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. 1996 Jun;70(6):4071–4080. doi: 10.1128/jvi.70.6.4071-4080.1996

mRNA export correlates with activation of transcription in human subgroup C adenovirus-infected cells.

U C Yang 1, W Huang 1, S J Flint 1
PMCID: PMC190288  PMID: 8648745

Abstract

To investigate the mechanisms by which viral mRNA species are distinguished from their cellular counterparts for export to the cytoplasm during the late phase of subgroup C adenovirus infection, we have examined the metabolism of several cellular and viral mRNAs in human cells productively infected by adenovirus type 5 (Ad5). Several cellular mRNAs that were refractory to, or could escape from, adenovirus-induced inhibition of export of mRNA from the nucleus have been identified. This group includes Hsp70 mRNAs synthesized upon heat shock of Ad5-infected 293 or HeLa cells during the late phase of infection. However, successful export in Ad5-infected cells is not a specific response to heat shock, for beta-tubulin and interferon-inducible mRNAs were also refractory to virus-induced export inhibition. The export of these cellular mRNAs, like that of viral late mRNAs, required the E1B 55-kDa protein. Export to the cytoplasm during the late phase of Ad5 infection of several cellular mRNAs, including members of the Hsp70 family whose export was inhibited under some, but not other, conditions, indicates that viral mRNA species cannot be selectively exported by virtue of specific sequence or structural features. Cellular and viral late mRNAs that can be exported from the nucleus to the cytoplasm were expressed from genes whose transcription was induced or activated during the late phase of Ad5 infection. Consistent with the possibility that successful export is governed by transcriptional activation in the late phase of adenovirus infection, newly synthesized viral early E1A mRNA was subject to export inhibition during the late phase of infection.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adam S. A., Dreyfuss G. Adenovirus proteins associated with mRNA and hnRNA in infected HeLa cells. J Virol. 1987 Oct;61(10):3276–3283. doi: 10.1128/jvi.61.10.3276-3283.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aebi M., Fäh J., Hurt N., Samuel C. E., Thomis D., Bazzigher L., Pavlovic J., Haller O., Staeheli P. cDNA structures and regulation of two interferon-induced human Mx proteins. Mol Cell Biol. 1989 Nov;9(11):5062–5072. doi: 10.1128/mcb.9.11.5062. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aiello L., Guilfoyle R., Huebner K., Weinmann R. Adenovirus 5 DNA sequences present and RNA sequences transcribed in transformed human embryo kidney cells (HEK-Ad-5 or 293). Virology. 1979 Apr 30;94(2):460–469. doi: 10.1016/0042-6822(79)90476-8. [DOI] [PubMed] [Google Scholar]
  4. Akusjärvi G., Persson H. Controls of RNA splicing and termination in the major late adenovirus transcription unit. Nature. 1981 Jul 30;292(5822):420–426. doi: 10.1038/292420a0. [DOI] [PubMed] [Google Scholar]
  5. Anderson C. W., Baum P. R., Gesteland R. F. Processing of adenovirus 2-induced proteins. J Virol. 1973 Aug;12(2):241–252. doi: 10.1128/jvi.12.2.241-252.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Babich A., Feldman L. T., Nevins J. R., Darnell J. E., Jr, Weinberger C. Effect of adenovirus on metabolism of specific host mRNAs: transport control and specific translational discrimination. Mol Cell Biol. 1983 Jul;3(7):1212–1221. doi: 10.1128/mcb.3.7.1212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Babiss L. E., Ginsberg H. S., Darnell J. E., Jr Adenovirus E1B proteins are required for accumulation of late viral mRNA and for effects on cellular mRNA translation and transport. Mol Cell Biol. 1985 Oct;5(10):2552–2558. doi: 10.1128/mcb.5.10.2552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Beltz G. A., Flint S. J. Inhibition of HeLa cell protein synthesis during adenovirus infection. Restriction of cellular messenger RNA sequences to the nucleus. J Mol Biol. 1979 Jun 25;131(2):353–373. doi: 10.1016/0022-2836(79)90081-0. [DOI] [PubMed] [Google Scholar]
