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. 1994 Nov;68(11):6871–6882. doi: 10.1128/jvi.68.11.6871-6882.1994

Induction of herpes simplex virus type 1 immediate-early gene expression by a cellular activity expressed in Vero and NB41A3 cells after growth arrest-release.

W M Ralph Jr 1, M S Cabatingan 1, P A Schaffer 1
PMCID: PMC237122  PMID: 7933067

Abstract

Infected cell protein 0 (ICP0), a major immediate-early regulatory protein of herpes simplex virus type 1 (HSV-1), activates expression of all classes of HSV genes as well as a variety of heterologous viral and cellular genes. Previous studies have shown that a cellular activity expressed maximally in Vero cells 8 h after release from growth arrest in the G0/G1 phase of the cell cycle can enhance plaque formation and gene expression of a mutant virus (7134) lacking both copies of the gene encoding ICP0 (W. Cai and P. Schaffer, J. Virol. 65:4078-4090, 1991). This observation suggests that the cellular activity can substitute for ICP0 to activate viral gene expression. To further characterize this cellular activity, Vero and NB41A3 (mouse neuroblastoma) cells were transfected at various times after release from growth arrest with promoter-chloramphenicol acetyltransferase (CAT) constructs containing promoters representing the major kinetic classes of HSV genes, and CAT activity was measured from 2 to 24 h postrelease. The results of these tests demonstrate that CAT expression from immediate-early promoter-CAT plasmids was enhanced 10- and 3-fold when Vero and NB41A3 cells were transfected at 6 and 2 h postrelease, respectively. In contrast, only low levels of immediate-early promoter-driven CAT activity were apparent when cells were transfected at later times postrelease. No significant stimulation of CAT activity was observed from promoter-CAT plasmids containing representative early or late HSV promoters or a heterologous viral (simian virus 40 early) promoter. Differences in the efficiency of uptake of plasmid DNA by cells at various times postrelease did not account for the observed differences in CAT expression. Unlike Vero cells, in which cell division resumed after release from growth arrest, division of NB41A3 cells did not resume. Rather, these cells displayed morphological features suggestive of a differentiated phenotype. Collectively, these findings demonstrate that a cellular activity expressed in Vero and NB41A3 cells after release from growth arrest can activate HSV gene expression by enhancing immediate-early gene expression.

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  1. Abraham I., Sampson K. E., Powers E. A., Mayo J. K., Ruff V. A., Leach K. L. Increased PKA and PKC activities accompany neuronal differentiation of NT2/D1 cells. J Neurosci Res. 1991 Jan;28(1):29–39. doi: 10.1002/jnr.490280104. [DOI] [PubMed] [Google Scholar]
  2. Ash R. J. Butyrate-induced reversal of herpes simplex virus restriction in neuroblastoma cells. Virology. 1986 Dec;155(2):584–592. doi: 10.1016/0042-6822(86)90218-7. [DOI] [PubMed] [Google Scholar]
  3. Bailey A. C., Thompson R. A sequence-specific DNA-binding protein recognising a GA-rich element cooperates with Oct-1 at the herpes simplex virus type 1 IE3 promoter. Intervirology. 1992;34(2):74–85. doi: 10.1159/000150265. [DOI] [PubMed] [Google Scholar]
  4. Batchelor A. H., O'Hare P. Localization of cis-acting sequence requirements in the promoter of the latency-associated transcript of herpes simplex virus type 1 required for cell-type-specific activity. J Virol. 1992 Jun;66(6):3573–3582. doi: 10.1128/jvi.66.6.3573-3582.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Batchelor A. H., O'Hare P. Regulation and cell-type-specific activity of a promoter located upstream of the latency-associated transcript of herpes simplex virus type 1. J Virol. 1990 Jul;64(7):3269–3279. doi: 10.1128/jvi.64.7.3269-3279.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  7. Breakfield X. O., Neale E. A., Neale J. H., Jacobowitz D. M. Localized catecholamine storage associated with granules in murine neuroblastoma cells. Brain Res. 1975 Jul 11;92(2):237–256. doi: 10.1016/0006-8993(75)90273-5. [DOI] [PubMed] [Google Scholar]
