Distinctive features of bovine alphaherpesvirus types 1 and 5 and the virus-host interactions that might influence clinical outcomes

Abstract

Bovine herpesvirus types 1 (BoHV-1) and 5 (BoHV-5) are two closely related alphaherpesviruses. BoHV-1 causes several syndromes in cattle, including respiratory disease and sporadic cases of encephalitis, whereas BoHV-5 is responsible for meningoencephalitis in calves. Although both viruses are neurotropic, they differ in their neuropathogenic potential. This review summarizes the findings on the specific mechanisms and pathways known to modulate the pathogenesis of BoHV-1 and BoHV-5, particularly in relation to respiratory and neurological syndromes, which characterize BoHV-1 and BoHV-5 infections, respectively.

This is a preview of subscription content, log in to check access.

Fig. 1

References

  1. 1.

    Roizman B, Desrosiers R, Fleckenstein B, Lopez C, Minston A, Studdert M (1992) The family Herpesviridae: an update. Arch Virol 123:425–449

    Google Scholar 

  2. 2.

    Barenfus M, Delliquadri C, Mcintyre R, Schroeder R (1963) Isolation of infectious bovine rhinotracheitis virus from calves with meningoencephalitis. J Am Vet Med Assoc 143:725–728

    CAS  PubMed  Google Scholar 

  3. 3.

    d’Offay JM, Mock RE, Fulton RW (1993) Isolation and characterization of encephalitic bovine herpesvirus type 1 isolates from cattle in North America. Am J Vet Res 54(4):534–539

    PubMed  Google Scholar 

  4. 4.

    Meyer G, Lemaire M, Ros C, Belak K, Gabriel A, Cassart D, Coignoul F, Belak S, Thiry E (2001) Comparative pathogenesis of acute and latent infections of calves with bovine herpesvirus types 1 and 5. Arch Virol 146:633–652

    CAS  PubMed  Google Scholar 

  5. 5.

    Silva MS, Brum MC, Loreto EL, Weiblen R, Flores EF (2007) Molecular and antigenic characterization of Brazilian bovine herpesvirus type 1 isolates recovered from the brain of cattle with neurological disease. Virus Res 129(2):191–199

    CAS  PubMed  Google Scholar 

  6. 6.

    Tikoo SK, Campos M, Babiuk LA (1995) Bovine herpesvirus 1 (BHV-1): biology, pathogenesis, and control. Adv Virus Res 45:191–223

    CAS  PubMed  Google Scholar 

  7. 7.

    Pérez S, Bretschneider G, Leunda M, Osorio F, Flores E, Odeón A (2002) Primary infection, latency and reactivation of Bovine Herpesvirus Type 5 (BVH-5) in the bovine nervous system. Vet Pathol 39:437–444

    PubMed  Google Scholar 

  8. 8.

    Del Médico Zajac MP, Ladelfa MF, Kotsias F, Muylkens B, Thiry J, Thiry E, Romera SA (2010) Biology of bovine herpesvirus 5. Vet J. 184(2):138–145

    PubMed  Google Scholar 

  9. 9.

    Schudel A, Carrillo B, Wyler R, Metzler A (1986) Infections of calves with antigenic variants of bovine herpesvirus 1 (BHV-1) and neurological disease. J Vet Med B 33:303–310

    CAS  Google Scholar 

  10. 10.

    Esteves PA, Spilki FR, Franco AC, Silva TC, Oliveira EA, Moojen V, Esmeraldino AM, Roehe PM (2003) Bovine herpesvirus type 5 in the semen of a bull not exhibiting clinical signs. Vet Rec 152:658–659

    CAS  PubMed  Google Scholar 

  11. 11.

    Kirkland PD, Poynting AI, Gu X, Davis RJ (2009) Infertility and venereal disease in cattle inseminated with semen containing bovine herpesvirus type 5. Vet Rec 165:111–113

    CAS  PubMed  Google Scholar 

  12. 12.

    Cascio E, Belknap P, Schultheiss A, Ames J, Collins J (1999) Encephalitis induced by bovine herpesvirus 5 and protection by prior vaccination or infection with bovine herpesvirus 1. J Vet Diagn Investig 11:134–149

    CAS  Google Scholar 

  13. 13.

    Isernhagen AJ, Cosenza M, da Costa MC, Médici KC, Balarin MR, Bracarense AP, Alfieri AA, Lisbôa JA (2011) Asymptomatic encephalitis in calves experimentally infected with bovine herpesvirus-5. Can Vet J 52(12):1312–1318

    PubMed  PubMed Central  Google Scholar 

  14. 14.

    Puentes R, Campos FS, Furtado A, Torres FD, Franco AC, Maisonnave J, Roehe PM (2016) Comparison between DNA detection in trigeminal nerve ganglia and serology to detect cattle infected with bovine herpesviruses types 1 and 5. PLoS One 11(5):e0155941. https://doi.org/10.1371/journal.pone.0155941

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Miller JM, Whetstone CA, Van der Maaten MM (1991) Abortifacient property of bovine herpesvirus type 1 isolates that represent three subtypes determined by restriction endonuclease analysis of viral DNA. Am J Vet Res 52:458–461

    CAS  PubMed  Google Scholar 

  16. 16.

    D’Arce RC, Almeida RS, Silva TC, Franco AC, Spilki F, Roehe PM, Arns CW (2002) Restriction endonuclease and monoclonal antibody analysis of Brazilian isolates of bovine herpesviruses types 1 and 5. Vet Microbiol 88(4):315–324

    PubMed  Google Scholar 

  17. 17.

    Maidana SS, Craig PO, Craig MI, Ludwig L, Mauroy A, Thiry E, Romera SA (2017) Evidence of natural interspecific recombinant viruses between bovine alphaherpesviruses 1 and 5. Virus Res 242:122–130

    CAS  PubMed  Google Scholar 

  18. 18.

    Varela AP, Holz CL, Cibulski SP, Teixeira TF, Antunes DA, Franco AC, Roehe LR, Oliveira MT, Campos FS, Dezen D, Cenci A, Brito WD, Roehe PM (2010) Neutralizing antibodies to bovine herpesvirus types 1 (BoHV-1) and 5 (BoHV-5) and its subtypes. Vet Microbiol 142(3–4):254–260

    CAS  PubMed  Google Scholar 

  19. 19.