  9. Berget S. M., Moore C., Sharp P. A. Spliced segments at the 5' terminus of adenovirus 2 late mRNA. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3171–3175. doi: 10.1073/pnas.74.8.3171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Berk A. J. Adenovirus promoters and E1A transactivation. Annu Rev Genet. 1986;20:45–79. doi: 10.1146/annurev.ge.20.120186.000401. [DOI] [PubMed] [Google Scholar]
  11. Berkner K. L., Sharp P. A. Effect of the tripartite leader on synthesis of a non-viral protein in an adenovirus 5 recombinant. Nucleic Acids Res. 1985 Feb 11;13(3):841–857. doi: 10.1093/nar/13.3.841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Beyer A. L., Bouton A. H., Hodge L. D., Miller O. L., Jr Visualization of the major late R strand transcription unit of adenovirus serotype 2. J Mol Biol. 1981 Apr 5;147(2):269–295. doi: 10.1016/0022-2836(81)90441-1. [DOI] [PubMed] [Google Scholar]
  13. Blobel G. Gene gating: a hypothesis. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8527–8529. doi: 10.1073/pnas.82.24.8527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Bridge E., Ketner G. Interaction of adenoviral E4 and E1b products in late gene expression. Virology. 1990 Feb;174(2):345–353. doi: 10.1016/0042-6822(90)90088-9. [DOI] [PubMed] [Google Scholar]
  15. Carter K. C., Bowman D., Carrington W., Fogarty K., McNeil J. A., Fay F. S., Lawrence J. B. A three-dimensional view of precursor messenger RNA metabolism within the mammalian nucleus. Science. 1993 Feb 26;259(5099):1330–1335. doi: 10.1126/science.8446902. [DOI] [PubMed] [Google Scholar]
  16. Castiglia C. L., Flint S. J. Effects of adenovirus infection on rRNA synthesis and maturation in HeLa cells. Mol Cell Biol. 1983 Apr;3(4):662–671. doi: 10.1128/mcb.3.4.662. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Chatterjee P. K., Flint S. J. Partition of E1A proteins between soluble and structural fractions of adenovirus-infected and -transformed cells. J Virol. 1986 Dec;60(3):1018–1026. doi: 10.1128/jvi.60.3.1018-1026.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Chow L. T., Gelinas R. E., Broker T. R., Roberts R. J. An amazing sequence arrangement at the 5' ends of adenovirus 2 messenger RNA. Cell. 1977 Sep;12(1):1–8. doi: 10.1016/0092-8674(77)90180-5. [DOI] [PubMed] [Google Scholar]
  19. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Cowan N. J., Wilde C. D., Chow L. T., Wefald F. C. Structural variation among human beta-tubulin genes. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4877–4881. doi: 10.1073/pnas.78.8.4877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Cutt J. R., Shenk T., Hearing P. Analysis of adenovirus early region 4-encoded polypeptides synthesized in productively infected cells. J Virol. 1987 Feb;61(2):543–552. doi: 10.1128/jvi.61.2.543-552.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Denome R. M., Werner E. A., Patterson R. J. RNA metabolism in nuclei: adenovirus and heat shock alter intranuclear RNA compartmentalization. Nucleic Acids Res. 1989 Mar 11;17(5):2081–2098. doi: 10.1093/nar/17.5.2081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Dolph P. J., Racaniello V., Villamarin A., Palladino F., Schneider R. J. The adenovirus tripartite leader may eliminate the requirement for cap-binding protein complex during translation initiation. J Virol. 1988 Jun;62(6):2059–2066. doi: 10.1128/jvi.62.6.2059-2066.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Enssle J., Kugler W., Hentze M. W., Kulozik A. E. Determination of mRNA fate by different RNA polymerase II promoters. Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10091–10095. doi: 10.1073/pnas.90.21.10091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  26. Flint J., Shenk T. Adenovirus E1A protein paradigm viral transactivator. Annu Rev Genet. 1989;23:141–161. doi: 10.1146/annurev.ge.23.120189.001041. [DOI] [PubMed] [Google Scholar]
