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Regulation of the latency–reactivation cycle by products encoded by the bovine herpesvirus 1 (BHV-1) latency-related gene

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Abstract

Like other α-herpesvirinae subfamily members, the primary site for bovine herpesvirus 1 (BHV-1) latency is ganglionic sensory neurons. Periodically BHV-1 reactivates from latency, virus is shed, and consequently virus transmission occurs. Transcription from the latency-related (LR) gene is readily detected in neurons of trigeminal ganglia (TG) of calves or rabbits latently infected with BHV-1. Two micro-RNAs and a transcript encompassing a small open reading frame (ORF-E) located within the LR promoter can also be detected in TG of latently infected calves. A BHV-1 mutant that contains stop codons near the beginning of the first open reading frame (ORF2) within the major LR transcript (LR mutant virus) has been characterized. The LR mutant virus does not express ORF2, a reading frame that lacks an initiating ATG (reading frame B), and has reduced expression of ORF1 during productive infection. The LR mutant virus does not reactivate from latency following dexamethasone treatment suggesting that LR protein expression regulates the latency–reactivation cycle. Higher levels of apoptosis occur in TG neurons of calves infected with the LR mutant viruses when compared to wild-type BHV-1 indicating that the anti-apoptotic properties of the LR gene is necessary for the latency–reactivation cycle. ORF2 inhibits apoptosis and regulates certain viral promoters, in part, because it interacts with three cellular transcription factors (C/EBP-alpha, Notch1, and Notch3). Although ORF2 is important for the latency–reactivation cycle, we predict that other LR gene products play a supportive role during life-long latency in cattle.

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References

  • Ahmed M, Lock M, Miller CG, Fraser NW (2002) Regions of the herpes simplex virus type 1 latency-associated transcript that protect cells from apoptosis in vitro and protect neuronal cells in vivo. J Virol 76:717–729

    Article  PubMed  CAS  Google Scholar 

  • Berezovska O, McLean P, Knowles R, Lu FM, Lux SE, Hyman BT (1999) Notch1 inhibits neurite outgrowth in postmitotic primary neurons. Neuroscience 93:433–439

    Article  PubMed  CAS  Google Scholar 

  • Bratanich AC, Jones CJ (1992) Localization of cis-acting sequences in the latency-related promoter of bovine herpesvirus 1 which are regulated by neuronal cell type factors and immediate-early genes. J Virol 66:6099–6106

    PubMed  CAS  Google Scholar 

  • Bratanich AC, Hanson ND, Jones C (1992) The latency-related gene of bovine herpesvirus 1 inhibits the activity of immediate-early transcription unit 1. Virology 191:988–991

    Article  PubMed  CAS  Google Scholar 

  • Bray SJ (2006) Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7:678–689

    Article  PubMed  CAS  Google Scholar 

  • Cantin EM, Hinton DR, Chen J, Openshaw H (1995) Gamma interferon expression during acute and latent nervous system infection by herpes simplex virus type 1. J Virol 69:4898–4905

    PubMed  CAS  Google Scholar 

  • Carter JJ, Weinberg AD, Pollard A, Reeves R, Magnuson JA, Magnuson NS (1989) Inhibition of T-lymphocyte mitogenic responses and effects on cell functions by bovine herpesvirus 1. J Virol 63:1525–1530

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Collins PL, McIntosh K, Chanock RM (2001) Respiratory syncytial virus. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin A, Roizman B, Straus SE (eds) Fields virology, 4th edn. Lippincott, Williams, and Wilkins, Philadelphia, pp 1443–1485

    Google Scholar 

  • Cornell R, Eisen JS (2005) Notch in the pathway: the roles of Notch signalling in neural crest development. Semin Cell Dev Biol 16:663–672

    Article  PubMed  CAS  Google Scholar 

  • Delhon G, Jones C (1997) Identification of DNA sequences in the latency related promoter of bovine herpes virus type 1 which are bound by neuronal specific factors. Virus Res 51:93–103

    Article  PubMed  CAS  Google Scholar 

  • Devireddy LR, Jones C (1998) Alternative splicing of the latency-related transcript of bovine herpesvirus 1 yields RNAs containing unique open reading frames. J Virol 72:7294–7301