    Thiry J, Keuser V, Muylkens B, Meurens F, Gogev S, Vanderplasschen A, Thiry E (2006) Ruminant alphaherpesviruses related to bovine herpesvirus 1. Vet Res 37(2):169–190

    CAS  PubMed  Google Scholar 

  20. 20.

    Mayfield JE, Good PJ, VanOort HJ, Campbell AR, Reed DE (1983) Cloning and cleavage site mapping of DNA from bovine herpesvirus 1 (Cooper strain). J Virol 47(1):259–264

    CAS  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Delhon G, Moraes MP, Lu Z, Afonso CL, Flores EF, Weiblen R, Kutish GF, Rock DL (2003) Genome of bovine herpesvirus 5. J Virol 77(19):10339–10347

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Schwyzer M, Ackermann M (1996) Molecular virology of ruminant herpesviruses. Vet Microbiol 53(1–2):17–29

    CAS  PubMed  Google Scholar 

  23. 23.

    Jefferson VA, Barber KA, El-Mayet FS, Jones C, Nanduri B, Meyer F (2018) Proteogenomic identification of a novel protein-encoding gene in bovine herpesvirus 1 that is expressed during productive infection. Viruses 10(9):499. https://doi.org/10.3390/v10090499

    CAS  Article  PubMed Central  Google Scholar 

  24. 24.

    Schwyzer M, Vlcek C, Menekse O, Fraefel C, Paces V (1993) Promoter, spliced leader, and coding sequence for BICP4, the largest of the immediate-early proteins of bovine herpesvirus 1. Virology 197(1):349–357

    CAS  PubMed  Google Scholar 

  25. 25.

    Wirth UV, Fraefel C, Vogt B, Vlcek C, Paces V, Schwyzer M (1992) Immediate-early RNA 2.9 and early RNA 2.6 of bovine herpesvirus 1 are 3′ coterminal and encode a putative zinc finger transactivator protein. J Virol 66(5):2763–2772

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Wirth UV, Vogt B, Schwyzer M (1991) The three major immediate-early transcripts of bovine herpesvirus 1 arise from two divergent and spliced transcription units. J Virol 65(1):195–205

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Gillette K, Misra V, Bratanich A (2002) Sequence analysis of the alpha trans-inducing factor of bovine herpesvirus type 5 (BHV-5). Virus Genes 24(2):149–152

    CAS  PubMed  Google Scholar 

  28. 28.

    Meyer F, Jones C (2009) The cellular transcription factor, CCAAT enhancer-binding protein alpha (C/EBP-alpha), has the potential to activate the bovine herpesvirus 1 immediate-early transcription unit 1 promoter. J Neurovirol 15(2):123–130

    CAS  PubMed  Google Scholar 

  29. 29.

    Sawant L, Kook I, Vogel JL, Kristie TM, Jones C (2018) The cellular coactivator HCF-1 is required for glucocorticoid receptor-mediated transcription of bovine herpesvirus 1 immediate early genes. J Virol 92(17):e00987. https://doi.org/10.1128/jvi.00987-18

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Schwyzer M, Wirth UV, Vogt B, Fraefel C (1994) BICP22 of bovine herpesvirus 1 is encoded by a spliced 1.7 kb RNA which exhibits immediate early and late transcription kinetics. J Gen Virol 75:1703–1711

    CAS  PubMed  Google Scholar 

  31. 31.

    Pokhriyal M, Verma OP, Ratta B, Kumar A, Saxena M, Sharma B (2016) Bovine herpes virus 1 major immediate early transcription unit 1 (IETU-1) uses alternative promoters to transcribe BICP0 and BICP4 transcripts. Curr Microbiol 72(4):420–425

    CAS  PubMed  Google Scholar 

  32. 32.

    Rock D, Lokensgard J, Lewis T, Kutish G (1992) Characterization of dexamethasone-induced reactivation of latent bovine herpesvirus 1. J Virol 66:2484–2490

    CAS  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Favier PA, Marin MS, Morán PE, Odeón AC, Verna AE, Pérez SE (2014) Latency of bovine herpesvirus type 5 (BoHV-5) in tonsils and peripheral blood leukocytes. Vet J 202(1):134–140

    CAS  PubMed  Google Scholar 

  34. 34.

    Belknap E, Collins J, Ayers V, Schultheiss P (1994) Experimental infection of neonatal calves with neurovirulent bovine herpesvirus type 1.3. Vet Pathol 31:358–365

    CAS  PubMed  Google Scholar 

  35. 35.

    Leite F, Kuckleburg C, Atapattu D, Schultz RD, Czuprynski CJ (2004) BHV-1 infection and inflammatory cytokines amplify the interaction of Mannheimia haemolytica leukotoxin with bovine leukocytes in vitro. Vet Immunol Immunopathol 99:193–202

    CAS  PubMed  Google Scholar 

  36. 36.

    Leite F, Atapattu D, Kuckleburg C, Schultz R, Czuprynski CJ (2004) Incubation of bovine PMNs with conditioned medium from BHV-1 infected peripheral blood mononuclear cells increases their susceptibility to Mannheimia haemolytica leukotoxin. Vet Immunol Immunopathol 103:187–193

    Google Scholar 

  37. 37.

    Marin MS, Quintana S, Leunda MR, Odeón AC, Pérez SE (2016) Distribution of bovine alpha-herpesviruses and expression of toll-like receptors in the respiratory system of experimentally infected calves. Res Vet Sci 105:53–55

    CAS  PubMed  Google Scholar 

  38. 38.

    Vogel FS, Caron L, Flores EF, Weiblen R, Winkelmann ER, Mayer SV, Bastos RG (2003) Distribution of bovine herpesvirus type 5 DNA in the central nervous systems of latently, experimentally infected calves. J Clin Microbiol 41(10):4512–4520

    CAS  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Ashbaugh SE, Thompson KE, Belknap EB, Schultheiss PC, Chowdhury S, Collins JK (1997) Specific detection of shedding and latency of bovine herpesvirus 1 and 5 using a nested polymerase chain reaction. J Vet Diagn Investig 9(4):387–394

    CAS  Google Scholar 

  40. 40.