  27. Flint S. J., Beltz G. A., Linzer D. I. Synthesis and processing of simian virus 40-specific RNA in adenovirus-infected, simian virus 40-transformed human cells. J Mol Biol. 1983 Jun 25;167(2):335–359. doi: 10.1016/s0022-2836(83)80339-8. [DOI] [PubMed] [Google Scholar]
  28. Flint S. J., Gallimore P. H., Sharp P. A. Comparison of viral RNA sequences in adenovirus 2-transformed and lytically infected cells. J Mol Biol. 1975 Jul 25;96(1):47–68. doi: 10.1016/0022-2836(75)90181-3. [DOI] [PubMed] [Google Scholar]
  29. Flint S. J., Plumb M. A., Yang U. C., Stein G. S., Stein J. L. Effect of adenovirus infection on expression of human histone genes. Mol Cell Biol. 1984 Jul;4(7):1363–1371. doi: 10.1128/mcb.4.7.1363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Flint S. J. Regulation of adenovirus mRNA formation. Adv Virus Res. 1986;31:169–228. doi: 10.1016/s0065-3527(08)60264-x. [DOI] [PubMed] [Google Scholar]
  31. Friedman R. L., Manly S. P., McMahon M., Kerr I. M., Stark G. R. Transcriptional and posttranscriptional regulation of interferon-induced gene expression in human cells. Cell. 1984 Oct;38(3):745–755. doi: 10.1016/0092-8674(84)90270-8. [DOI] [PubMed] [Google Scholar]
  32. Gaynor R. B., Hillman D., Berk A. J. Adenovirus early region 1A protein activates transcription of a nonviral gene introduced into mammalian cells by infection or transfection. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1193–1197. doi: 10.1073/pnas.81.4.1193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Goldfarb D. S. Nuclear transport. Curr Opin Cell Biol. 1989 Jun;1(3):441–446. doi: 10.1016/0955-0674(89)90003-3. [DOI] [PubMed] [Google Scholar]
  34. Graham F. L., Smiley J., Russell W. C., Nairn R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol. 1977 Jul;36(1):59–74. doi: 10.1099/0022-1317-36-1-59. [DOI] [PubMed] [Google Scholar]
  35. Groudine M., Peretz M., Weintraub H. Transcriptional regulation of hemoglobin switching in chicken embryos. Mol Cell Biol. 1981 Mar;1(3):281–288. doi: 10.1128/mcb.1.3.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Gunning P., Ponte P., Okayama H., Engel J., Blau H., Kedes L. Isolation and characterization of full-length cDNA clones for human alpha-, beta-, and gamma-actin mRNAs: skeletal but not cytoplasmic actins have an amino-terminal cysteine that is subsequently removed. Mol Cell Biol. 1983 May;3(5):787–795. doi: 10.1128/mcb.3.5.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Halbert D. N., Cutt J. R., Shenk T. Adenovirus early region 4 encodes functions required for efficient DNA replication, late gene expression, and host cell shutoff. J Virol. 1985 Oct;56(1):250–257. doi: 10.1128/jvi.56.1.250-257.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Hayes B. W., Telling G. C., Myat M. M., Williams J. F., Flint S. J. The adenovirus L4 100-kilodalton protein is necessary for efficient translation of viral late mRNA species. J Virol. 1990 Jun;64(6):2732–2742. doi: 10.1128/jvi.64.6.2732-2742.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Hearing P., Shenk T. Sequence-independent autoregulation of the adenovirus type 5 E1A transcription unit. Mol Cell Biol. 1985 Nov;5(11):3214–3221. doi: 10.1128/mcb.5.11.3214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Ho Y. S., Galos R., Williams J. Isolation of type 5 adenovirus mutants with a cold-sensitive host range phenotype: genetic evidence of an adenovirus transformation maintenance function. Virology. 1982 Oct 15;122(1):109–124. doi: 10.1016/0042-6822(82)90381-6. [DOI] [PubMed] [Google Scholar]
