Enterovirus E infects bovine peripheral blood mononuclear cells. Implications for pathogenesis?

Małaczewska, Joanna; Wróbel, Małgorzata; Kaczorek-Łukowska, Edyta; Rękawek, Wojciech

doi:10.2478/jvetres-2023-0061

Abstract

Introduction

Enterovirus E (EV-E) is a common viral pathogen endemic in cattle worldwide. Little is known, however, about its potential interactions with bovine immune cells.

Material and Methods

The EV-E-permissiveness of bovine peripheral blood mononuclear cells (PBMCs) was evaluated. The infectious titres of extracellular virus were measured and the intracellular viral RNA levels were determined by reverse transcription quantitative PCR after cell inoculation. The effects of EV-E on cell viability and proliferative response were investigated with a methyl thiazolyl tetrazolium bromide reduction assay, the percentages of main lymphocyte subsets and oxidative burst activity of blood phagocytes were determined with flow cytometry, and pro-inflammatory cytokine secretion was measured with an ELISA.

Results

Enterovirus E productively infected bovine PBMCs. The highest infectious dose of EV-E decreased cell viability and T-cell proliferation. All of the tested doses of virus inhibited the proliferation of high responding to lipopolysaccharide B cells and stimulated the secretion of interleukin 1β, interleukin 6 and tumour necrosis factor α pro-inflammatory cytokines.

Conclusion

Interactions of EV-E with bovine immune cells may indicate potential evasion mechanisms of the virus. There is also a risk that an infection with this virus can predispose the organism to secondary infections, especially bacterial ones.