    Megid J, Ferreira Vicente A, Appolinario CM, Allendorf SD, de Souza Ribeiro Mioni M, Gasparini Baraldi T, Cortez A, Bryan Heinemann M, Reinaldo Silva Fonseca C, Cristina Pelícia V, Devidé Ribeiro BL, Hiromi Okuda L, Pituco EM (2015) Outbreak control and clinical, pathological, and epidemiological aspects and molecular characterization of a bovine herpesvirus type 5 on a feedlot farm in São Paulo State. Biomed Res Int. https://doi.org/10.1155/2015/981230

    Article  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Gershwin LJ, Van Eenennaam AL, Anderson ML, McEligot HA, Shao MX, Toaff-Rosenstein R, Taylor JF, Neibergs HL, Womack J (2015) Bovine respiratory disease complex coordinated agricultural project research team single pathogen challenge with agents of the bovine respiratory disease complex. PLoS One 10(11):e0142479. https://doi.org/10.1371/journal.pone.0142479

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Szeredi L, Jánosi S, Pálfi V (2010) Microbiological and pathological examination of fatal calf pneumonia cases induced by bacterial and viral respiratory pathogens. Acta Vet Hung 58(3):341–356

    PubMed  Google Scholar 

  43. 43.

    Furuoka H, Izumida N, Horiuchi M, Osame S, Matsui T (1995) Bovine herpesvirus meningoencephalitis association with infectious bovine rhinotracheitis (IBR) vaccine. Acta Neuropathol 90(6):565–571

    CAS  PubMed  Google Scholar 

  44. 44.

    Lee BJ, Weiss ML, Mosier D, Chowdhury SI (1999) Spread of bovine herpesvirus type 5 (BHV-5) in the rabbit brain after intranasal inoculation. J Neurovirol 5(5):474–484

    CAS  PubMed  Google Scholar 

  45. 45.

    Beltrao N, Flores E, Weiblen R, Silva A, Roehe P, Irigoyen L (2000) Infecção e enfermidade neurológica pelo herpesvírus bovino tipo 5 (BHV-5): coelhos como modelo experimental-5): coelhos como modelo experimental. Pesq Vet Bras 20(4):144–150

    Google Scholar 

  46. 46.

    Marin MS, Leunda MR, Verna AE, Morán PE, Odeón AC, Pérez SE (2016) Distribution of bovine herpesvirus type 1 in the nervous system of experimentally infected calves. Vet J 209:82–86

    CAS  PubMed  Google Scholar 

  47. 47.

    Elias F, Schild AL, Riet-Correa F (2004) Meningoencefalite e encefalomalacia por Herpesvírus bovino-5: distribuição das lesões no sistema nervoso central de bovinos naturalmente infectados. Pesq Vet Bras 24(3):123–131

    Google Scholar 

  48. 48.

    Cardoso TC, Ferreira HL, Okamura LH, Giroto TP, Oliveira BR, Fabri CU, Gameiro R, Flores EF (2016) Cellular response markers and cytokine gene expression in the central nervous system of cattle naturally infected with bovine herpesvirus 5. Vet J 218:71–77

    CAS  PubMed  Google Scholar 

  49. 49.

    Roels S, Charlier G, Letellier C, Meyer G, Schynts F, Kerkhofs P, Thiry E, Vanopdenbosch E (2000) Natural case of bovine herpesvirus 1 meningoencephalitis in an adult cow. Vet Rec 146(20):586–588

    CAS  PubMed  Google Scholar 

  50. 50.

    Wang P, Hurley DJ, Braun LJ, Chase CC (2001) Detection of bovine herpesvirus-1 in peripheral blood mononuclear cells eight months postinfection. J Vet Diagn Investig 13:424–427

    CAS  Google Scholar 

  51. 51.

    Abril C, Engels M, Liman A, Hilbe M, Albini S, Franchini M, Suter M, Ackermann M (2004) Both viral and host factors contribute to neurovirulence of bovine herpesviruses 1 and 5 in interferon receptor-deficient mice. J Virol 78(7):3644–3653

    CAS  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Levings RL, Roth JA (2013) Immunity to bovine herpesvirus 1: I. Viral lifecycle and innate immunity. Anim Health Res Rev 14(1):88–102

    PubMed  Google Scholar 

  53. 53.

    Jones C (2003) Herpes simplex virus type 1 and bovine herpesvirus 1 latency. Clin Microbiol Rev 16(1):79–95

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Inman M, Lovato L, Doster A, Jones C (2002) A mutation in the latency-related gene of bovine herpesvirus 1 disrupts the latency reactivation cycle in calves. J Virol 76(13):6771–6779

    CAS  PubMed  PubMed Central  Google Scholar 

  55. 55.

    Kutish G, Mainprize T, Rock D (1990) Characterization of the latency-related transcriptionally active region of the bovine herpesvirus 1 genome. J Virol 64(12):5730–5737

    CAS  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Feldman LT, Ellison AR, Voytek CC, Yang L, Krause P, Margolis TP (2002) Spontaneous molecular reactivation of herpes simplex virus type 1 latency in mice. Proc Natl Acad Sci USA 99(2):978–983

    CAS  PubMed  Google Scholar 

  57. 57.

    Mweene AS, Okazaki K, Kida H (1996) Detection of viral genome in non-neural tissues of cattle experimentally infected with bovine herpesvirus 1. Jpn J Vet Res 44:165–174

    CAS  PubMed  Google Scholar 

  58. 58.

    Winkler M, Schang L, Doster A, Holt T, Jones C (2000) Analysis of cyclins in trigeminal ganglia of calves infected with bovine herpesvirus-1. J Gen Virol 81:2993–2998

    CAS  PubMed  Google Scholar 

  59. 59.

    Pérez S, Inman M, Doster A, Jones C (2005) Latency-related gene encoded by bovine herpesvirus 1 promotes virus growth and reactivation from latency in tonsils of infected calves. J Clin Microbiol 43(1):393–401

    PubMed  PubMed Central  Google Scholar 

  60. 60.