  41. Huang J. T., Schneider R. J. Adenovirus inhibition of cellular protein synthesis involves inactivation of cap-binding protein. Cell. 1991 Apr 19;65(2):271–280. doi: 10.1016/0092-8674(91)90161-q. [DOI] [PubMed] [Google Scholar]
  42. Huang S., Spector D. L. Nascent pre-mRNA transcripts are associated with nuclear regions enriched in splicing factors. Genes Dev. 1991 Dec;5(12A):2288–2302. doi: 10.1101/gad.5.12a.2288. [DOI] [PubMed] [Google Scholar]
  43. Hunt C., Morimoto R. I. Conserved features of eukaryotic hsp70 genes revealed by comparison with the nucleotide sequence of human hsp70. Proc Natl Acad Sci U S A. 1985 Oct;82(19):6455–6459. doi: 10.1073/pnas.82.19.6455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Izaurralde E., Mattaj I. W. Transport of RNA between nucleus and cytoplasm. Semin Cell Biol. 1992 Aug;3(4):279–288. doi: 10.1016/1043-4682(92)90029-u. [DOI] [PubMed] [Google Scholar]
  45. Kao H. T., Nevins J. R. Transcriptional activation and subsequent control of the human heat shock gene during adenovirus infection. Mol Cell Biol. 1983 Nov;3(11):2058–2065. doi: 10.1128/mcb.3.11.2058. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Katze M. G., Chen Y. T., Krug R. M. Nuclear-cytoplasmic transport and VAI RNA-independent translation of influenza viral messenger RNAs in late adenovirus-infected cells. Cell. 1984 Jun;37(2):483–490. doi: 10.1016/0092-8674(84)90378-7. [DOI] [PubMed] [Google Scholar]
  47. Kaufman R. J. Identification of the components necessary for adenovirus translational control and their utilization in cDNA expression vectors. Proc Natl Acad Sci U S A. 1985 Feb;82(3):689–693. doi: 10.1073/pnas.82.3.689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Kelly J. M., Porter A. C., Chernajovsky Y., Gilbert C. S., Stark G. R., Kerr I. M. Characterization of a human gene inducible by alpha- and beta-interferons and its expression in mouse cells. EMBO J. 1986 Jul;5(7):1601–1606. doi: 10.1002/j.1460-2075.1986.tb04402.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Lawrence J. B., Singer R. H., Marselle L. M. Highly localized tracks of specific transcripts within interphase nuclei visualized by in situ hybridization. Cell. 1989 May 5;57(3):493–502. doi: 10.1016/0092-8674(89)90924-0. [DOI] [PubMed] [Google Scholar]
  50. Leff T., Elkaim R., Goding C. R., Jalinot P., Sassone-Corsi P., Perricaudet M., Kédinger C., Chambon P. Individual products of the adenovirus 12S and 13S EIa mRNAs stimulate viral EIIa and EIII expression at the transcriptional level. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4381–4385. doi: 10.1073/pnas.81.14.4381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Leppard K. N. Selective effects on adenovirus late gene expression of deleting the E1b 55K protein. J Gen Virol. 1993 Apr;74(Pt 4):575–582. doi: 10.1099/0022-1317-74-4-575. [DOI] [PubMed] [Google Scholar]
  52. Leppard K. N., Shenk T. The adenovirus E1B 55 kd protein influences mRNA transport via an intranuclear effect on RNA metabolism. EMBO J. 1989 Aug;8(8):2329–2336. doi: 10.1002/j.1460-2075.1989.tb08360.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Lindquist S. The heat-shock response. Annu Rev Biochem. 1986;55:1151–1191. doi: 10.1146/annurev.bi.55.070186.005443. [DOI] [PubMed] [Google Scholar]
  54. Logan J., Shenk T. Adenovirus tripartite leader sequence enhances translation of mRNAs late after infection. Proc Natl Acad Sci U S A. 1984 Jun;81(12):3655–3659. doi: 10.1073/pnas.81.12.3655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Maquat L. E. Nuclear mRNA export. Curr Opin Cell Biol. 1991 Dec;3(6):1004–1012. doi: 10.1016/0955-0674(91)90121-e. [DOI] [PubMed] [Google Scholar]