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Devireddy L, Zhang Y, Jones C (2003) Cloning and initial characterization of an alternatively spliced transcript encoded by the bovine herpes virus 1 latency related (LR) gene. J Neurovirol 9:612–622

    PubMed  CAS  Google Scholar 

  • Ehebauer M, Penelope P, Arias AM (2006) Notch, a universal arbiter of cell fate decisions. Science 314:1414–1415

    Article  PubMed  CAS  Google Scholar 

  • Eskra L, Splitter GA (1997) Bovine herpesvirus-1 infects activated CD4+ lymphocytes. J Gen Virol 78:2159–2166

    PubMed  CAS  Google Scholar 

  • Fraefel C, Zeng J, Choffat Y, Engels M, Schwyzer M, Ackermann M (1994) Identification and zinc dependence of the bovine herpesvirus 1 transactivator protein BICP0. J Virol 68:3154–3162

    PubMed  CAS  Google Scholar 

  • Frank GH (1984) Bacteria as etiologic agents in bovine respiratory disease. In: Loan RW (ed) Bovine respiratory disease. Texas A&M University Press, College Station, pp 384–392

    Google Scholar 

  • Freeman RS, Estus S, Johnson EM Jr (1994) Analysis of cell cycle-related gene expression in postmitotic neurons: selective induction of Cyclin D1 during programmed cell death. Neuron 12:343–355

    Article  PubMed  CAS  Google Scholar 

  • Fuchs M, Hubert P, Detterer J, Rziha HJ (1999) Detection of bovine herpesvirus type 1 in blood from naturally infected cattle by using a sensitive PCR that discriminates between wild-type virus and virus lacking glycoprotein E. J Clin Microbiol 37:2498–2507

    PubMed  CAS  Google Scholar 

  • Geiser V, Jones C (2005) The latency related gene encoded by bovine herpesvirus 1 encodes a small regulatory RNA that inhibits cell growth. J Neurovirol 11:563–570

    Article  PubMed  CAS  Google Scholar 

  • Geiser V, Inman M, Zhang Y, Jones C (2002) The latency related (LR) gene of bovine herpes virus 1 (BHV-1) can inhibit the ability of bICP0 to activate productive infection. J Gen Virol 83:2965–2971

    PubMed  CAS  Google Scholar 

  • Gill JS, Windebank AJ (1998) Cisplatin-induced apoptosis in rat dorsal root ganglion neurons is associated with attempted entry into the cell cycle. J Clin Invest 101:2842–2850

    Article  PubMed  CAS  Google Scholar 

  • Griebel P, Qualtiere L, Davis WC, Gee A, Bielefeldt Ohmann H, Lawman MJ, Babiuk LA (1987a) T lymphocyte population dynamics and function following a primary bovine herpesvirus type-1 infection. Viral Immunol 1:287–304

    Article  PubMed  Google Scholar 

  • Griebel PJ, Qualtiere L, Davis WC, Lawman MJ, Babiuk LA (1987b) Bovine peripheral blood leukocyte subpopulation dynamics following a primary bovine herpesvirus-1 infection. Viral Immunol 1:267–286

    Article  PubMed  Google Scholar 

  • Griebel P, Ohmann HB, Lawman MJ, Babiuk LA (1990) The interaction between bovine herpesvirus type 1 and activated bovine T lymphocytes. J Gen Virol 71:369–377

    Article  PubMed  Google Scholar 

  • Halford WP, Gebhardt BM, Carr DJ (1996) Persistent cytokine expression in trigeminal ganglion latently infected with herpes simplex virus type 1. J Immunol 157:3542–3549

    PubMed  CAS  Google Scholar 

  • Hariharan MJ, Nataraj C, Srikumaran S (1993) Down regulation of murine MHC class I expression by bovine herpesvirus 1. Viral Immunol 6:273–284

    Article  PubMed  CAS  Google Scholar 

  • Henderson G, Zhang Y, Jones C (2005) The bovine herpesvirus 1 gene encoding infected cell protein 0 (bICP0) can inhibit interferon-dependent transcription in the absence of other viral genes. J Gen Virol 86:2697–2702

    Article  PubMed  CAS  Google Scholar 

  • Herrup K, Busser JC (1995) The induction of multiple cell cycle events precedes target-related neuronal death. Development 121:2385–2395