    Vogel FS, Flores EF, Weiblen R, Winkelmann ER, Moraes MP, Bragança JF (2004) Intrapreputial infection of young bulls with bovine herpesvirus type 1.2 (BHV-1.2): acute balanoposthitis, latent infection and detection of viral DNA in regional neural and non-neural tissues 50 days after experimental reactivation. Vet Microbiol 98:185–196

    CAS  PubMed  Google Scholar 

  61. 61.

    Jones C (1998) Alphaherpesvirus latency: its role in disease and survival of the virus in nature. Adv Virus Res 51:81–133

    CAS  PubMed  Google Scholar 

  62. 62.

    Hossain A, Schang LM, Jones C (1995) Identification of gene products encoded by the latency-related gene of bovine herpesvirus 1. J Virol 69(9):5345–5352

    CAS  PubMed  PubMed Central  Google Scholar 

  63. 63.

    Devireddy LR, Jones CJ (1999) Activation of caspases and p53 by bovine herpesvirus 1 infection results in programmed cell death and efficient virus release. J Virol 73(5):3778–3788

    CAS  PubMed  PubMed Central  Google Scholar 

  64. 64.

    Silvestro C, Bratanich A (2016) The latency related gene of bovine herpesvirus types 1 and 5 and its modulation of cellular processes. Arch Virol 161(12):3299–3308

    CAS  PubMed  Google Scholar 

  65. 65.

    Jones C, da Silva LF, Sinani D (2011) Regulation of the latency-reactivation cycle by products encoded by the bovine herpesvirus 1 (BHV-1) latency-related gene. J Neurovirol 17(6):535–545

    CAS  PubMed  Google Scholar 

  66. 66.

    Pérez S, Meyer F, Saira K, Doster A, Jones C (2008) Premature expression of the latency-related RNA encoded by bovine herpesvirus type 1 correlates with higher levels of beta interferon RNA expression in productively infected cells. J Gen Virol 89(Pt 6):1338–1345

    PubMed  Google Scholar 

  67. 67.

    Pérez S, Meyer F, Henderson G, Jiang Y, Sherman S, Doster A, Inman M, Jones C (2007) A protein encoded by the bovine herpesvirus 1 open reading frame E gene induces neurite-like morphological changes in mouse neuroblastoma cells and is expressed in trigeminal ganglionic neurons. J Neurovirol 13(2):139–149

    PubMed  Google Scholar 

  68. 68.

    Whetstone CA, Miller JM, Seal BS, Bello LJ, Lawrence WC (1992) Latency and reactivation of a thymidine kinase-negative bovine herpesvirus 1 deletion mutant. Arch Virol 122(1–2):207–214

    CAS  PubMed  Google Scholar 

  69. 69.

    Caron L, Flores EF, Weiblen R, Scherer CF, Irigoyen LF, Roehe PM, Odeon A, Sur JH (2002) Latent infection by bovine herpesvirus type-5 in experimentally infected rabbits: virus reactivation, shedding and recrudescence of neurological disease. Vet Microbiol 84(4):285–295

    CAS  PubMed  Google Scholar 

  70. 70.

    Mayer SV, Quadros VL, Vogel FS, Winkelmann ER, Arenhart S, Weiblen R, Flores EF (2006) Dexamethasone-induced reactivation of bovine herpesvirus type 5 latent infection in experimentally infected rabbits results in a broader distribution of latent viral DNA in the brain. Braz J Med Biol Res 39:335–343

    CAS  PubMed  Google Scholar 

  71. 71.

    El-Mayet FS, Sawant L, Thunuguntla P, Jones C (2017) Combinatorial effects of the glucocorticoid receptor and Krüppel-like transcription factor 15 on bovine herpesvirus 1 transcription and productive infection. J Virol 91(21):e00904. https://doi.org/10.1128/jvi.00904-17

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  72. 72.

    Kook I, Doster A, Jones C (2015) Bovine herpesvirus 1 regulatory proteins are detected in trigeminal ganglionic neurons during the early stages of stress-induced escape from latency. J Neurovirol 21(5):585–591

    CAS  PubMed  Google Scholar 

  73. 73.

    Zhu L, Thompson J, Ma F, Eudy J, Jones C (2017) Effects of the synthetic corticosteroid dexamethasone on bovine herpesvirus 1 productive infection. Virology 505:71–79

    CAS  PubMed  Google Scholar 

  74. 74.

    Guo J, Li Q, Jones C (2019) The bovine herpesvirus 1 regulatory proteins, bICP4 and bICP22, are expressed during the escape from latency. J Neurovirol 25(1):42–49

    CAS  PubMed  Google Scholar 

  75. 75.

    Workman A, Eudy J, Smith L, da Silva LF, Sinani D, Bricker H, Cook E, Doster A, Jones C (2012) Cellular transcription factors induced in trigeminal ganglia during dexamethasone-induced reactivation from latency stimulate bovine herpesvirus 1 productive infection and certain viral promoters. J Virol 86(5):2459–2473

    CAS  PubMed  PubMed Central  Google Scholar 

  76. 76.

    Workman A, Perez S, Doster A, Jones C (2009) Dexamethasone treatment of calves latently infected with bovine herpesvirus 1 leads to activation of the bICP0 early promoter, in part by the cellular transcription factor C/EBP-alpha. J Virol 83(17):8800–8809

    CAS  PubMed  PubMed Central  Google Scholar 

  77. 77.

    Workman A, Sinani D, Pittayakhajonwut D, Jones C (2011) A protein (ORF2) encoded by the latency-related gene of bovine herpesvirus 1 interacts with Notch1 and Notch3. J Virol 85(6):2536–2546

    CAS  PubMed  Google Scholar 

  78. 78.

    Silva LF, Jones C (2012) Two microRNAs encoded within the bovine herpesvirus 1 latency-related gene promote cell survival by interacting with RIG-I and stimulating NF-κB-dependent transcription and beta interferon signaling pathways. J Virol 86(3):1670–1682

    PubMed  PubMed Central  Google Scholar 

  79. 79.

    Clarke P, Tyler KL (2009) Apoptosis in animal models of virus-induced disease. Nat Rev Microbiol 7(2):144–155

    CAS  PubMed  PubMed Central  Google Scholar 

  80. 80.

