The abundant latency-associated transcripts of herpes simplex virus type 1 are bound to polyribosomes in cultured neuronal cells and during latent infection in mouse trigeminal ganglia

Journal of Virology

Volumn 71, Issue 4, 1997, Pages 2897-2904

  Goldenberg, Daniel ^a   Mador, Nurith ^a   Ball, Melvyn J ^b   Panet, Amos ^c   Steiner, Israel ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b HEBREW UNIVERSITY   (Israel)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; EDETIC ACID; RIBOSOME RNA; VIRUS RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; FEMALE; HERPES SIMPLEX VIRUS 1; LATENT VIRUS INFECTION; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; POLYSOME; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRIGEMINUS GANGLION; VIRUS TRANSCRIPTION;

EID: 0030945465     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.71.4.2897-2904.1997     Document Type: Article

References (62)

1. Ausubel, F. M. 1994. Current protocols in molecular biology. John Wiley & Sons, Inc., New York, N.Y.
2. 2+ superoxide dismutase. Gene 99:191-195.
3. Block, T. M., S. Deshmane, J. Masonis, J. Maggioncalda, T. Valyi-Nagi, and N. W. Fraser. 1993. An HSV LAT null mutant reactivates slowly from latent infection and makes small plaques on CV-1 monolayers. Virology 192:618-630.
4. Block, T. M., J. G. Spivack, I. Steiner, S. Deshmane, M. T. McIntosh, R. P. Lirette, and N. W. Fraser. 1990. A herpes simplex virus type 1 latency-associated transcript mutant reactivates with normal kinetics from latent infection. J. Virol. 64:3417-3426. (Erratum, 64:4603.)
5. Bloom, D. C., G. B. Devi-Rao, J. M. Hill, J. G. Stevens, and E. K. Wagner. 1994. Molecular analysis of herpes simplex virus type 1 during epinephrine-induced reactivation of latently infected rabbits in vivo. J. Virol. 68:1283-1292.
6. Bloom, D. C., J. M. Hill, G. Devi-Rao, E. K. Wagner, L. T. Feldman, and J. G. Stevens. 1996. A 348-base-pair region in the latency-associated transcript facilitates herpes simplex virus type 1 reactivation. J. Virol. 70:2449-2459.
7. Brannan, C. I., E. C. Dees, R. S. Ingram, and S. M. Tilghman. 1990. The product of the H19 gene may function as an RNA. Mol. Cell. Biol. 10:28-36.
8. Chen, X., M. C. Schmidt, W. F. Goins, and J. C. Glorioso. 1995. Two herpes simplex virus type 1 latency-active promoters differ in their contribution to latency-associated transcript expression during lytic and latent infections. J. Virol. 69:7899-7908.
9. Croen, K. D., J. M. Ostrove, L. J. Dragovic, J. E. Smialek, and S. E. Straus. 1987. Latent herpes simplex virus in human trigeminal ganglia. Detection of an immediate early gene "anti-sense" transcription by in situ hybridization. N. Engl. J. Med. 317:1427-1432.
10. Deatly, A. M., J. G. Spivack, E. Lavi, and N. W. Fraser. 1987 RNA from an immediate early region of the HSV-1 genome is present in the trigeminal ganglia of latently infected mice. Proc. Natl. Acad. Sci. USA 84:3204-3208.
11. Devi-Rao, G. B., S. A. Goodart, L. M. Hecht, R. Rochford, M. K. Rice, and E. K. Wagner. 1991. Relationship between polyadenylated and nonpolyadenylated herpes simplex virus type 1 latency-associated transcripts. J. Virol. 65:2179-2190.
12. Doerig, C., L. I. Pizer, and C. L. Wilcox. 1991. An antigen encoded by the latency-associated transcript in neuronal cell cultures latently infected with herpes simplex virus type 1. J. Virol. 65:2724-2727.
13. Eckner, R., W. Ellmeier, and M. L. Birnstiel. 1991. Mature mRNA 3′ end formation stimulates RNA export from the nucleus. EMBO J. 10:3513-3522.