    PubMed  CAS  Google Scholar 

  • Highlander SK (2001) Molecular genetic analysis of virulence in Mannheimia (Pasteurella) haemolytica. Front Biosci :D1128–1150

  • Highlander SK, Fedorova MD, Dusek DM, Panciera R, Alvarez LE, Renehart C (2000) Inactivation of Pasteurella (Mannheimia) haemolytica leukotoxin causes partial attenuation of virulence in a calf challenge model. Infect Immun 68:3916–3922

    Article  PubMed  CAS  Google Scholar 

  • Hinkley S, Hill AB, Srikumaran S (1998) Bovine herpesvirus-1 infection affects the peptide transport activity in bovine cells. Virus Res 53:91–96

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Inman M, Perng G-C, Henderson G, Ghiasi H, Nesburn AB, Wechsler SL, Jones C (2001a) Region of herpes simplex virus type 1 latency-associated transcript sufficient for wild-type spontaneous reactivation promotes cell survival in tissue culture. J Virol 75:3636–3646

    Article  PubMed  CAS  Google Scholar 

  • Inman M, Lovato L, Doster A, Jones C (2001b) A mutation in the latency-related gene of bovine herpesvirus 1 leads to impaired ocular shedding in acutely infected calves. J Virol 75:8507–8515

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Inman M, Zhou J, Webb H, Jones C (2004) Identification of a novel transcript containing a small open reading frame that is expressed during latency, and is antisense to the latency related gene of bovine herpes virus 1 (BHV-1). J Virol 78:5438–5447

    Article  PubMed  CAS  Google Scholar 

  • Jaber T, Henderson G, Li S, Perng G-C, Carpenter D, Wechsler S, Jones C (2009) Identification of a novel herpes simplex virus type 1 (HSV-1) transcript and protein (AL3) expressed during latency. J Gen Virol 90:2342–2352

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jaber T, Workman A, Jones C (2010b) Small non-coding RNAs encoded within the bovine herpesvirus 1 latency related gene can reduce steady state levels of infected cell protein 0 (bICP0). J Virol 84

  • 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 72:8133–8142

    PubMed  CAS  Google Scholar 

  • Jiang Y, Inman M, Zhang Y, Posadas NA, Jones C (2004) A mutation in the latency related gene of bovine herpesvirus 1 (BHV-1) inhibits protein expression of a protein from open reading frame 2 (ORF-2) and an adjacent reading frame during productive infection. J Virol 78:3184–3189

    Article  PubMed  CAS  Google Scholar 

  • Jin L, Perng G-C, Nesburn AB, Jones C, Wechsler SL (2005) The baculovirus inhibitor of apoptosis gene (cpIAP) can restore reactivation of latency to a herpes simplex virus type 1 that does not express the latency associated transcript (LAT). J Virol 79:12286–12295

    Google Scholar 

  • Jin L, Carpenter D, Moerdyk-Schauwecker M, Vanarsdall AL, Osorio N, Hsiang C, Jones C, Wechsler SL (2008) Cellular FLIP can substitute for the herpes simplex virus type 1 LAT gene to support a wild type virus reactivation phenotype in mice. J Neurovirol 14:389–400

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jones C, Delhon G, Bratanich A, Kutish G, Rock D (1990) Analysis of the transcriptional promoter which regulates the latency-related transcript of bovine herpesvirus 1. J Virol 64:1164–1170

    PubMed  CAS  Google Scholar 

  • Jones C, Newby TJ, Holt T, Doster A, Stone M, Ciacci-Zanella J, Webster CJ, Jackwood MW (2000) Analysis of latency in cattle after inoculation with a temperature sensitive mutant of bovine herpesvirus 1 (RLB106). Vaccine 18:3185–3195

    Article  PubMed  CAS  Google Scholar 

  • Justice NJ, Jan YN (2002) Variations on the Notch pathway in neural development. Curr Opin Neurobiol 12:64–70

    Article  PubMed  CAS  Google Scholar 

  • Khanna KM, Bonneau RH, Kinchington PR, Hendricks RL (2003) Herpes simplex virus-specific memory CD8+ T cells are selectively activated and retained in latently infected sensory ganglia. Immunity 18:593–603