  56. Martinez-Palomo A., Granboulan N. Electron microscopy of adenovirus 12 replication. II. High-resolution autoradiography of infected KB cells labeled with tritiated thymidine. J Virol. 1967 Oct;1(5):1010–1018. doi: 10.1128/jvi.1.5.1010-1018.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Martínez-Palomo A. Ultrastructural study of the replication of human adenovirus type 12 in cultured cells. Pathol Microbiol (Basel) 1968;31(3):147–164. doi: 10.1159/000162013. [DOI] [PubMed] [Google Scholar]
  58. Mathews M. B., Shenk T. Adenovirus virus-associated RNA and translation control. J Virol. 1991 Nov;65(11):5657–5662. doi: 10.1128/jvi.65.11.5657-5662.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. McMaster G. K., Carmichael G. G. Analysis of single- and double-stranded nucleic acids on polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4835–4838. doi: 10.1073/pnas.74.11.4835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Moore M., Schaack J., Baim S. B., Morimoto R. I., Shenk T. Induced heat shock mRNAs escape the nucleocytoplasmic transport block in adenovirus-infected HeLa cells. Mol Cell Biol. 1987 Dec;7(12):4505–4512. doi: 10.1128/mcb.7.12.4505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Moyne G., Pichard E., Bernhard W. Localization of simian adenovirus 7 (SA 7) transcription and replication in lytic infection. An ultracytochemical and autoradiographical study. J Gen Virol. 1978 Jul;40(1):77–92. doi: 10.1099/0022-1317-40-1-77. [DOI] [PubMed] [Google Scholar]
  62. Nevins J. R., Wilson M. C. Regulation of adenovirus-2 gene expression at the level of transcriptional termination and RNA processing. Nature. 1981 Mar 12;290(5802):113–118. doi: 10.1038/290113a0. [DOI] [PubMed] [Google Scholar]
  63. O'Malley R. P., Duncan R. F., Hershey J. W., Mathews M. B. Modification of protein synthesis initiation factors and the shut-off of host protein synthesis in adenovirus-infected cells. Virology. 1989 Jan;168(1):112–118. doi: 10.1016/0042-6822(89)90409-1. [DOI] [PubMed] [Google Scholar]
  64. Ornelles D. A., Shenk T. Localization of the adenovirus early region 1B 55-kilodalton protein during lytic infection: association with nuclear viral inclusions requires the early region 4 34-kilodalton protein. J Virol. 1991 Jan;65(1):424–429. doi: 10.1128/jvi.65.1.424-429.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Osborne M. A., Silver P. A. Nucleocytoplasmic transport in the yeast Saccharomyces cerevisiae. Annu Rev Biochem. 1993;62:219–254. doi: 10.1146/annurev.bi.62.070193.001251. [DOI] [PubMed] [Google Scholar]
  66. Pilder S., Moore M., Logan J., Shenk T. The adenovirus E1B-55K transforming polypeptide modulates transport or cytoplasmic stabilization of viral and host cell mRNAs. Mol Cell Biol. 1986 Feb;6(2):470–476. doi: 10.1128/mcb.6.2.470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Riley D., Flint S. J. RNA-binding properties of a translational activator, the adenovirus L4 100-kilodalton protein. J Virol. 1993 Jun;67(6):3586–3595. doi: 10.1128/jvi.67.6.3586-3595.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Rosbash M., Singer R. H. RNA travel: tracks from DNA to cytoplasm. Cell. 1993 Nov 5;75(3):399–401. doi: 10.1016/0092-8674(93)90373-x. [DOI] [PubMed] [Google Scholar]
  69. Sarnow P., Hearing P., Anderson C. W., Halbert D. N., Shenk T., Levine A. J. Adenovirus early region 1B 58,000-dalton tumor antigen is physically associated with an early region 4 25,000-dalton protein in productively infected cells. J Virol. 1984 Mar;49(3):692–700. doi: 10.1128/jvi.49.3.692-700.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Schneider R. J. Cap-independent translation in adenovirus infected cells. Curr Top Microbiol Immunol. 1995;203:117–129. doi: 10.1007/978-3-642-79663-0_6. [DOI] [PubMed] [Google Scholar]
  71. Schröder H. C., Bachmann M., Diehl-Seifert B., Müller W. E. Transport of mRNA from nucleus to cytoplasm. Prog Nucleic Acid Res Mol Biol. 1987;34:89–142. doi: 10.1016/s0079-6603(08)60494-8. [DOI] [PubMed] [Google Scholar]