    Chowdhury S, Lee B, Onderici M, Weiss M, Mosier D (2000) Neurovirulence of glycoprotein C (gC)-deleted bovine herpesvirus type-5 (BHV-5) and BHV-5 expressing BHV-1 gC in a rabbit seizure model. J Neurovirol 6(4):284–295

    CAS  PubMed  Google Scholar 

  81. 81.

    Liman A, Engels M, Meyer G, Ackermann M (2000) Glycoprotein C of bovine herpesvirus 5 (BHV-5) confers a distinct heparin-binding phenotype to BHV-1. Arch Virol 145(10):2047–2059

    CAS  PubMed  Google Scholar 

  82. 82.

    Chowdhury SI, Lee BJ, Ozkul A, Weiss ML (2000) Bovine herpesvirus 5 glycoprotein E is important for neuroinvasiveness and neurovirulence in the olfactory pathway of the rabbit. J Virol 74(5):2094–2106

    CAS  PubMed  PubMed Central  Google Scholar 

  83. 83.

    Rijsewijk FA, Kaashoek MJ, Langeveld JP, Maris-Veldhuis MA, Magdalena J, Verschuren SB, Meloen RH, van Oirschot JT (2000) Epitopes on glycoprotein E and on the glycoprotein E/glycoprotein I complex of bovine herpesvirus 1 are expressed by all of 222 isolates and 11 vaccine strains. Arch Virol 145(5):921–936

    CAS  PubMed  Google Scholar 

  84. 84.

    Al-Mubarak A, Chowdhury S (2004) In the absence of glycoprotein I (gI), gE determines bovine herpesvirus type 5 neuroinvasiveness and neurovirulence. J Neurovirol 10(4):233–243

    CAS  PubMed  Google Scholar 

  85. 85.

    Al-Mubarak A, Zhou Y, Chowdhury SI (2004) A glycine-rich bovine herpesvirus 5 (BHV-5) gE-specific epitope within the ectodomain is important for BHV-5 neurovirulence. J Virol 78(9):4806–4816

    CAS  PubMed  PubMed Central  Google Scholar 

  86. 86.

    Liu ZF, Brum MC, Doster A, Jones C, Chowdhury SI (2008) A bovine herpesvirus type 1 mutant virus specifying a carboxyl-terminal truncation of glycoprotein E is defective in anterograde neuronal transport in rabbits and calves. J Virol 82(15):7432–7442

    CAS  PubMed  PubMed Central  Google Scholar 

  87. 87.

    Chowdhury SI, Coats J, Neis RA, Navarro SM, Paulsen DB, Feng JM (2010) A bovine herpesvirus type 1 mutant virus with truncated glycoprotein E cytoplasmic tail has defective anterograde neuronal transport in rabbit dorsal root ganglia primary neuronal cultures in a microfluidic chamber system. J Neurovirol 16(6):457–465

    CAS  PubMed  Google Scholar 

  88. 88.

    Spilki FR, Silva AD, Hübner S, Esteves PA, Franco AC, Driemeier D, Roehe PM (2004) Partial protection induced by a BHV-1 recombinant vaccine against challenge with BHV-5. Ann N Y Acad Sci 1026:247–250

    CAS  PubMed  Google Scholar 

  89. 89.

    Silva AD, Spilki FR, Franco AC, Esteves PA, Hübner SO, Driemeier D, Oliveira AP, Rijsewijk F, Roehe PM (2006) Vaccination with a gE-negative bovine herpesvirus type 1 vaccine confers insufficient protection to a bovine herpesvirus type 5 challenge. Vaccine 24(16):3313–3320

    CAS  PubMed  Google Scholar 

  90. 90.

    Chowdhury SI, Onderci M, Bhattacharjee PS, Al-Mubarak A, Weiss ML, Zhou Y (2002) Bovine herpesvirus 5 (BHV-5) Us9 is essential for BHV-5 neuropathogenesis. J Virol 76(8):3839–3851

    CAS  PubMed  PubMed Central  Google Scholar 

  91. 91.

    Butchi NB, Jones C, Pérez S, Doster A, Chowdhury SI (2007) Envelope protein Us9 is required for the anterograde transport of bovine herpesvirus type 1 from trigeminal ganglia to nose and eye upon reactivation. J Neurovirol 13(4):384–388

    CAS  PubMed  Google Scholar 

  92. 92.

    Chowdhury SI, Mahmood S, Simon J, Al-Mubarak A, Zhou Y (2006) The Us9 gene of bovine herpesvirus 1 (BHV-1) effectively complements a Us9-null strain of BHV-5 for anterograde transport, neurovirulence, and neuroinvasiveness in a rabbit model. J Virol 80(9):4396–4405

    CAS  PubMed  PubMed Central  Google Scholar 

  93. 93.

    Hübner SO, Oliveira AP, Franco AC, Esteves PA, Silva AD, Spilki FR, Rijsewijk FA, Roehe PM (2005) Experimental infection of calves with a gI, gE, US9 negative bovine herpesvirus type 5. Comp Immunol Microbiol Infect Dis 28(3):187–196

    PubMed  Google Scholar 

  94. 94.

    Zhao J, Poelaert KCK, Steukers L, Favoreel HW, Li Y, Chowdhury SI, van Drunen Littel-van den Hurk S, Caij B, Nauwynck HJ (2017) Us3 and Us9 proteins contribute to the stromal invasion of bovine herpesvirus 1 in the respiratory mucosa. J Gen Virol 98:1089. https://doi.org/10.1099/jgv.0.000764

    CAS  Article  PubMed  Google Scholar 

  95. 95.

    Abdelmagid OY, Minocha HC, Collins JK, Chowdhury SI (1995) Fine mapping of bovine herpesvirus-1 (BHV-1) glycoprotein D (gD) neutralizing epitopes by type-specific monoclonal antibodies and sequence comparison with BHV-5 gD. Virology 206(1):242–253

    CAS  PubMed  Google Scholar 

  96. 96.

    Gabev E, Tobler K, Abril C, Hilbe M, Senn C, Franchini M, Campadelli-Fiume G, Fraefel C, Ackermann M (2010) Glycoprotein D of bovine herpesvirus 5 (BoHV-5) confers an extended host range to BoHV-1 but does not contribute to invasion of the brain. J Virol 84(11):5583–5593

    CAS  PubMed  PubMed Central  Google Scholar 

  97. 97.