    Article  PubMed  CAS  Google Scholar 

  • Knickelbein JE, Khanna KM, Yee MB, Baty CJ, Kinchington PR, Hendricks RL (2008) Noncytotoxic lytic granule-mediated CD8+ T cell inhibition of HSV-1 reactivation from neuronal latency. Science 322:268–272

    Article  PubMed  CAS  Google Scholar 

  • Koppers-Lalic EA, Reits EAJ, Ressing ME, Lipinska AD, Abele R, Koch J, Rezende MM, Admiraal P, van Leeuwen D, Bienkowsaka-Szewczyc K, Mettenleiter TC, Rijsewijk FAM, Tampe R, Neefjes J, Wiertz EJHJ (2005) Varicelloviruses avoid T cell recognition by UL49.5-mediated inactivation of the transporter associated with antigen processing. Proc Natl Acad Sci USA 102:5144–5149

    Article  PubMed  CAS  Google Scholar 

  • KosZ-Vnenchak JJ, Coen DM, Knipe DM (1993) Evidence for a novel regulatory pathway for herpes simplex virus gene expression in trigeminal ganglion neurons. J Virol 67:5383–5393

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Levkau B, Koyama H, Raines EW, Clurman BE, Herren B, Orth K, Roberts JM, Ross R (1998) Cleavage of p21Cip1/Waf1 and p27Kip1 mediates apoptosis in endothelial cells through activation of Cdk2: role of a caspase cascade. Mol Cell 1:553–563

    Article  PubMed  CAS  Google Scholar 

  • Liu T, Tang Q, Hendricks RL (1996) Inflammatory infiltration of the trigeminal ganglion after herpes simplex virus type 1 corneal infection. J Virol 70:264–271

    PubMed  CAS  Google Scholar 

  • Liu T, Khanna KM, Chen X, Fink DJ, Hendricks RL (2000) CD8(+) T cells can block herpes simplex virus type 1 (HSV-1) reactivation from latency in sensory neurons. J Exp Med 191:1459–1466

    Article  PubMed  CAS  Google Scholar 

  • Liu T, Khanna KM, Carriere BN, Hendricks RL (2001) Gamma interferon can prevent herpes simplex virus type 1 reactivation from latency in sensory neurons. J Virol 75:11178–11184

    Article  PubMed  CAS  Google Scholar 

  • Lovato L, Inman M, Henderson G, Doster A, Jones C (2003) Infection of cattle with a bovine herpesvirus 1 (BHV-1) strain that contains a mutation in the latency related gene leads to increased apoptosis in trigeminal ganglia during the transition from acute infection to latency. J Virol 77:4848–4857

    Article  PubMed  CAS  Google Scholar 

  • Meikrantz W, Schlegel R (1996) Suppression of apoptosis by dominant negative mutants of cyclin-dependent protein kinases. J Biol Chem 271:10205–10209

    Article  PubMed  CAS  Google Scholar 

  • Meikrantz W, Geisselbrecht S, Tam SW, Schlegel R (1994) Activation of cyclin A-dependent protein kinases during apoptosis. Proc Natl Acad Sci USA 91:3754–3758

    Article  PubMed  CAS  Google Scholar 

  • Meyer F, Perez S, Jiang Y, Zhou Y, Henderson G, Jones C (2007a) Identification of a novel protein encoded by the latency-related gene of bovine herpesvirus 1. J Neurovirol 13:569–578

    Article  PubMed  CAS  Google Scholar 

  • Meyer F, Perez S, Geiser V, Sintek M, Inman M, Jones C (2007b) A protein encoded by the bovine herpes virus 1 (BHV-1) latency related gene interacts with specific cellular regulatory proteins, including the CCAAT enhancer binding protein alpha (C/EBP-a). J Virol 81:59–67

    Article  PubMed  CAS  Google Scholar 

  • Misra V, Bratanich AC, Carpenter D, O’Hare P (1994) Protein and DNA elements involved in transactivation of the promoter of the bovine herpesvirus (BHV) 1 IE-1 transcription unit by the BHV alpha gene trans-inducing factor. J Virol 68:4898–4909

    PubMed  CAS  Google Scholar 

  • Misra V, Walker S, Hayes S, O’Hare P (1995) The bovine herpesvirus alpha gene trans-inducing factor activates transcription by mechanisms different from those of its herpes simplex virus type 1 counterpart VP16. J Virol 69:5209–5216