  72. Shaw A. R., Ziff E. B. Transcripts from the adenovirus-2 major late promoter yield a single early family of 3' coterminal mRNAs and five late families. Cell. 1980 Dec;22(3):905–916. doi: 10.1016/0092-8674(80)90568-1. [DOI] [PubMed] [Google Scholar]
  73. Smiley J. K., Young M. A., Bansbach C. C., Flint S. J. The metabolism of small cellular RNA species during productive subgroup C adenovirus infection. Virology. 1995 Jan 10;206(1):100–107. doi: 10.1016/s0042-6822(95)80024-7. [DOI] [PubMed] [Google Scholar]
  74. Smiley J. K., Young M. A., Flint S. J. Intranuclear location of the adenovirus type 5 E1B 55-kilodalton protein. J Virol. 1990 Sep;64(9):4558–4564. doi: 10.1128/jvi.64.9.4558-4564.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Theodorakis N. G., Morimoto R. I. Posttranscriptional regulation of hsp70 expression in human cells: effects of heat shock, inhibition of protein synthesis, and adenovirus infection on translation and mRNA stability. Mol Cell Biol. 1987 Dec;7(12):4357–4368. doi: 10.1128/mcb.7.12.4357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Thimmappaya B., Weinberger C., Schneider R. J., Shenk T. Adenovirus VAI RNA is required for efficient translation of viral mRNAs at late times after infection. Cell. 1982 Dec;31(3 Pt 2):543–551. doi: 10.1016/0092-8674(82)90310-5. [DOI] [PubMed] [Google Scholar]
  77. Weinberg D. H., Ketner G. Adenoviral early region 4 is required for efficient viral DNA replication and for late gene expression. J Virol. 1986 Mar;57(3):833–838. doi: 10.1128/jvi.57.3.833-838.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Wilson M. C., Darnell J. E., Jr Control of messenger RNA concentration by differential cytoplasmic half-life. Adenovirus messenger RNAs from transcription units 1A and 1B. J Mol Biol. 1981 May 25;148(3):231–251. doi: 10.1016/0022-2836(81)90537-4. [DOI] [PubMed] [Google Scholar]
  79. Wolgemuth D. J., Hsu M. T. Visualization of nascent RNA transcripts and simultaneous transcription and replication in viral nucleoprotein complexes from adenovirus 2-infected HeLa cells. J Mol Biol. 1981 Apr 5;147(2):247–268. doi: 10.1016/0022-2836(81)90440-x. [DOI] [PubMed] [Google Scholar]
  80. Wu B. J., Hurst H. C., Jones N. C., Morimoto R. I. The E1A 13S product of adenovirus 5 activates transcription of the cellular human HSP70 gene. Mol Cell Biol. 1986 Aug;6(8):2994–2999. doi: 10.1128/mcb.6.8.2994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Wu B., Hunt C., Morimoto R. Structure and expression of the human gene encoding major heat shock protein HSP70. Mol Cell Biol. 1985 Feb;5(2):330–341. doi: 10.1128/mcb.5.2.330. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Xing Y., Johnson C. V., Dobner P. R., Lawrence J. B. Higher level organization of individual gene transcription and RNA splicing. Science. 1993 Feb 26;259(5099):1326–1330. doi: 10.1126/science.8446901. [DOI] [PubMed] [Google Scholar]
  83. Yoder S. S., Robberson B. L., Leys E. J., Hook A. G., Al-Ubaidi M., Yeung C. Y., Kellems R. E., Berget S. M. Control of cellular gene expression during adenovirus infection: induction and shut-off of dihydrofolate reductase gene expression by adenovirus type 2. Mol Cell Biol. 1983 May;3(5):819–828. doi: 10.1128/mcb.3.5.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Zhang Y., Feigenblum D., Schneider R. J. A late adenovirus factor induces eIF-4E dephosphorylation and inhibition of cell protein synthesis. J Virol. 1994 Nov;68(11):7040–7050. doi: 10.1128/jvi.68.11.7040-7050.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. de la Peña P., Zasloff M. Enhancement of mRNA nuclear transport by promoter elements. Cell. 1987 Aug 14;50(4):613–619. doi: 10.1016/0092-8674(87)90034-1. [DOI] [PubMed] [Google Scholar]

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