  8. Bzik D. J., Preston C. M. Analysis of DNA sequences which regulate the transcription of herpes simplex virus immediate early gene 3: DNA sequences required for enhancer-like activity and response to trans-activation by a virion polypeptide. Nucleic Acids Res. 1986 Jan 24;14(2):929–943. doi: 10.1093/nar/14.2.929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cai W. Z., Schaffer P. A. Herpes simplex virus type 1 ICP0 plays a critical role in the de novo synthesis of infectious virus following transfection of viral DNA. J Virol. 1989 Nov;63(11):4579–4589. doi: 10.1128/jvi.63.11.4579-4589.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cai W., Schaffer P. A. A cellular function can enhance gene expression and plating efficiency of a mutant defective in the gene for ICP0, a transactivating protein of herpes simplex virus type 1. J Virol. 1991 Aug;65(8):4078–4090. doi: 10.1128/jvi.65.8.4078-4090.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ciesielski-Treska J., Ulrich G. Monoamine regulation of adenosine 3',5'-monophosphate in homogeneous neuronal cultures from chick brain hemispheres. Neurochem Res. 1980 Oct;5(10):1097–1106. doi: 10.1007/BF00966167. [DOI] [PubMed] [Google Scholar]
  12. Cole A. J., Saffen D. W., Baraban J. M., Worley P. F. Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature. 1989 Aug 10;340(6233):474–476. doi: 10.1038/340474a0. [DOI] [PubMed] [Google Scholar]
  13. Cook M. L., Stevens J. G. Pathogenesis of herpetic neuritis and ganglionitis in mice: evidence for intra-axonal transport of infection. Infect Immun. 1973 Feb;7(2):272–288. doi: 10.1128/iai.7.2.272-288.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Curran T., Morgan J. I. Barium modulates c-fos expression and post-translational modification. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8521–8524. doi: 10.1073/pnas.83.22.8521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. DeLuca N. A., Schaffer P. A. Activation of immediate-early, early, and late promoters by temperature-sensitive and wild-type forms of herpes simplex virus type 1 protein ICP4. Mol Cell Biol. 1985 Aug;5(8):1997–2008. doi: 10.1128/mcb.5.8.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. DeLuca N. A., Schaffer P. A. Activities of herpes simplex virus type 1 (HSV-1) ICP4 genes specifying nonsense peptides. Nucleic Acids Res. 1987 Jun 11;15(11):4491–4511. doi: 10.1093/nar/15.11.4491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. DeLuca N. A., Schaffer P. A. Physical and functional domains of the herpes simplex virus transcriptional regulatory protein ICP4. J Virol. 1988 Mar;62(3):732–743. doi: 10.1128/jvi.62.3.732-743.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Dixon R. A., Schaffer P. A. Fine-structure mapping and functional analysis of temperature-sensitive mutants in the gene encoding the herpes simplex virus type 1 immediate early protein VP175. J Virol. 1980 Oct;36(1):189–203. doi: 10.1128/jvi.36.1.189-203.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Dobson A. T., Sederati F., Devi-Rao G., Flanagan W. M., Farrell M. J., Stevens J. G., Wagner E. K., Feldman L. T. Identification of the latency-associated transcript promoter by expression of rabbit beta-globin mRNA in mouse sensory nerve ganglia latently infected with a recombinant herpes simplex virus. J Virol. 1989 Sep;63(9):3844–3851. doi: 10.1128/jvi.63.9.3844-3851.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Dreyer L. L., Sydiskis R. J., Bashirelahi N. Effect of dexamethasone on herpes simplex virus replication in mouse neuroblastoma cells (NB41A3): receptor characteristics. J Clin Lab Anal. 1989;3(4):236–243. doi: 10.1002/jcla.1860030408. [DOI] [PubMed] [Google Scholar]
  21. Efstathiou S., Minson A. C., Field H. J., Anderson J. R., Wildy P. Detection of herpes simplex virus-specific DNA sequences in latently infected mice and in humans. J Virol. 1986 Feb;57(2):446–455. doi: 10.1128/jvi.57.2.446-455.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Everett R. D. The products of herpes simplex virus type 1 (HSV-1) immediate early genes 1, 2 and 3 can activate HSV-1 gene expression in trans. J Gen Virol. 1986 Nov;67(Pt 11):2507–2513. doi: 10.1099/0022-1317-67-11-2507. [DOI] [PubMed] [Google Scholar]