    PubMed  CAS  Google Scholar 

  • Mott K, Osorio N, Jin L, Brick D, Naito J, Cooper J, Henderson G, Inman M, Jones C, Wechsler SL, Perng G-C (2003) The bovine herpesvirus 1 LR ORF2 is crucial for this gene's ability to restore the high reactivation phenotype to a Herpes simplex virus-1 LAT null mutant. J Gen Virol 84:2975–2985

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Naidr P, Somasundaram K, Krishna S (2003) Activated Notch1 inhibits p53-induced apoptosis and sustains transformation by human papilloma virus type 16 E6 and E7 oncogenes through a PI3K-PKB/Akt-dependent pathway. J Virol 77:7106–7112

    Article  CAS  Google Scholar 

  • Nataraj C, Eidmann S, Hariharan MJ, Sur JH, Perry GA, Srikumaran S (1997) Bovine herpesvirus 1 downregulates the expression of bovine MHC class I molecules. Viral Immunol 10:21–34

    Article  PubMed  CAS  Google Scholar 

  • Nichol PF, Chang JY, Johnson EM Jr, Olivo PD (1996) Herpes simplex virus gene expression in neurons: viral DNA synthesis is a critical regulatory event in the branch point between lytic and latent pathways. J Virol 70:5476–5486

    Google Scholar 

  • Park DS, Farinelli SE, Greene LA (1996) Inhibitors of cyclin-dependent kinases promote survival of post-mitotic neuronally differentiated PC12 cells and sympathetic neurons. J Biol Chem 271:8161–8169

    Article  PubMed  Google Scholar 

  • Park DS, Levine B, Ferrari G, Greene LA (1997a) Cyclin dependent kinase inhibitors and dominant negative cyclin dependent kinase 4 and 6 promote survival of NGF-deprived sympathetic neurons. J Neurosci 17:8975–8983

    PubMed  CAS  Google Scholar 

  • Park DS, Morris EJ, Greene LA, Geller HM (1997b) G1/S cell cycle blockers and inhibitors of cyclin-dependent kinases suppress camptothecin-induced neuronal apoptosis. J Neurosci 17:1256–1270

    PubMed  CAS  Google Scholar 

  • Perez 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 43:393–401

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Perng G-C, Jones C, Ciacci-Zanella J, Stone M, Henderson G, Yukht A, Slanina SM, Hoffman FM, Ghiasi H, Nesburn AB, Wechsler SL (2000) Virus-induced neuronal apoptosis blocked by the herpes simplex virus latency-associated transcript (LAT). Science 287:1500–1503

    Article  PubMed  CAS  Google Scholar 

  • Perng G-C, Maguen B, Jing L, Mott KR, Osorio N, Slanina SM, Yukht A, Ghiasi H, Nesburn AB, Inman M, Henderson G, Jones C, Wechsler SL (2002a) A novel herpes simplex virus type 1 (HSV-1) transcript (AL-RNA) antisense to the 5’ end of LAT (latency associated transcript) produces a protein in infected rabbits. J Virol 76:8003–8010

    Article  PubMed  CAS  Google Scholar 

  • Perng G-C, Maguen B, Jin L, Mott KR, Osorio N, Slanina SM, Yukht A, Ghiasi H, Nesburn AB, Inman M, Henderson G, Jones C, Wechsler SL (2002b) A gene capable of blocking apoptosis can substitute for the herpes simplex virus type 1 latency-associated transcript gene and restore wild-type reactivation levels. J Virol 76:1224–1235

    Article  PubMed  CAS  Google Scholar 

  • Pesola JM, Zhu J, Knipe DM, Coen DM (2005) Herpes simplex virus 1 immediate-early and early gene expression during reactivation from latency under conditions that prevent infectious virus production. J Virol 79:14516–14525

    Article  PubMed  CAS  Google Scholar 

  • Prbhakaran K, Sheridan BS, Kinchington PR, Khanna KM, Decman V, Lathrop K, Hendricks RL (2005) Sensory neurons regulate the effector functions of CD8+ T cells in controlling HSV-1 latency ex vivo. Immunity 23:515–523

    Article  CAS  Google Scholar 

  • Rice SA, Long MC, Lam V, Schaffer PA, Spencer CA (1995) Herpes simplex virus immediate-early protein ICP22 is required for viral modification of host RNA polymerase II and establishment of the normal viral transcription program. J Virol 69:5550–5559