    Traesel CK, e Silva MS, Weiss M, Spilki FR, Weiblen R, Flores EF (2014) Genetic diversity of 3′ region of glycoprotein D gene of bovine herpesvirus 1 and 5. Virus Genes 48(3):438–447

    CAS  PubMed  Google Scholar 

  98. 98.

    Wilcox DR, Longnecker R (2016) The herpes simplex virus neurovirulence factor γ34.5: revealing virus-host interactions. PLoS Pathog 12(3):e1005449

    PubMed  PubMed Central  Google Scholar 

  99. 99.

    Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136(2):215–233

    CAS  PubMed  PubMed Central  Google Scholar 

  100. 100.

    Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297

    CAS  PubMed  Google Scholar 

  101. 101.

    Piedade D, Azevedo-Pereira JM (2016) The role of microRNAs in the pathogenesis of herpesvirus infection. Viruses 8:156. https://doi.org/10.3390/v8060156

    CAS  Article  PubMed Central  Google Scholar 

  102. 102.

    Glazov EA, Horwood PF, Assavalapsakul W, Kongsuwan K, Mitchell RW, Mitter N, Mahony TJ (2010) Characterization of microRNAs encoded by the bovine herpesvirus 1 genome. J Gen Virol 91(Pt 1):32–41

    CAS  PubMed  Google Scholar 

  103. 103.

    Tang Q, Wu YQ, Chen DS, Zhou Q, Chen HC, Liu ZF (2014) Bovine herpesvirus 5 encodes a unique pattern of microRNAs compared with bovine herpesvirus 1. J Gen Virol 95(Pt 3):671–678

    CAS  PubMed  Google Scholar 

  104. 104.

    Jaber T, Workman A, Jones C (2010) Small noncoding RNAs encoded within the bovine herpesvirus 1 latency-related gene can reduce steady-state levels of infected cell protein 0 (bICP0). J Virol 84(13):6297–6307

    CAS  PubMed  PubMed Central  Google Scholar 

  105. 105.

    Oliveira BRSM, Vieira FV, de Vieira S, da Silva SEL, Gameiro R, Flores EF, Cardoso TC (2017) Expression of miR-155 associated with Toll-like receptors 3, 7, and 9 transcription in the olfactory bulbs of cattle naturally infected with BHV5. J Neurovirol 23(5):772–778

    CAS  PubMed  Google Scholar 

  106. 106.

    Paludan SR, Bowie AG, Horan KA, Fitzgerald KA (2011) Recognition of herpesviruses by the innate immune system. Nat Rev Immunol 11(2):143–154

    CAS  PubMed  PubMed Central  Google Scholar 

  107. 107.

    Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124(4):783–801

    CAS  PubMed  Google Scholar 

  108. 108.

    Taborda N, Acevedo L, Patiño C, Forero J, López-Herrera A (2007) Actividad antiviral in vitro de extractos de Hura crepitans y Codiaeum variegatum en la replicación de herpes virus bovino tipo-1 y virus de estomatitis vesicular. Rev Colomb Ciencias Pecuarias 20:3

    Google Scholar 

  109. 109.

    Alexopoulou L, Holt A, Medzhitov R, Flavell R (2001) Recognition of double-stranded RNA and activation of NF-kappaB by Toll like receptor 3. Nature 413:732–738

    CAS  PubMed  Google Scholar 

  110. 110.

    Heil F, Hemmi H, Hochrein H, Ampenberger F, Kirschning C, Akira S, Lipford G, Wagner H, Bauer S (2004) Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303:1526–1529

    CAS  PubMed  Google Scholar 

  111. 111.

    Bauer S, Kirschning C, Häcker H, Redecke V, Hausmann S, Akira S, Wagner H, Lipford G (2001) Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc Natl Acad Sci USA 98:9237–9242

    CAS  PubMed  Google Scholar 

  112. 112.

    Borrow P, Martínez-Sobrido L, de la Torre JC (2010) Inhibition of the type I interferon antiviral response during arenavirus infection. Viruses 2(11):2443–2480

    CAS  PubMed  PubMed Central  Google Scholar 

  113. 113.

    Rensetti D, Marin M, Quintana S, Morán P, Verna A, Odeón A, Pérez S (2016) Involvement of toll-like receptors 3 and 7/8 in the neuropathogenesis of bovine herpesvirus types 1 and 5. Res Vet Sci 107:1–7

    CAS  PubMed  Google Scholar 

  114. 114.

    Marin MS, Quintana S, Faverín C, Leunda MR, Odeón AC, Pérez SE (2014) Toll-like receptor activation and expression in bovine alpha-herpesvirus infections. Res Vet Sci 96(1):196–203

    CAS  PubMed  Google Scholar 

  115. 115.

    Lundberg P, Welander P, Han X, Cantin E (2003) Herpes simplex virus type 1 DNA is immunostimulatory in vitro and in vivo. J Virol 77(20):11158–11169

    CAS  PubMed  PubMed Central  Google Scholar 

  116. 116.

    Marin MS, Quintana S, Leunda MR, Odeón AC, Pérez SE (2014) Toll-like receptor expression in the nervous system of bovine alpha-herpesvirus-infected calves. Res Vet Sci 97(2):422–429

    CAS  PubMed  Google Scholar 

  117. 117.

    Takeda K, Akira S (2004) Microbial recognition by Toll-like receptors. J Dermatol Sci 34(2):73–82

    CAS  PubMed  Google Scholar 

  118. 118.

    Kawai T, Akira S (2007) Signaling to NF-kappaB by toll-like receptors. Trends Mol Med 13:460–469

    CAS  PubMed  Google Scholar 

  119. 119.

    Ning S, Pagano JS, Barber GN (2011) IRF7: activation, regulation, modification and function. Genes Immun 12:399–414

    CAS  PubMed  PubMed Central  Google Scholar 

  120. 120.

    Liu S, Cai X, Wu J, Cong Q, Chen X, Li T et al (2015) Phosphorylation of innate immune adaptor proteins MAVS, STING, and TRIF induces IRF3 activation. Science. https://doi.org/10.1126/science.aaa2630

    Article  PubMed  PubMed Central  Google Scholar 

  121. 121.