  23. Everett R. D. Trans activation of transcription by herpes virus products: requirement for two HSV-1 immediate-early polypeptides for maximum activity. EMBO J. 1984 Dec 20;3(13):3135–3141. doi: 10.1002/j.1460-2075.1984.tb02270.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Felgner P. L., Gadek T. R., Holm M., Roman R., Chan H. W., Wenz M., Northrop J. P., Ringold G. M., Danielsen M. Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7413–7417. doi: 10.1073/pnas.84.21.7413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gelman I. H., Silverstein S. Identification of immediate early genes from herpes simplex virus that transactivate the virus thymidine kinase gene. Proc Natl Acad Sci U S A. 1985 Aug;82(16):5265–5269. doi: 10.1073/pnas.82.16.5265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gerster T., Roeder R. G. A herpesvirus trans-activating protein interacts with transcription factor OTF-1 and other cellular proteins. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6347–6351. doi: 10.1073/pnas.85.17.6347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Greenberg M. E., Greene L. A., Ziff E. B. Nerve growth factor and epidermal growth factor induce rapid transient changes in proto-oncogene transcription in PC12 cells. J Biol Chem. 1985 Nov 15;260(26):14101–14110. [PubMed] [Google Scholar]
  28. Greenberg M. E., Ziff E. B., Greene L. A. Stimulation of neuronal acetylcholine receptors induces rapid gene transcription. Science. 1986 Oct 3;234(4772):80–83. doi: 10.1126/science.3749894. [DOI] [PubMed] [Google Scholar]
  29. Hamlin J. L., Pardee A. B. S phase synchrony in monolayer CHO cultures. Exp Cell Res. 1976 Jul;100(2):265–275. doi: 10.1016/0014-4827(76)90147-6. [DOI] [PubMed] [Google Scholar]
  30. He X., Treacy M. N., Simmons D. M., Ingraham H. A., Swanson L. W., Rosenfeld M. G. Expression of a large family of POU-domain regulatory genes in mammalian brain development. Nature. 1989 Jul 6;340(6228):35–41. doi: 10.1038/340035a0. [DOI] [PubMed] [Google Scholar]
  31. Honess R. W., Roizman B. Regulation of herpesvirus macromolecular synthesis. I. Cascade regulation of the synthesis of three groups of viral proteins. J Virol. 1974 Jul;14(1):8–19. doi: 10.1128/jvi.14.1.8-19.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Honess R. W., Roizman B. Regulation of herpesvirus macromolecular synthesis: sequential transition of polypeptide synthesis requires functional viral polypeptides. Proc Natl Acad Sci U S A. 1975 Apr;72(4):1276–1280. doi: 10.1073/pnas.72.4.1276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Leib D. A., Coen D. M., Bogard C. L., Hicks K. A., Yager D. R., Knipe D. M., Tyler K. L., Schaffer P. A. Immediate-early regulatory gene mutants define different stages in the establishment and reactivation of herpes simplex virus latency. J Virol. 1989 Feb;63(2):759–768. doi: 10.1128/jvi.63.2.759-768.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Leib D. A., Nadeau K. C., Rundle S. A., Schaffer P. A. The promoter of the latency-associated transcripts of herpes simplex virus type 1 contains a functional cAMP-response element: role of the latency-associated transcripts and cAMP in reactivation of viral latency. Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):48–52. doi: 10.1073/pnas.88.1.48. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Liao C. F., Schilling W. P., Birnbaumer M., Birnbaumer L. Cellular responses to stimulation of the M5 muscarinic acetylcholine receptor as seen in murine L cells. J Biol Chem. 1990 Jul 5;265(19):11273–11284. [PubMed] [Google Scholar]
  36. Mackem S., Roizman B. Structural features of the herpes simplex virus alpha gene 4, 0, and 27 promoter-regulatory sequences which confer alpha regulation on chimeric thymidine kinase genes. J Virol. 1982 Dec;44(3):939–949. doi: 10.1128/jvi.44.3.939-949.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Maxwell I. H., Harrison G. S., Wood W. M., Maxwell F. A DNA cassette containing a trimerized SV40 polyadenylation signal which efficiently blocks spurious plasmid-initiated transcription. Biotechniques. 1989 Mar;7(3):276–280. [PubMed] [Google Scholar]