    PubMed  CAS  Google Scholar 

  • Rice JA, LC-M, Hodgins DC, Shewen PE (2008) Mannheimia haemolytica and bovine respiratory disease. Anim Health Res Rev 8:117–128

    Article  Google Scholar 

  • Rivera-Rivas JJ, Kisiela D, Czuprynski CJ (2009) Bovine herpesvirus type 1 infection of bovine bronchial epithelial cells increases neutrophil adhesion and activation. Vet Immunol Immunopathol 131:167–176

    Article  PubMed  CAS  Google Scholar 

  • Rock DL, Beam SL, Mayfield JE (1987) Mapping bovine herpesvirus type 1 latency-related RNA in trigeminal ganglia of latently infected rabbits. J Virol 61:3827–3831

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Sade H, Krishna S, Sarin A (2004) The anti-apoptotic effect of Notch-1 requires p56lck-dependent, AKT/PKB-mediated signaling in T cells. J Biol Chem 279:2937–2944

    Article  PubMed  CAS  Google Scholar 

  • Saira K, Jones C (2009) The infected cell protein 0 encoded by bovine herpesvirus 1 (bICP0) associates with interferon regulatory factor 7 (IRF7), and consequently inhibits beta interferon promoter activity. J Virol 83:3977–3981

    Article  PubMed  CAS  Google Scholar 

  • 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 (IRF3), and consequently inhibits beta interferon promoter activity. J Virol 81:3077–3086

    Article  PubMed  CAS  Google Scholar 

  • Schang L, Jones C (1997) Analysis of bovine herpesvirus 1 transcripts during a primary infection of trigeminal ganglia of cattle. J Virol 71:6786–6795

    PubMed  CAS  Google Scholar 

  • 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 70:3807–3814

    PubMed  CAS  Google Scholar 

  • 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 82:10940–10945

    Article  PubMed  CAS  Google Scholar 

  • Shen W, Silva MS, Jaber T, Vitvitskaia O, Li S, Henderson G, Jones C (2009) Two small RNAs encoded within the first 1.5 kb of the herpes simplex virus type 1 (HSV-1) latency-associated transcript (LAT) can inhibit productive infection, and cooperate to inhibit apoptosis. J Virol 90:9131–9139

    Article  CAS  Google Scholar 

  • Shimeld C, Whiteland JL, Nicholls SM, Grinfeld E, Easty DL, Gao H, Hill TJ (1995) Immune cell infiltration and persistence in the mouse trigeminal ganglion after infection of the cornea with herpes simplex virus type 1. J Neuroimmunol 61:7–16

    Article  PubMed  CAS  Google Scholar 

  • Shimeld C, Whiteland JL, Williams NA, Easty DL, Hill TJ (1996) Reactivation of herpes simplex virus type 1 in the mouse trigeminal ganglion: an in vivo study of virus antigen and immune cell infiltration. J Gen Virol 77:2583–2590

    Article  PubMed  CAS  Google Scholar 

  • Shimeld C, Whiteland JL, Williams NA, Easty DL, Hill TJ (1997) Cytokine production in the nervous system of mice during acute and latent infection with herpes simplex virus type 1. J Gen Virol 78:3317–3325

    PubMed  CAS  Google Scholar 

  • Shirvan A, Ziv I, Barzilai A, Djaldeti R, Zilkh-Falb R, Michlin T, Melamed E (1997a) Induction of mitosis-related genes during dopamine-triggered apoptosis in sympathetic neurons. J Neural Transm (Suppl 50):67–78

  • Shirvan A, Ziv I, Machlin T, Zilkha-Falb R, Melamed E, Barzilai A (1997b) Two waves of cyclin B and proliferating cell nuclear antigen expression during dopamine-triggered neuronal apoptosis. J Neurochem 69:539–549

    Article  PubMed  CAS  Google Scholar 

  • Shirvan A, Ziv I, Zilkha-Falb R, Machlyn T, Barzilai A, Melamed E (1998) Expression of cell cycle-related genes during neuronal apoptosis: is there a distinct pattern? Neurochem Res 23:767–777

