1): 31–35.Takeda M., Ohtsuka R., Nakayama Y., Doi K. The role of CD4(+) T cells in biphasic hind limb paralysis induced by the D variant of encephalomyocarditis virus (EMC-D) in DBA/2 mice. Exp. Anim. 2004; 53(1): 31–35.Ano Y., Sakudo A., Kimata T., Uraki R., Sugiura K., Onodera T. Oxidative damage to neurons caused by the induction of microglial NADPH oxidase in encephalomyocarditis virus infection. Neurosci. Lett. 2010; 469(1): 39–43. DOI: 10.1016/j.neulet.2009.11.040Ano Y., Sakudo A., Kimata T., Uraki R., Sugiura K., Onodera T. Oxidative damage to neurons caused by the induction of microglial NADPH oxidase in encephalomyocarditis virus infection. Neurosci. Lett. 2010; 469(1): 39–43. DOI: 10.1016/j.neulet.2009.11.040Bardina M.V., Lidsky P.V., Sheval E.V., Fominykh K.V., van Kuppeveld F.J., Polyakov V.Y., Agol V.I. Mengovirus-induced rearrangement of the nuclear pore complex: hijacking cellular phosphorylation machinery. J. Virol. 2009; 83(7): 3150–3161. DOI: 10.1128/JVI.01456-08Bardina M.V., Lidsky P.V., Sheval E.V., Fominykh K.V., van Kuppeveld F.J., Polyakov V.Y., Agol V.I. Mengovirus-induced rearrangement of the nuclear pore complex: hijacking cellular phosphorylation machinery. J. Virol. 2009; 83(7): 3150–3161. DOI: 10.1128/JVI.01456-08Porter F.W., Brown B., Palmenberg A.C. Nucleoporin phosphorylation triggered by the encephalomyocarditis virus leader protein is mediated by mitogen-activated protein kinases. J. Virol. 2010; 84(24): 12538–12548. DOI: 10.1128/JVI.01484-09Porter F.W., Brown B., Palmenberg A.C. Nucleoporin phosphorylation triggered by the encephalomyocarditis virus leader protein is mediated by mitogen-activated protein kinases. J. Virol. 2010; 84(24): 12538–12548. DOI: 10.1128/JVI.01484-09Porter F.W., Palmenberg A.C. Leader-induced phosphorylation of nucleoporins correlates with nuclear traffcking inhibition by cardioviruses. J. Virol. 2009; 83(4): 1941–1951. DOI: 10.1128/JVI.01752-08Porter F.W., Palmenberg A.C. Leader-induced phosphorylation of nucleoporins correlates with nuclear traffcking inhibition by cardioviruses. J. Virol. 2009; 83(4): 1941–1951. DOI: 10.1128/JVI.01752-08Porter F.W., Bochkov Y.A., Albee A.J., Wiese C., Palmenberg A.C. A picornavirus protein interacts with Ran-GTPase and disrupts nucleocytoplasmic transport. Proc. Natl. Acad. Sci. USA. 2006; 103(33): 12417–12422. DOI: 10.1073/pnas.0605375103Porter F.W., Bochkov Y.A., Albee A.J., Wiese C., Palmenberg A.C. A picornavirus protein interacts with Ran-GTPase and disrupts nucleocytoplasmic transport. Proc. Natl. Acad. Sci. USA. 2006; 103(33): 12417–12422. DOI: 10.1073/pnas.0605375103Borghese F., Michiels T. The leader protein of cardioviruses inhibits stress granule assembly. J. Virol. 2011; 85(18): 9614–9622. DOI: 10.1128/JVI.00480-11Borghese F., Michiels T. The leader protein of cardioviruses inhibits stress granule assembly. J. Virol. 2011; 85(18): 9614–9622. DOI: 10.1128/JVI.00480-11Okuwa T., Taniura N., Saito M., Himeda T., Ohara Y. Opposite effects of two nonstructural proteins of Theiler’s murine encephalomyelitis virus regulates apoptotic cell death in BHK-21 cells. Microbiol. Immunol. 2010; 54(10): 639–643. DOI: 10.1111/j.1348-0421.2010.00260.xOkuwa T., Taniura N., Saito M., Himeda T., Ohara Y. Opposite effects of two nonstructural proteins of Theiler’s murine encephalomyelitis virus regulates apoptotic cell death in BHK-21 cells. Microbiol. Immunol. 2010; 54(10): 639–643. DOI: 10.1111/j.1348-0421.2010.00260.xGroppo R., Palmenberg A.C. Cardiovirus 2A protein associates with 40S but not 80S ribosome subunits during infection. J. Virol. 