  38. McCarthy A. M., McMahan L., Schaffer P. A. Herpes simplex virus type 1 ICP27 deletion mutants exhibit altered patterns of transcription and are DNA deficient. J Virol. 1989 Jan;63(1):18–27. doi: 10.1128/jvi.63.1.18-27.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. McKnight J. L., Kristie T. M., Roizman B. Binding of the virion protein mediating alpha gene induction in herpes simplex virus 1-infected cells to its cis site requires cellular proteins. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7061–7065. doi: 10.1073/pnas.84.20.7061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. McMahan L., Schaffer P. A. The repressing and enhancing functions of the herpes simplex virus regulatory protein ICP27 map to C-terminal regions and are required to modulate viral gene expression very early in infection. J Virol. 1990 Jul;64(7):3471–3485. doi: 10.1128/jvi.64.7.3471-3485.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Milbrandt J. Nerve growth factor rapidly induces c-fos mRNA in PC12 rat pheochromocytoma cells. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4789–4793. doi: 10.1073/pnas.83.13.4789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Murphy R. A., Pantazis N. J., Arnason B. G., Young M. Secretion of a nerve growth factor by mouse neuroblastoma cells in culture. Proc Natl Acad Sci U S A. 1975 May;72(5):1895–1898. doi: 10.1073/pnas.72.5.1895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. O'Hare P., Goding C. R. Herpes simplex virus regulatory elements and the immunoglobulin octamer domain bind a common factor and are both targets for virion transactivation. Cell. 1988 Feb 12;52(3):435–445. doi: 10.1016/s0092-8674(88)80036-9. [DOI] [PubMed] [Google Scholar]
  44. O'Hare P., Hayward G. S. Three trans-acting regulatory proteins of herpes simplex virus modulate immediate-early gene expression in a pathway involving positive and negative feedback regulation. J Virol. 1985 Dec;56(3):723–733. doi: 10.1128/jvi.56.3.723-733.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Patwardhan S., Gashler A., Siegel M. G., Chang L. C., Joseph L. J., Shows T. B., Le Beau M. M., Sukhatme V. P. EGR3, a novel member of the Egr family of genes encoding immediate-early transcription factors. Oncogene. 1991 Jun;6(6):917–928. [PubMed] [Google Scholar]
  46. Perry L. J., McGeoch D. J. The DNA sequences of the long repeat region and adjoining parts of the long unique region in the genome of herpes simplex virus type 1. J Gen Virol. 1988 Nov;69(Pt 11):2831–2846. doi: 10.1099/0022-1317-69-11-2831. [DOI] [PubMed] [Google Scholar]
  47. Perry L. J., Rixon F. J., Everett R. D., Frame M. C., McGeoch D. J. Characterization of the IE110 gene of herpes simplex virus type 1. J Gen Virol. 1986 Nov;67(Pt 11):2365–2380. doi: 10.1099/0022-1317-67-11-2365. [DOI] [PubMed] [Google Scholar]
  48. Preston C. M., Frame M. C., Campbell M. E. A complex formed between cell components and an HSV structural polypeptide binds to a viral immediate early gene regulatory DNA sequence. Cell. 1988 Feb 12;52(3):425–434. doi: 10.1016/s0092-8674(88)80035-7. [DOI] [PubMed] [Google Scholar]
  49. Rice S. A., Knipe D. M. Gene-specific transactivation by herpes simplex virus type 1 alpha protein ICP27. J Virol. 1988 Oct;62(10):3814–3823. doi: 10.1128/jvi.62.10.3814-3823.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Rock D. L., Fraser N. W. Detection of HSV-1 genome in central nervous system of latently infected mice. Nature. 1983 Apr 7;302(5908):523–525. doi: 10.1038/302523a0. [DOI] [PubMed] [Google Scholar]
  51. Rock D. L., Fraser N. W. Latent herpes simplex virus type 1 DNA contains two copies of the virion DNA joint region. J Virol. 1985 Sep;55(3):849–852. doi: 10.1128/jvi.55.3.849-852.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Rock D. L., Nesburn A. B., Ghiasi H., Ong J., Lewis T. L., Lokensgard J. R., Wechsler S. L. Detection of latency-related viral RNAs in trigeminal ganglia of rabbits latently infected with herpes simplex virus type 1. J Virol. 1987 Dec;61(12):3820–3826. doi: 10.1128/jvi.61.12.3820-3826.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Russell J., Stow N. D., Stow E. C., Preston C. M. Herpes simplex virus genes involved in latency in vitro. J Gen Virol. 1987 Dec;68(Pt 12):3009–3018. doi: 10.1099/0022-1317-68-12-3009. [DOI] [PubMed] [Google Scholar]
  54. Sacks W. R., Schaffer P. A. Deletion mutants in the gene encoding the herpes simplex virus type 1 immediate-early protein ICP0 exhibit impaired growth in cell culture. J Virol. 1987 Mar;61(3):829–839. doi: 10.1128/jvi.61.3.829-839.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Sainz de la Maza M., Wells P. A., Foster C. S. Cyclic nucleotide modulation of herpes simplex virus latency and reactivation. Invest Ophthalmol Vis Sci. 1989 Oct;30(10):2154–2159. [PubMed] [Google Scholar]