    Article  PubMed  CAS  Google Scholar 

  • Smith CA, Bates P, Rivera-Gonzalez R, Gu B, DeLuca NA (1993) ICP4, the major transcriptional regulatory protein of herpes simplex virus type 1, forms a tripartite complex with TATA-binding protein and TFIIB. J Virol 67:4676–4687

    PubMed  CAS  Google Scholar 

  • Songer JG, Post KW (2005) The Genera Mannheimia and Pasteurella. In: Duncan L (ed) Veterinary microbiology: bacterial and fungal agents of animal disease. Elsevier Saunders, St Louis

    Google Scholar 

  • Srikumaran S, Ambagela A, Kelling CL (2007) Immune evasion by pathogens of bovine respiratory disease complex. Anim Health Res Rev 8:215–229

    Article  PubMed  Google Scholar 

  • Tal-Singer R, Lasner TM, Podrzucki W, Skokotas A, Leary JJ, Berger SL, Frazer NW (1997) Gene expression during reactivation of herpes simplex virus type 1 from latency in the peripheral nervous system is different from that during lytic infection of tissue cultures. J Virol 71:5268–5276

    PubMed  CAS  Google Scholar 

  • Theil D, Derfuss T, Paripovic I, Herberger S, Meinl E, Schueler O, Strupp M, Arbusow V, Brandt T (2003) Latent herpesvirus infection in human trigeminal ganglia causes chronic immune response. Am J Pathol 163:2179–2184

    Article  PubMed  CAS  Google Scholar 

  • Thompson RL, Preston CM, Sawtell NM (2009) De novo synthesis of VP16 coordinates the exit form HSV latency in vivo. Plos Pathog 5:1–12

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wang T, Holt CM, Xu C, Ridley C, Jones R, Baron M, Trump D (2007) Notch 3 activation modulates growth behavior and cross talks to Wnt/TCF signalling pathway. Cell Signal 19:2458–2467

    Article  PubMed  CAS  Google Scholar 

  • 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 73:8657–8668

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Winkler MTC, Doster A, Jones C (2000b) Persistence and reactivation of bovine herpesvirus 1 in the tonsil of latently infected calves. J Virol 74:5337–5346

    Article  PubMed  CAS  Google Scholar 

  • Winkler MT, Doster A, Sur JH, Jones C (2002) Analysis of bovine trigeminal ganglia following infection with bovine herpesvirus 1. Vet Microbiol 86:139–155

    Article  PubMed  CAS  Google Scholar 

  • Wirth UV, Gunkel K, Engels M, Schwyzer M (1989) Spatial and temporal distribution of bovine herpesvirus 1 transcripts. J Virol 63:4882–4889

    PubMed  CAS  Google Scholar 

  • 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 65:195–205

    PubMed  CAS  Google Scholar 

  • 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 66:2763–2772

    PubMed  CAS  Google Scholar 

  • Workman A, Jones C (2010) Bovine herpesvirus 1 productive infection and bICP0 early promoter activity are stimulated by E2F1. J Virol 84:6308–6317

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 85:2536–2546

    Article  PubMed  CAS  Google Scholar 

  • Yang L, Voytek CC, Margolis TP (2000) Immunohistochemical analysis of primary sensory neurons latently infected with herpes simplex virus type 1. J Virol 74:209–217

    Article  PubMed  CAS  Google Scholar 

  • Zecchinon L, Fett T, Desmecht D (2005) How Mannheimia haemolytica defeats host defense through a kiss of death mechanism. Vet Res 36:133–156

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported by grants from the USDA, Agriculture and Food Research Initiative Competitive Grants Program (08-00891 and 09-01653). A grant to the Nebraska Center for Virology (1P20RR15635) supported certain aspects of these studies. Devis Sinani was partially supported by a fellowship from a Ruth L. Kirschstein National Research Service Award 1 T32 AIO60547 (National Institute of Allergy and Infectious Diseases).

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Correspondence to Clinton Jones.

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Jones, C., da Silva, L.F. & Sinani, D. Regulation of the latency–reactivation cycle by products encoded by the bovine herpesvirus 1 (BHV-1) latency-related gene. J. Neurovirol. 17, 535–545 (2011). https://doi.org/10.1007/s13365-011-0060-3

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  • DOI: https://doi.org/10.1007/s13365-011-0060-3

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