14. Farced, M. U., and J. G. Spivack. 1994. Two open reading frames (ORF1 and ORF2) within the 2.0-kilobase latency-associated transcript of herpes simplex virus type 1 are not essential for reactivation from latency. J. Virol. 68:8071-8081.
15. Farrell, M. J., J. M. Hill, T. P. Margolis, J. G. Stevens, E. K. Wagner, and L. T. Feldman. 1993. The herpes simplex virus type 1 reactivation function lies outside the latency-associated transcript open reading frame ORF-2. J. Virol. 67:3653-3655.
16. 15a. Goldenberg, D., et al. Unpublished data.
17. Gordon, Y. J., J. L. McKnight, J. M. Ostrove, E. Romanowski, and T. Araullo-Cruz. 1990. Host species and strain differences affect the ability of an HSV-1 ICP0 deletion mutant to establish latency and spontaneously reactivate in vivo. Virology 178:469-477.
18. Gupta, K. C., E. Ono, and X. Xu. 1996. Lack of correlation between Sendai virus P/C mRNA structure and its utilization of two AUG start sites from alternate reading frames: implications for viral bicistronic mRNAs. Biochemistry 35:1223-1231.
19. Hill, J. M., F. Sedarati, R. T. Javier, E. K. Wagner, and J. G. Stevens. 1990. Herpes simplex virus latent phase transcription facilitates in vivo reactivation. Virology 174:117-125.
20. Ho, D. Y., and E. S. Mocarski. 1989. Herpes simplex virus latent RNA (LAT) is not required for latent infection in the mouse. Proc. Natl. Acad. Sci. USA 86:7596-7600.
21. Hossain, A., L. M. Schang, and C. Jones. 1995. Identification of gene products encoded by the latency-related gene of bovine herpesvirus 1. J. Virol. 69:5345-5352.
22. Javier, R. T., J. G. Stevens, V. B. Dissette, and E. K. Wagner. 1988. A herpes simplex virus transcript abundant in latently infected neurons is dispensable for establishment of the latent state. Virology 166:254-257.
23. Klebe, R. J., and F. H. Ruddle. 1969. Neuroblastoma: cell culture analysis of a differentiating stem cell system. J. Cell. Biol. 43:69A.
24. Kozak, M. 1987. An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 15:8125-8148.
25. Kozak, M. 1991. An analysis of vertebrate mRNA sequences: intimations of translational control. J. Cell Biol. 115:887-903.
26. 134.5 gene and transcribed by an RNA 3′ coterminal with the unspliced latency-associated transcript. J. Virol. 68: 6021-6028.
27. Leib, D. A., C. L. Bogard, M. Kosz-Vnenchak, K. A. Hicks, D. M. Coen, D. M. Knipe, and P. A. Schaffer. 1989. A deletion mutant of the latency-associated transcript of herpes simplex virus type 1 reactivates from the latent state with reduced frequency. J. Virol. 63:2893-2900.
28. Leib, D. A., D. M. Coen, C. L. Bogard, K. A. Hicks, D. R. Yager, D. M. Knipe, K. L. Tyler, and P. A. Schaffer. 1989. Immediate-early regulatory gene mutants define different stages in the establishment and reactivation of herpes simplex virus latency. J. Virol. 63:759-768.
29. Lovett, P. S. 1994. Nascent peptide regulation of translation. J. Bacteriol. 176:6415-6417.
30. Mador, N., A. Panel, D. Latchman, and I. Steiner. 1995. Expression and splicing of the latency-associated transcripts of herpes simplex virus type 1 in neuronal and non-neuronal cell lines. J. Biochem. 117:1288-1297.
31. Maggioncalda, J., A. Mehta, N. W. Fraser, and T. M. Block. 1994. Analysis of a herpes simplex virus type 1 LAT mutant with a deletion between the putative promoter and the 5′ end of the 2.0-kilobase transcript. J. Virol. 68:7816-7824.