2007; 81(23): 13067–13074. DOI: 10.1128/JVI.00185-07Groppo R., Palmenberg A.C. Cardiovirus 2A protein associates with 40S but not 80S ribosome subunits during infection. J. Virol. 2007; 81(23): 13067–13074. DOI: 10.1128/JVI.00185-07Groppo R., Brown B.A, Palmenberg A.C. Mutational analysis of the EMCV 2A protein identifes a nuclear localization signal and an eIF4E binding site. Virology. 2011; 410(1): 257–267. DOI: 10.1016/j.virol.2010.11.002Groppo R., Brown B.A, Palmenberg A.C. Mutational analysis of the EMCV 2A protein identifes a nuclear localization signal and an eIF4E binding site. Virology. 2011; 410(1): 257–267. DOI: 10.1016/j.virol.2010.11.002Ohguchi A., Nakayama Y., Yasoshima A., Doi C., Mikami T., Uetsuka K., Doi K. Encepalomyocarditis virus-induced apoptosis and ultrastructural changes in the lacrimal and parotid glands of mice. Exp. Mol. Pathol. 2006; 80(2): 201–207. DOI: 10.1016/j.yexmp.2005.06.003Ohguchi A., Nakayama Y., Yasoshima A., Doi C., Mikami T., Uetsuka K., Doi K. Encepalomyocarditis virus-induced apoptosis and ultrastructural changes in the lacrimal and parotid glands of mice. Exp. Mol. Pathol. 2006; 80(2): 201–207. DOI: 10.1016/j.yexmp.2005.06.003Buenz E.J., Sauer B.M., Lafrance-Corey R.G., Deb C., Denic A., German C.L., Howe C.L. Apoptosis of hippocampal pyramidal neurons is virus independent in a mouse model of acute neurovirulent picornavirus infection. Am. J. Pathol. 2009; 175(2): 668–684. DOI: 10.2353/ajpath.2009.081126Buenz E.J., Sauer B.M., Lafrance-Corey R.G., Deb C., Denic A., German C.L., Howe C.L. Apoptosis of hippocampal pyramidal neurons is virus independent in a mouse model of acute neurovirulent picornavirus infection. Am. J. Pathol. 2009; 175(2): 668–684. DOI: 10.2353/ajpath.2009.081126Roos F.C., Roberts A.M, Hwang I.I.L, Moriyama E.H, Evans A.J., Sybingco S., Watson I.R., Carneiro L.A., Gedye C., Girardin S.E., Ailles L.E., Jewett M.A., Milosevic M., Wilson B.C., Bell J.C., Der S.D., Ohh M. Oncolytic targeting of renal cell carcinoma via encephalomyocarditis virus. EMBO Mol. Med. 2010; 2(7): 275–288. DOI: 10.1002/emmm.201000081Roos F.C., Roberts A.M, Hwang I.I.L, Moriyama E.H, Evans A.J., Sybingco S., Watson I.R., Carneiro L.A., Gedye C., Girardin S.E., Ailles L.E., Jewett M.A., Milosevic M., Wilson B.C., Bell J.C., Der S.D., Ohh M. Oncolytic targeting of renal cell carcinoma via encephalomyocarditis virus. EMBO Mol. Med. 2010; 2(7): 275–288. DOI: 10.1002/emmm.201000081Christmann B.S., Moran J.M., McGraw J.A., Buller R.M.L., Corbett J.A. Ccr5 Regulates Inflammatory Gene Expression in Response to Encephalomyocarditis Virus Infection. Am. J. Pathol. 2011; 179(6): 2941–2951. DOI: 10.1016/j.ajpath.2011.08.012Christmann B.S., Moran J.M., McGraw J.A., Buller R.M.L., Corbett J.A. Ccr5 Regulates Inflammatory Gene Expression in Response to Encephalomyocarditis Virus Infection. Am. J. Pathol. 2011; 179(6): 2941–2951. DOI: 10.1016/j.ajpath.2011.08.012Luo Y.K., Liang L., Tang Q.H., Zhou L., Shi L.J., Cong Y.Y., Lin W.C., Cui S.J. Isolation and characterization of encephalomyocarditis virus from dogs in China Sci. Rep. 2017; 7(1): 438. DOI: 10.1038/s41598-017-00435-xLuo Y.K., Liang L., Tang Q.H., Zhou L., Shi L.J., Cong Y.Y., Lin W.C., Cui S.J. Isolation and characterization of encephalomyocarditis virus from dogs in China Sci. Rep. 2017; 7(1): 438. DOI: 10.1038/s41598-017-00435-xMaurice H., Nielen M., Brocchi E., Nowotny N., Kassimi L.B., Billinis C. The occurrence of encephalomyocarditis virus (EMCV) in European pigs from 1990 to 2001. Epidemiol. Infect. 