    Babiuk LA, van Drunen Littel-van den Hurk S, Tikoo SK (1996) Immunology of bovine herpesvirus 1 infection. Vet Microbiol 53(1–2):31–42

    CAS  PubMed  Google Scholar 

  122. 122.

    Machado GF, Bernardi F, Hosomi FY, Peiró JR, Weiblen R, Roehe PM, Alessi AC, Melo GD, Ramos AT, Maiorka PC (2013) Bovine herpesvirus-5 infection in a rabbit experimental model: immunohistochemical study of the cellular response in the CNS. Microb Pathog 57:10–16

    CAS  PubMed  Google Scholar 

  123. 123.

    Jones C (2009) Regulation of innate immune responses by bovine herpesvirus 1 and infected cell protein 0 (bICP0). Viruses 1(2):255–275

    CAS  PubMed  PubMed Central  Google Scholar 

  124. 124.

    da Silva LF, Sinani D, Jones C (2012) ICP27 protein encoded by bovine herpesvirus type 1 (bICP27) interferes with promoter activity of the bovine genes encoding beta interferon 1 (IFN-β1) and IFN-β3. Virus Res 169(1):162–168

    PubMed  PubMed Central  Google Scholar 

  125. 125.

    Jones C, Chowdhury S (2010) Bovine herpesvirus type 1 (BHV-1) is an important cofactor in the bovine respiratory disease complex. Vet Clin N Am Food Anim Pract 26(2):303–321

    Google Scholar 

  126. 126.

    Saira K, Zhou Y, Jones C (2007) The infected cell protein 0 encoded by bovine herpesvirus 1 (bICP0) induces degradation of interferon response factor 3 and consequently, inhibits beta interferon promoter activity. J Virol 81(7):3077–3086

    CAS  PubMed  PubMed Central  Google Scholar 

  127. 127.

    Burucúa M, Quintana S, Odeón A, Pérez S, Marin M (2018) IFNβ expression in the nervous and respiratory system of bovine alpha-herpesviruses-infected calves. In: LXVI Annual meeting of the Argentinean Society of Immunology

  128. 128.

    Rosales J, Burucúa M, Odeón A, Marin M, Pérez S (2018) Expresión de interferón lambda en tejido nervioso de bovinos infectados con BoHV-1 o BoHV-5. In: XXXVIII Annual meeting of the Argentinean Society for Virology, p 19

  129. 129.

    Li J, Hu S, Zhou L, Ye L, Wang X, Ho J, Ho W (2011) Interferon lambda inhibits herpes simplex virus type I infection of human astrocytes and neurons. Glia 59(1):58–67

    PubMed  Google Scholar 

  130. 130.

    Hermant P, Michiels T (2014) Interferon-λ in the context of viral infections: production, response and therapeutic implications. J Innate Immun 6(5):563–574

    CAS  PubMed  PubMed Central  Google Scholar 

  131. 131.

    Zanetti M (2004) Cathelicidins, multifunctional peptides of the innate immunity. J Leukoc Biol 75(1):39–48

    PubMed  Google Scholar 

  132. 132.

    Boyton RJ, Openshaw PJ (2002) Pulmonary defences to acute respiratory infection. Br Med Bull 61:1–12

    CAS  PubMed  Google Scholar 

  133. 133.

    Baumann A, Kiener MS, Haigh B, Perreten V, Summerfield A (2017) Differential ability of bovine antimicrobial cathelicidins to mediate nucleic acid sensing by epithelial cells. Front Immunol 8:59

    PubMed  PubMed Central  Google Scholar 

  134. 134.

    Burucúa MM, Quintana S, Lendez P, Cobo ER, Ceriani MC, Dolcini G, Odeón AC, Pérez SE, Marin MS (2019) Modulation of cathelicidins, IFNβ and TNFα by bovine alpha-herpesviruses is dependent on the stage of the infectious cycle. Mol Immunol 111:136–144

    PubMed  Google Scholar 

  135. 135.

    Marin M, Burucúa M, Rensetti, D, Odeón A, Cobo E, Quintana S, Pérez S (2017) Apoptosis and host-defense peptide cathelicidins determine different outcomes of bovine alpha-herpesviruses neuropathogenesis. In: International Society of Neurochemistry (ISN) and the European Society for Neurochemistry (ESN) Meeting, Paris, France

  136. 136.

    Hydbring P, Malumbres M, Sicinski P (2016) Non-canonical functions of cell cycle cyclins and cyclin-dependent kinases. Nat Rev Mol Cell Biol 17(5):280–292

    CAS  PubMed  PubMed Central  Google Scholar 

  137. 137.

    Schang LM, Hossain A, Jones C (1996) The latency-related gene of bovine herpesvirus 1 encodes a product which inhibits cell cycle progression. J Virol 70(6):3807–3814

    CAS  PubMed  PubMed Central  Google Scholar 

  138. 138.

    Jiang Y, Hossain A, Winkler MT, Holt T, Doster A, Jones C (1998) A protein encoded by the latency-related gene of bovine herpesvirus 1 is expressed in trigeminal ganglionic neurons of latently infected cattle and interacts with cyclin-dependent kinase 2 during productive infection. J Virol 72(10):8133–8142

    CAS  PubMed  PubMed Central  Google Scholar 

  139. 139.

    Kawaguchy Y, Van Sant C, Roizman B (1997) Herpes simplex virus 1 alpha regulatory protein ICP0 interacts with and stabilizes the cell cycle regulator cyclin D3. J Virol 71(10):7328–7336

    Google Scholar 

  140. 140.

    Marin M, Burucúa M, Rensetti D, Rosales JJ, Odeón A, Pérez S (2019) Differential expression of cyclins mRNA in neural tissues of BoHV-1- and BoHV-5-infected cattle. Microb Pathog 136:103691. https://doi.org/10.1016/j.micpath.2019.103691

    CAS  Article  PubMed  Google Scholar 

  141. 141.

    Brzozowska A, Lipińska AD, Derewońko N, Lesiak D, Rychłowski M, Rąbalski Ł, Bieńkowska-Szewczyk K (2018) Inhibition of apoptosis in BHV-1-infected cells depends on Us3 serine/threonine kinase and its enzymatic activity. Virology 513:136–145

    CAS  PubMed  Google Scholar 

  142. 142.