32. Maquat, L. E. 1995. When cells stop making sense: effects of nonsense codons on RNA metabolism in vertebrate cells. RNA 1:453-465.
33. McMorris, F. A., and F. H. Ruddle. 1974. Expression of neuronal phenotypes in neuroblastoma cell hybrids. Dev. Biol. 39:226-246.
34. Meyuhas, O., E. A. Thompson, Jr., and R. P. Perry. 1987. Glucocorticoids selectively inhibit translation of ribosomal protein mRNAs in P1798 lymphosarcoma cells. Mol. Cell. Biol. 7:2691-2699.
35. Mitchell, W. J., R. P. Lirette, and N. W. Fraser. 1990. Mapping of low abundance latency-associated RNA in the trigeminal ganglia of mice latently infected with herpes simplex virus type 1. J. Gen. Virol. 71:125-132.
36. Mitchell, W. J., I. Steiner, S. M. Brown, A. R. MacLean, J. H. Subak-Sharpe, and N. W. Fraser. 1990. A herpes simplex virus type 1 variant, deleted in the promoter region of the latency-associated transcripts, does not produce any detectable minor RNA species during latency in the mouse trigeminal ganglion. J. Gen. Virol. 71:953-957.
37. Nicosia, M., J. M. Zabolotny, R. P. Lirette, and N. W. Fraser. 1994. The HSV-1 2-kb latency-associated transcript is found in the cytoplasm comigrating with ribosomal subunits during productive infection. Virology 204:717-728.
38. Perng, G.-C., E. C. Dunkel, P. A. Geary, S. M. Slanina, H. Ghiasi, R. Kaiwar, A. B. Nesburn, and S. L. Wechsler. 1994. The latency-associated transcript gene of herpes simplex virus type 1 (HSV-1) is required for efficient in vivo spontaneous reactivation of HSV-1 from latency. J. Virol. 68:8045-8055.
39. Perng, G.-C., H. Ghiasi, S. M. Slanina, A. B. Nesburn, and S. L. Wechsler. 1996. The spontaneous reactivation function of the herpes simplex virus type 1 LAT gene resides completely within the first 1.5 kilobases of the 8.3-kilobase primary transcript. J. Virol. 70:976-984:
40. Perng, G.-C., S. M. Slanina, H. Ghiasi, A. B. Nesburn, and S. L. Wechsler. 1996. A 371-nucleotide region between the herpes simplex virus type 1 (HSV-1) LAT promoter and the 2-kilobase LAT is not essential for efficient spontaneous reactivation of latent HSV-1. J. Virol. 70:2014-2018.
41. + transcript of herpes simplex virus type 1 in trigeminal ganglia of latently infected mice. J. Virol: 61:1700-1703.
42. Rock, D. L., A. B. Nesburn, H. Ghiasi, J. Ong, T. L. Lewis, J. R. Lokensgard, and S. L. Wechsler. 1987. Detection of latency-related viral RNAs in trigeminal ganglia of rabbits latently infected with herpes simplex virus type 1. J. Virol. 61:3820-3826.
43. Roizman, B., and A. E. Sears. 1993. Herpes simplex viruses and their replication. Raven Press, New York, N.Y.
44. Sawtell, N. M., and R. L. Thompson. 1992. Herpes simplex virus type 1 latency-associated transcription unit promotes anatomical site-dependent establishment and reactivation from latency. J. Virol. 66:2157-2169.
45. Schang, L. M., A. Hossain, and C. Jones. 1996. The latency-related gene of bovine herpesvirus 1 encodes a product which inhibits cell cycle progression. J. Virol. 70:3807-3814.
46. Spivack, J. G., and N. W. Fraser. 1987. Detection of herpes simplex virus type 1 transcripts during latent infection in mice. J. Virol. 61:3841-3847.
47. Spivack, J. G., G. M. Woods, and N. W. Fraser. 1991. Identification of a novel latency-specific splice donor signal within the herpes simplex virus type 1 2.0-kilobase latency-associated transcript (LAT): translation inhibition of LAT open reading frames by the intron within the 2.0-kilobase LAT. J. Virol. 65:6800-6810.