References

Amadori M., Soares-Filipe J.F., Riva F., Vitali A., Ruggeri J., Lacetera N.: Characterization of the blastogenic response to LPS of bovine peripheral blood mononuclear cells. PLoS One 2018, 13, e0204827, doi: 10.1371/journal.pone.0204827.
Open DOI Search in Google Scholar Back to article
Birdane F.M., Gür S.: Precolostral evaluation of Bovine Enterovirus Type 1 (BEV1) infection in a dairy herd. Vet Arh 2019, 89, 1-10, doi: 10.24099/vet.arhiv.0163.
Open DOI Search in Google Scholar Back to article
Blas-Machado U., Saliki J.T., Sánchez S., Brown C.C., Zhang J., Keys D., Woolums A., Harvey S.B.: Pathogenesis of a bovine enterovirus-1 isolate in experimentally infected calves. Vet Pathol 2011, 48, 1075-1084, doi: 10.1177/0300985810395728.
Open DOI Search in Google Scholar Back to article
Brundage L.J., Derbyshire J.B., Wilkie B.N.: Cell mediated responses in a porcine enterovirus infection in piglets. Can J Comp Med 1980, 44, 61-69.
Search in Google Scholar Back to article
Catalani E., Amadori M., Vitali A., Lacetera N.: Short communication: Lymphoproliferative response to lipopolysaccharide and incidence of infections in periparturient dairy cows. J Dairy Sci 2013, 96, 7077-7081, doi: 10.3168/jds.2013-6854.
Open DOI Search in Google Scholar Back to article
Chang L.-Y., Hsiung C.A., Lu C.-Y., Lin T.-Y., Huang F.-Y., Lai Y.-H., Chiang Y.-P., Chiang B.-L., Lee C.-Y., Huang L.-M.: Status of cellular rather than humoral immunity is correlated with clinical outcome of enterovirus 71. Pediatr Res 2006, 60, 466-471, doi: 10.1203/01.pdr.0000238247.86041.19.
Open DOI Search in Google Scholar Back to article
Chen L.-C., Shyu H.-W., Chen S.-H., Lei H.-Y., Yu C.-K., Yeh T.-M.: Enterovirus 71 infection induces Fas ligand expression and apoptosis of Jurkat cells. J Med Virol 2006, 78, 780-786, doi: 10.1002/jmv.20623.
Open DOI Search in Google Scholar Back to article
Chen L.-C., Yeh T.-M.: Enterovirus 71 infection of human immune cells induces the production of proinflammatory cytokines. J Biomed Lab Sci 2009, 21, 82-90.
Search in Google Scholar Back to article
Gong X., Zhou J., Zhu W., Liu N., Li J., Li L., Jin Y., Duan Z.: Excessive proinflammatory cytokine and chemokine responses of human monocyte-derived macrophages to enterovirus 71 infection. BMC Infect Dis 2012, 12, 224, doi: 10.1186/1471-2334-12-224.
Open DOI Search in Google Scholar Back to article
Grammatikos A., Donati M., Johnston S.L., Gompels M.M.: Peripheral B cell deficiency and predisposition to viral infections: the paradigm of immune deficiencies. Front Immunol 2021, 12, 731643, doi: 10.3389/fimmu.2021.731643.
Open DOI Search in Google Scholar Back to article
Gras C.K., Demolier M., Eisen A.K.A., Spilki F.R., Hezel A.: Seroprevalence of bovine adenovirus and enterovirus antibodies reveals different infection dynamics in cattle herds. Acta Sci Vet 2017, 45, 6, doi: 10.22456/1679-9216.80212.
Open DOI Search in Google Scholar Back to article
Henke A., Mohr C., Sprenger H., Graebner C., Stelzner A., Nain M., Gemsa D.: Coxsackievirus B3-induced production of tumor necrosis factor-alpha, IL-1 beta, and IL-6 in human monocytes. J Immunol 1992, 148, 2270-2277, doi: 10.4049/jimmunol.148.7.2270.
Open DOI Search in Google Scholar Back to article
Henke A., Spengler H.P., Stelzner A., Nain M., Gemsa D.: Lipopolysaccharide suppresses cytokine release from coxsackie virus-infected human monocytes. Res Immunol 1992, 143, 65-70, doi: 10.1016/0923-2494(92)80081-u.
Open DOI Search in Google Scholar Back to article
Kalter S.S.: Animal “orphan” enteroviruses. Bull World Health Organ 1960, 22, 319-337.
Search in Google Scholar Back to article
Kandolf R., Sauter M., Aepinus C., Schnorr J.J., Selinka H.C., Klingel K.: Mechanisms and consequences of enterovirus persistence in cardiac myocytes and cells of the immune system. Virus Res 1999, 62, 149-158, doi: 10.1016/s0168-1702(99)00041-6.