    Hanon E, Lambot M, Hoornaert S, Lyaku J, Pastoret PP (1998) Bovine herpesvirus 1-induced apoptosis: phenotypic characterization of susceptible peripheral blood mononuclear cells. Arch Virol 143(3):441–452

    CAS  PubMed  Google Scholar 

  143. 143.

    Winkler MT, Doster A, Jones C (1999) Bovine herpesvirus 1 can infect CD4(+) T lymphocytes and induce programmed cell death during acute infection of cattle. J Virol 73(10):8657–8668

    CAS  PubMed  PubMed Central  Google Scholar 

  144. 144.

    Geiser V, Rose S, Jones C (2008) Bovine herpesvirus type 1 induces cell death by a cell-type-dependent fashion. Microb Pathog 44(6):459–466

    CAS  PubMed  Google Scholar 

  145. 145.

    Xu X, Zhang K, Huang Y, Ding L, Chen G, Zhang H, Tong D (2012) Bovine herpes virus type 1 induces apoptosis through Fas-dependent and mitochondria-controlled manner in Madin-Darby bovine kidney cells. Virol J 9:202

    CAS  PubMed  PubMed Central  Google Scholar 

  146. 146.

    Garcia AF, Novais JB, Antello TF, Silva-Frade C, Ferrarezi MC, Flores EF, Cardoso TC (2013) Bovine herpesvirus type 5 infection regulates Bax/BCL-2 ratio. Genet Mol Res 12(3):3897–3904

    CAS  PubMed  Google Scholar 

  147. 147.

    Hanon E, Keil G, van Drunen Littel-van den Hurk S, Griebel P, Griebel P (1999) Bovine herpesvirus 1-induced apoptotic cell death: role of glycoprotein D. Virology 257(1):191–197

    CAS  PubMed  Google Scholar 

  148. 148.

    Afroz S, Garg R, Fodje M, van Drunen Littel-van den Hurk S (2018) The major tegument protein of bovine herpesvirus 1, vp8, interacts with dna damage response proteins and induces apoptosis. J Virol. https://doi.org/10.1128/JVI.00773-18

    Article  PubMed  PubMed Central  Google Scholar 

  149. 149.

    Ladelfa MF, Kotsias F, Del Médico Zajac MP, Van den Broeke C, Favoreel H, Romera SA, Calamante G (2011) Effect of the Us3 protein of bovine herpesvirus 5 on the actin cytoskeleton and apoptosis. Vet Microbiol 153(3–4):361–366

    CAS  PubMed  Google Scholar 

  150. 150.

    Ciacci-Zanella J, Stone M, Henderson G, Jones C (1999) The latency-related gene of bovine herpesvirus 1 inhibits programmed cell death. J Virol 73(12):9734–9740

    CAS  PubMed  PubMed Central  Google Scholar 

  151. 151.

    Inman M, Lovato L, Doster A, Jones C (2002) A mutation in the latency-related gene of bovine herpesvirus 1 leads to impaired ocular shedding in acutely infected calves. J Virol 75(18):8507–8515

    Google Scholar 

  152. 152.

    Henderson G, Perng GC, Nesburn AB, Wechsler SL, Jones C (2004) The latency-related gene encoded by bovine herpesvirus 1 can suppress caspase 3 and caspase 9 cleavage during productive infection. J Neurovirol 10(1):64–70

    CAS  PubMed  Google Scholar 

  153. 153.

    Shen W, Jones C (2008) Open reading frame 2, encoded by the latency-related gene of bovine herpesvirus 1, has antiapoptotic activity in transiently transfected neuroblastoma cells. J Virol 82(21):10940–10945

    CAS  PubMed  PubMed Central  Google Scholar 

  154. 154.

    Silvestro C, Jones C, Bratanich A (2019) Functional analysis of the latency-related gene of bovine herpesvirus types 1 and 5. J Neurovirol. https://doi.org/10.1007/s13365-019-00745-y

    Article  PubMed  Google Scholar 

  155. 155.

    Rensetti DE, Marin MS, Morán PE, Odeón AC, Verna AE, Pérez SE (2018) Bovine herpesvirus type 5 replication and induction of apoptosis in vitro and in the trigeminal ganglion of experimentally-infected cattle. Comp Immunol Microbiol Infect Dis 57:8–14

    PubMed  Google Scholar 

  156. 156.

    Delhon G, González M, Murcia P (2002) Susceptibility of sensory neurons to apoptosis following infection by bovine herpesvirus type 1. J Gen Virol 83:2257–2267

    CAS  PubMed  Google Scholar 

  157. 157.

    Köppel R, Vogt B, Schwyzer M (1997) Immediate-early protein BICP22 of bovine herpesvirus 1 trans-represses viral promoters of different kinetic classes and is itself regulated by BICP0 at transcriptional and posttranscriptional levels. Arch Virol 142(12):2447–2464

    PubMed  Google Scholar 

  158. 158.

    Eisenberg RJ, Ponce de Leon M, Friedman HM, Fries LF, Frank MM, Hastings JC, Cohen GH (1987) Complement component C3b binds directly to purified glycoprotein C of herpes simplex virus types 1 and 2. Microb Pathog 3(6):423–435

    CAS  PubMed  Google Scholar 

  159. 159.

    Meyer G, Hanon E, Georlette D, Pastoret PP, Thiry E (1998) Bovine herpesvirus type 1 glycoprotein H is essential for penetration and propagation in cell culture. J Gen Virol 79(Pt 8):1983–1987

    CAS  PubMed  Google Scholar 

  160. 160.

    Meyer G, Bare O, Thiry E (1999) Identification and characterization of bovine herpesvirus type 5 glycoprotein H gene and gene products. J Gen Virol 80(Pt 11):2849–2859

    CAS  PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Sandra Pérez.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Handling Editor: Akbar Dastjerdi.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Marin, M., Burucúa, M., Rensetti, D. et al. Distinctive features of bovine alphaherpesvirus types 1 and 5 and the virus-host interactions that might influence clinical outcomes. Arch Virol 165, 285–301 (2020). https://doi.org/10.1007/s00705-019-04494-5

Download citation