48. Steinberg, R. M., A. S. Depto, J. Fortney, and J. A. Nelson. 1989. Regulated expression of early and late RNAs and proteins from the human cytomegalovirus immediate-early gene region. J. Virol. 63:2699-2708.
49. Steiner, I., and P. G. E. Kennedy. 1995. Herpes simplex virus latent infection in the nervous system. J. Neurovirol. 1:19-29.
50. Steiner, I., J. G. Spivack, S. L. Deshmane, C. I. Ace, C. M. Preston, and N. W. Fraser. 1990. A herpes simplex virus type 1 mutant containing a nontransinducing Vmw65 protein establishes latent infection in vivo in the absence of viral replication and reactivates efficiently from explanted trigeminal ganglia. J. Virol. 64:1630-1638.
51. Steiner, I., J. G. Spivack, R. P. Lirette, S. M. Brown, A. R. MacLean, J. H. Subak-Sharpe, and N. W. Fraser. 1989. Herpes simplex virus type 1 latency-associated transcripts are evidently not essential for latent infection. EMBO J. 8:505-511.
52. Steiner, I., J. G. Spivack, D. R. O'Boyle II, E. Lavi, and N. W. Fraser. 1988. Latent herpes simplex virus type 1 transcription in human trigeminal ganglia. J. Virol. 62:3493-3496.
53. Stevens, J. G. 1989. Human herpesviruses: a consideration of the latent state. Microbiol. Rev. 53:318-332.
54. Stevens, J. G., E. K. Wagner, G. B. Devi-Rao, M. L. Cook, and L. T. Feldman. 1987. RNA complementary to a herpesvirus a gene mRNA is prominent in latently infected neurons. Science 235:1056-1059.
55. Tenson, T., A. DeBlasio, and A. Mankin. 1996. A functional peptide encoded in the Escherichia coli 23S rRNA. Proc. Natl. Acad. Sci. USA 93:5641-5646.
56. Trousdale, M. D., I. Steiner, J. G. Spivack, S. L. Deshmane, S. M. Brown, A. R. MacLean, J. H. Subak-Sharpe, and N. W. Fraser. 1991. In vivo and in vitro reactivation impairment of a herpes simplex virus type 1 latency-associated transcript variant in a rabbit eye model. J. Virol. 65:6989-6993.
57. Tycowski, K. T., M.-D. Shu, and J. A. Steitz. 1996. A mammalian gene with introns instead of exons generating stable RNA products. Nature 379:464-466.
58. van der Most, R. G., W. Luytjes, S. Rutjes, and W. J. M. Spaan. 1995. Translation but not the encoded sequence is essential for the efficient propagation of the defective interfering RNAs of the coronavirus mouse hepatitis virus. J. Virol. 69:3744-3751.
59. Wagner, E. K., G. Devi-Rao, L. T. Feldman, A. T. Dobson, Y.-F. Zhang, W. M. Flanagan, and J. G. Stevens. 1988. Physical characterization of the herpes simplex virus latency-associated transcript in neurons. J. Virol. 62: 1194-1202.
60. Wagner. E. K., W. M. Flanagan, G. Devi-Rao, Y.-F. Zhang, J. M. Hill, K. P. Anderson, and J. G. Stevens. 1988. The herpes simplex virus latency-associated transcript is spliced during the latent phase of infection. J. Virol. 62:4577-4585.
61. Wroblewska, Z., J. G. Spivack, J. Otte, I. Steiner, M. Brown, A. MacLean, and N. W. Fraser. 1991. The HSV-1 latency associated transcript (LAT) variants 1704 and 1705 are glycoprotein C negative. Virus Res. 20:193-200.
62. Wu, T.-T., Y.-H. Su, T. M. Block, and J. M. Taylor. 1996. Evidence that two latency-associated transcripts of herpes simplex virus type 1 are nonlinear. J. Virol. 70:5962-5967.