Open DOI Search in Google Scholar Back to article
King A.M.Q., Lefkowitz E.J., Mushegian A.R., Adams M.J., Dutilh B.E., Gorbalenya A.E., Harrach B., Harrison R.L., Junglen S., Knowles N.J., Kropinski A.M., Krupovic M., Kuhn J.H., Nibert M.L., Rubino L., Sabanadzovic S., Sanfaçon H., Siddell S.G., Simmonds P., Varsani A., Zerbini F.M., Davison A.J.: Changes to taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2018). Arch Virol 2018, 163, 2601-2631, doi: 10.1007/s00705-018-3847-1.
Open DOI Search in Google Scholar Back to article
Klingel K., Stephan S., Sauter M., Zell R., McManus B.M., Bültmann B., Kandolf R.: Pathogenesis of murine enterovirus myocarditis: virus dissemination and immune cell targets. J Virol 1996, 70, 8888-8895, doi: 10.1128/JVI.70.12.8888-8895.1996.
Open DOI Search in Google Scholar Back to article
Kramer M., Schulte B.M., Toonen L.W., de Bruijni M.A., Galama J.M., Adema G.J., van Kuppeveld F.J.: Echovirus infection causes rapid loss-of-function and cell death in human dendritic cells. Cell Microbiol 2007, 9, 1507-1518, doi: 10.1111/j.1462-5822.2007.00888.x.
Open DOI Search in Google Scholar Back to article
Lin T.Y., Chang L.Y., Huang Y.C., Hsu K.H., Chiu C.H., Yang K.D.: Different proinflammatory reactions in fatal and non-fatal enterovirus 71 infections: implications for early recognition and therapy. Acta Paediatr 2002, 91, 632-635, doi: 10.1080/080352502760069016.
Open DOI Search in Google Scholar Back to article
Lin Y.W., Chang K.C., Kao C.M., Chang S.P., Tung Y.Y., Chen S.H.: Lymphocyte and antibody responses reduce enterovirus 71 lethality in mice by decreasing tissue viral loads. J Virol 2009, 83, 6477-6483, doi: 10.1128/JVI.00434-09.
Open DOI Search in Google Scholar Back to article
Liu D., Hu J., Dong H., Huang L., Wei Y., Xia D., Zhu H., Wang X., Wu H., Wang X., Liu C.: Identification of three linear B cell epitopes using monoclonal antibodies against bovine enterovirus VP2 protein. Appl Microbiol Biotechnol 2019, 103, 7467-7480, doi: 10.1007/s00253-019-09971-0.
Open DOI Search in Google Scholar Back to article
Małaczewska J.: The in vitro effect of commercially available noble metal nanocolloids on the splenocyte proliferative response and cytokine production in mice. Pol J Vet Sci 2014, 17, 37-45, doi: 10.2478/pjvs-2014-0005.
Open DOI Search in Google Scholar Back to article
Małaczewska J.: Effect of oral administration of commercial gold nanocolloid on peripheral blood leukocytes in mice. Pol J Vet Sci 2015, 18, 273-282, doi: 10.1515/pjvs-2015-0036.
Open DOI Search in Google Scholar Back to article
Małaczewska J., Wójcik R., Kaczorek E., Rękawek W., Siwicki A.K.: Commercial gold nanocolloid inhibits synthesis of IL-2 and proliferation of porcine T lymphocytes. Res Vet Sci 2017, 4-11, doi: 10.1016/j.rvsc.2016.10.013.
Open DOI Search in Google Scholar Back to article
McGill J.L., Sacco R.E.: The immunology of bovine respiratory disease: recent advancements. Vet Clin North Am Food Anim Pract 2020, 36, 333-348, doi: 10.1016/j.cvfa.2020.03.002.
Open DOI Search in Google Scholar Back to article
Mena I., Perry C.M., Harkins S., Rodriguez F., Gebhard J., Whitton J.L.: The role of B lymphocytes in coxsackievirus B3 infection. Am J Pathol 1999, 155, 1205-1215, doi: 10.1016/S0002-9440(10)65223-6.
Open DOI Search in Google Scholar Back to article
Nascimbeni M., Shin E.C., Chiriboga L., Kleiner D.E., Rehermann B.: Peripheral CD4(+)CD8(+) T cells are differentiated effector memory cells with antiviral functions. Blood 2004, 104, 478-486, doi: 10.1182/blood-2003-12-4395.
Open DOI Search in Google Scholar Back to article
Onah D.N., Hopkins J., Luckins A.G.: Induction of CD4+CD8+ double positive T cells and increase in CD5+ B cells in efferent lymph in sheep infected with Trypanosoma evansi. Parasite Immunol 1998, 20, 121-134, doi: 10.1111/j.1365-3024.1998.00125.x.
Open DOI Search in Google Scholar Back to article