2005; 133(3): 547–557. DOI: 10.1017/S0950268804003668Maurice H., Nielen M., Brocchi E., Nowotny N., Kassimi L.B., Billinis C. The occurrence of encephalomyocarditis virus (EMCV) in European pigs from 1990 to 2001. Epidemiol. Infect. 2005; 133(3): 547–557. DOI: 10.1017/S0950268804003668Higuchi H., Hara M., Yamamoto K., Miyamoto T., Kinoshita M., Yamada T., Uchiyama K., Matsumori A. Mast cells play a critical role in the pathogenesis of viral myocarditis. Circulation. 2008; 118(4): 363–372. DOI: 10.1161/CIRCULATIONAHA.107.741595Higuchi H., Hara M., Yamamoto K., Miyamoto T., Kinoshita M., Yamada T., Uchiyama K., Matsumori A. Mast cells play a critical role in the pathogenesis of viral myocarditis. Circulation. 2008; 118(4): 363–372. DOI: 10.1161/CIRCULATIONAHA.107.741595Onodera T., Yoon J.W., Brown K.S., Notkina A.L. Evidence for a single locus controlling susceptibility to virus-induced diabetes mellitus. Nature. 1978; 274: 693–696. DOI: 10.1038/274693a0Onodera T., Yoon J.W., Brown K.S., Notkina A.L. Evidence for a single locus controlling susceptibility to virus-induced diabetes mellitus. Nature. 1978; 274: 693–696. DOI: 10.1038/274693a0Aminev A.G., Amineva S.P., Palmenberg A.C. Encephalomyocarditis viral protein 2A localizes to nucleoli and inhibits cap-dependent mRNA translation. Virus. Res. 2003; 95(1–2): 45–57. DOI: 10.1016/S0168-1702(03)00162-XAminev A.G., Amineva S.P., Palmenberg A.C. Encephalomyocarditis viral protein 2A localizes to nucleoli and inhibits cap-dependent mRNA translation. Virus. Res. 2003; 95(1–2): 45–57. DOI: 10.1016/S0168-1702(03)00162-XMartin L.R., Neal Z.C., McBride M.S., Palmenberg A.C. Mengovirus and encephalomyocarditis virus poly(C) tract lengths can affect virus growth in murine cell culture. J. Virol. 2000; 74(7): 3074–3081. DOI: 10.1128/JVI.74.7.3074-3081.2000Martin L.R., Neal Z.C., McBride M.S., Palmenberg A.C. Mengovirus and encephalomyocarditis virus poly(C) tract lengths can affect virus growth in murine cell culture. J. Virol. 2000; 74(7): 3074–3081. DOI: 10.1128/JVI.74.7.3074-3081.2000Banerjee R., Tsai W., Kim W., Dasgupta A. InteractionBanerjee R., Tsai W., Kim W., Dasgupta A. Interactionof poliovirus-encoded 2C/2BC polypeptides with theof poliovirus-encoded 2C/2BC polypeptides with the′ terminus negative-strand cloverleaf requires an′ terminus negative-strand cloverleaf requires anintact stem-loop b. Virology. 2001; 280 (1):41–51.intact stem-loop b. Virology. 2001; 280 (1):41–51.DOI: 10.1006/viro.2000.0770DOI: 10.1006/viro.2000.0770Helwig F.C., Schmidt C.H. A flter-passing agentHelwig F.C., Schmidt C.H. A flter-passing agentproducing interstitial myocarditis in anthropoid apesproducing interstitial myocarditis in anthropoid apesand small animals. Science. 1945; 102(2637): 31–33.and small animals. Science. 1945; 102(2637): 31–33.DOI: 10.1126/science.102.2637.31DOI: 10.1126/science.102.2637.31Dea S., Bilodeau R., Sauvageau R., Martineau G.P.Dea S., Bilodeau R., Sauvageau R., Martineau G.P.Outbreaks in Quebec pig farms of respiratory andOutbreaks in Quebec pig farms of respiratory andreproductive problems associated with encephalomyocarditis virus. J. Vet. Diagn. Invest. 1991; 3(4):reproductive problems associated with encephalomyocarditis virus. J. Vet. Diagn. Invest. 1991; 3(4):–282. DOI: 10.1177/104063879100300401–282. DOI: 10.1177/104063879100300401

The authors declare that there are no conflicts of interest present.