  56. Schaffner W. How do different transcription factors binding the same DNA sequence sort out their jobs? Trends Genet. 1989 Feb;5(2):37–39. doi: 10.1016/0168-9525(89)90017-6. [DOI] [PubMed] [Google Scholar]
  57. Schneider F. H. Effects of sodium butyrate on mouse neuroblastoma cells in culture. Biochem Pharmacol. 1976 Oct 15;25(20):2309–2317. doi: 10.1016/0006-2952(76)90015-0. [DOI] [PubMed] [Google Scholar]
  58. Schubert D., Humphreys S., Baroni C., Cohn M. In vitro differentiation of a mouse neuroblastoma. Proc Natl Acad Sci U S A. 1969 Sep;64(1):316–323. doi: 10.1073/pnas.64.1.316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Sears A. E., Halliburton I. W., Meignier B., Silver S., Roizman B. Herpes simplex virus 1 mutant deleted in the alpha 22 gene: growth and gene expression in permissive and restrictive cells and establishment of latency in mice. J Virol. 1985 Aug;55(2):338–346. doi: 10.1128/jvi.55.2.338-346.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Sheff K. Y., Yorek M. A., Long J. P. Hemicholinium-3 derivatives A-4 and A-5 alter choline metabolism in NB41A3 neuroblastoma cells. J Pharmacol Exp Ther. 1991 Apr;257(1):323–330. [PubMed] [Google Scholar]
  61. Smith R. L., Pizer L. I., Johnson E. M., Jr, Wilcox C. L. Activation of second-messenger pathways reactivates latent herpes simplex virus in neuronal cultures. Virology. 1992 May;188(1):311–318. doi: 10.1016/0042-6822(92)90760-m. [DOI] [PubMed] [Google Scholar]
  62. Stevens J. G. Human herpesviruses: a consideration of the latent state. Microbiol Rev. 1989 Sep;53(3):318–332. doi: 10.1128/mr.53.3.318-332.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Su L., Knipe D. M. Herpes simplex virus alpha protein ICP27 can inhibit or augment viral gene transactivation. Virology. 1989 Jun;170(2):496–504. doi: 10.1016/0042-6822(89)90441-8. [DOI] [PubMed] [Google Scholar]
  64. Tanaka M., Grossniklaus U., Herr W., Hernandez N. Activation of the U2 snRNA promoter by the octamer motif defines a new class of RNA polymerase II enhancer elements. Genes Dev. 1988 Dec;2(12B):1764–1778. doi: 10.1101/gad.2.12b.1764. [DOI] [PubMed] [Google Scholar]
  65. Triezenberg S. J., LaMarco K. L., McKnight S. L. Evidence of DNA: protein interactions that mediate HSV-1 immediate early gene activation by VP16. Genes Dev. 1988 Jun;2(6):730–742. doi: 10.1101/gad.2.6.730. [DOI] [PubMed] [Google Scholar]
  66. Walicke P. A., Patterson P. H. On the role of cyclic nucleotides in the transmitter choice made by cultured sympathetic neurons. J Neurosci. 1981 Apr;1(4):333–342. doi: 10.1523/JNEUROSCI.01-04-00333.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Wheatley S. C., Dent C. L., Wood J. N., Latchman D. S. Elevation of cyclic AMP levels in cell lines derived from latently infectable sensory neurons increases their permissivity for herpes virus infection by activating the viral immediate-early 1 gene promoter. Brain Res Mol Brain Res. 1992 Jan;12(1-3):149–154. doi: 10.1016/0169-328x(92)90078-p. [DOI] [PubMed] [Google Scholar]
  68. Wickramasinghe S. N. Neuroglial and neuroblastoma cell lines are capable of metabolizing ethanol via an alcohol-dehydrogenase-independent pathway. Alcohol Clin Exp Res. 1987 Jun;11(3):234–237. doi: 10.1111/j.1530-0277.1987.tb01295.x. [DOI] [PubMed] [Google Scholar]
  69. Wymer J. P., Aprhys C. M., Chung T. D., Feng C. P., Kulka M., Aurelian L. Immediate early and functional AP-1 cis-response elements are involved in the transcriptional regulation of the large subunit of herpes simplex virus type 2 ribonucleotide reductase (ICP10). Virus Res. 1992 May;23(3):253–270. doi: 10.1016/0168-1702(92)90112-m. [DOI] [PubMed] [Google Scholar]
  70. Zwaagstra J. C., Ghiasi H., Nesburn A. B., Wechsler S. L. Identification of a major regulatory sequence in the latency associated transcript (LAT) promoter of herpes simplex virus type 1 (HSV-1). Virology. 1991 May;182(1):287–297. doi: 10.1016/0042-6822(91)90672-x. [DOI] [PubMed] [Google Scholar]
  71. de De La Peña N. C., Bal E., Puricelli L., Diaz A., De Lustig E. S. Interferon in the replication of herpes simplex virus in normal and pathological nerve cells. IARC Sci Publ. 1978;(24 Pt 2):1055–1066. [PubMed] [Google Scholar]

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