Perino L.J.: Immunosuppressive effects of bovine viral pathogens: A review. Bov Pract 1989, 24, 42-48, doi: 10.21423/bovine-vol0no24p42-48.
Open DOI Search in Google Scholar Back to article
Plekhova N.G., Somova L.M., Koroleva G.A., Zlobin V.I., Dolzhikov S.V., Frolova T.V., Karan L.S.: The entry of the Picornaviridae virus family in resident macrophages. Cell Tiss Biol 2008, 2, 311-321, doi: 10.1134/S1990519X08030127.
Open DOI Search in Google Scholar Back to article
Reed L.J., Muench H.: A simple method of estimating fifty percent endpoints. Am J Hyg 1938, 27, 493-497.
Search in Google Scholar Back to article
Shingu M., Chinami M., Taguchi T., Shingu M. Jr.: Therapeutic effects of bovine enterovirus infection on rabbits with experimentally induced adult T cell leukaemia. J Gen Virol 1991, 72, 2031-2034, doi: 10.1099/0022-1317-72-8-2031.
Open DOI Search in Google Scholar Back to article
Sinclair W., Omar M.: Enterovirus (Updated 2022 Aug 1), In: StatPearls (Internet). StatPearls Publishing, Treasure Island, FL, 2022.https://www.ncbi.nlm.nih.gov/books/NBK562330/.
Search in Google Scholar Back to article
Smura T., Ylipaasto P., Klemola P., Kaijalainen S., Kyllönen L., Sordi V., Piemonti L., Roivainen M.: Cellular tropism of human enterovirus D species serotypes EV-94, EV-70, and EV-68 in vitro: implications for pathogenesis. J Med Virol 2010, 82, 1940-1949, doi: 10.1002/jmv.21894.
Open DOI Search in Google Scholar Back to article
Smyth M., Symonds A., Brazinova S., Martin J.: Bovine enterovirus as an oncolytic virus: foetal calf serum facilitates its infection of human cells. Int J Mol Med 2002, 10, 49-53, doi: 10.3892/ijmm.10.1.49.
Open DOI Search in Google Scholar Back to article
Sobhy N.M., Mor S.K., Mohammed M.E., Bastawecy I.M., Fakhry H.M., Youssef C.R., Abouzeid N.Z., Goyal S.M.: Isolation and molecular characterization of bovine enteroviruses in Egypt. Vet J 2015, 206, 317-321, doi: 10.1016/j.tvjl.2015.10.011.
Open DOI Search in Google Scholar Back to article
Vreugdenhil G.R., Wijnands P.G., Netea M.G., van der Meer J.W., Melchers W.J., Galama J.M.: Enterovirus-induced production of pro-inflammatory and T-helper cytokines by human leukocytes. Cytokine 2000, 12, 1793-1796, doi: 10.1006/cyto.2000.0786.
Open DOI Search in Google Scholar Back to article
Vu D.L., Kaiser L.: The concept of commensal viruses almost 20 years later: redefining borders in clinical virology. Clin Microbiol Infect 2017, 23, 688-690, doi: 10.1016/j.cmi.2017.03.005.
Open DOI Search in Google Scholar Back to article
Wongsa A., Noulsri E., Phawong C., Puthavathana P., Tassaneetrithep B.: Replication and cytokine profiles of different subgenotypes of enterovirus 71 isolated from Thai patients in peripheral blood mononuclear cells. Microb Pathog 2019, 132, 215-221, doi: 10.1016/j.micpath.2019.05.008.
Open DOI Search in Google Scholar Back to article
Wróbel M., Małaczewska J., Kaczorek-Łukowska E.: Antiviral effect of bovine lactoferrin against enterovirus E. Molecules 2022, 27, 5569, doi: 10.3390/molecules27175569.
Open DOI Search in Google Scholar Back to article
Yang Y., Ma J., Xiu J., Bai L., Guan F., Zhang L., Liu J., Zhang L.: Deferoxamine compensates for decreases in B cell counts and reduces mortality in enterovirus 71-infected mice. Mar Drugs 2014, 12, 4086-4095, doi: 10.3390/md12074086.
Open DOI Search in Google Scholar Back to article
Zhang H., Liu H., Bao J., Guo Y., Peng T., Zhou P., Zhang W., Ma B., Wang J., Gao M.: Characterization of an enterovirus species E isolated from naturally infected bovine in China. Virus Res 2014, 191, 101-107, doi: 10.1016/j.virusres.2014.07.032.
Open DOI Search in Google Scholar Back to article
Zhu L., Xing Z., Gai X., Li S., San Z., Wang X.: Identification of a novel enterovirus E isolates HY12 from cattle with severe respiratory and enteric diseases. PLoS One 2014, 9, e97730, doi: 10.1371/journal.pone.0097730.
Open DOI Search in Google Scholar Back to article