Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1996 Sep;70(9):6323–6335. doi: 10.1128/jvi.70.9.6323-6335.1996

Adenovirus early region 4 34-kilodalton protein directs the nuclear localization of the early region 1B 55-kilodalton protein in primate cells.

F D Goodrum 1, T Shenk 1, D A Ornelles 1
PMCID: PMC190658  PMID: 8709260

Abstract

The localization of the adenovirus type 5 34-kDa E4 and 55-kDa E1B proteins was determined in the absence of other adenovirus proteins. When expressed by transfection in human, monkey, hamster, rat, and mouse cell lines, the E1B protein was predominantly cytoplasmic and typically was excluded from the nucleus. When expressed by transfection, the E4 protein accumulated in the nucleus. Strikingly, when coexpressed by transfection in human, monkey, or baby hamster kidney cells, the E1B protein colocalized in the nucleus with the E4 protein. A complex of the E4 and E1B proteins was identified by coimmunoprecipitation in transfected HeLa cells. By contrast to the interaction observed in primate and baby hamster kidney cells, the E4 protein failed to direct the E1B protein to the nucleus in rat and mouse cell lines as well as CHO and V79 hamster cell lines. This failure of the E4 protein to direct the nuclear localization of the E1B protein in REF-52 rat cells was overcome by fusion with HeLa cells. Within 4 h of heterokaryon formation and with protein synthesis inhibited, a portion of the E4 protein present in the REF-52 nuclei migrated to the HeLa nuclei. Simultaneously, the previously cytoplasmic E1B protein colocalized with the E4 protein in both human and rat cell nuclei. These results suggest that a primate cell-specific factor mediates the functional interaction of the E1B and E4 proteins of adenovirus.

Full Text

The Full Text of this article is available as a PDF (1.6 MB).

Selected References

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

  1. Baker S. J., Markowitz S., Fearon E. R., Willson J. K., Vogelstein B. Suppression of human colorectal carcinoma cell growth by wild-type p53. Science. 1990 Aug 24;249(4971):912–915. doi: 10.1126/science.2144057. [DOI] [PubMed] [Google Scholar]
  2. Blair Zajdel M. E., Barker M. D., Dixon S. C., Blair G. E. The use of monoclonal antibodies to study the proteins specified by the transforming region of human adenoviruses. Biochem J. 1985 Feb 1;225(3):649–655. doi: 10.1042/bj2250649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blair G. E., Dixon S. C., Griffiths S. A., Zajdel M. E. Restricted replication of human adenovirus type 5 in mouse cell lines. Virus Res. 1989 Dec;14(4):339–346. doi: 10.1016/0168-1702(89)90026-9. [DOI] [PubMed] [Google Scholar]
  4. Borer R. A., Lehner C. F., Eppenberger H. M., Nigg E. A. Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell. 1989 Feb 10;56(3):379–390. doi: 10.1016/0092-8674(89)90241-9. [DOI] [PubMed] [Google Scholar]
  5. Boulikas T. Nuclear localization signals (NLS). Crit Rev Eukaryot Gene Expr. 1993;3(3):193–227. [PubMed] [Google Scholar]
  6. Bours V., Villalobos J., Burd P. R., Kelly K., Siebenlist U. Cloning of a mitogen-inducible gene encoding a kappa B DNA-binding protein with homology to the rel oncogene and to cell-cycle motifs. Nature. 1990 Nov 1;348(6296):76–80. doi: 10.1038/348076a0. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Bridge E., Ketner G. Redundant control of adenovirus late gene expression by early region 4. J Virol. 1989 Feb;63(2):631–638. doi: 10.1128/jvi.63.2.631-638.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bridge E., Medghalchi S., Ubol S., Leesong M., Ketner G. Adenovirus early region 4 and viral DNA synthesis. Virology. 1993 Apr;193(2):794–801. doi: 10.1006/viro.1993.1188. [DOI] [PubMed] [Google Scholar]
  10. Brigati D. J., Myerson D., Leary J. J., Spalholz B., Travis S. Z., Fong C. K., Hsiung G. D., Ward D. C. Detection of viral genomes in cultured cells and paraffin-embedded tissue sections using biotin-labeled hybridization probes. Virology. 1983 Apr 15;126(1):32–50. doi: 10.1016/0042-6822(83)90460-9. [DOI] [PubMed] [Google Scholar]
  11. Brown C. R., Doxsey S. J., White E., Welch W. J. Both viral (adenovirus E1B) and cellular (hsp 70, p53) components interact with centrosomes. J Cell Physiol. 1994 Jul;160(1):47–60. doi: 10.1002/jcp.1041600107. [DOI] [PubMed] [Google Scholar]
  12. Buchou T., Kranenburg O., van Dam H., Roelen D., Zantema A., Hall F. L., van der Eb A. Increased cyclin A and decreased cyclin D levels in adenovirus 5 E1A-transformed rodent cell lines. Oncogene. 1993 Jul;8(7):1765–1773. [PubMed] [Google Scholar]
  13. 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]
  14. Davidson R. L., Gerald P. S. Improved techniques for the induction of mammalian cell hybridization by polyethylene glycol. Somatic Cell Genet. 1976 Mar;2(2):165–176. doi: 10.1007/BF01542629. [DOI] [PubMed] [Google Scholar]
  15. Doerfler W. Nonproductive infection of baby hamster kidney cells (BHK21) with adenovirus type 12. Virology. 1969 Aug;38(4):587–606. doi: 10.1016/0042-6822(69)90179-2. [DOI] [PubMed] [Google Scholar]
  16. Doucas V., Ishov A. M., Romo A., Juguilon H., Weitzman M. D., Evans R. M., Maul G. G. Adenovirus replication is coupled with the dynamic properties of the PML nuclear structure. Genes Dev. 1996 Jan 15;10(2):196–207. doi: 10.1101/gad.10.2.196. [DOI] [PubMed] [Google Scholar]
  17. Eggerding F. A., Pierce W. C. Molecular biology of adenovirus type 2 semipermissive infections. I. Viral growth and expression of viral replicative functions during restricted adenovirus infection. Virology. 1986 Jan 15;148(1):97–113. doi: 10.1016/0042-6822(86)90406-x. [DOI] [PubMed] [Google Scholar]
  18. Elkind N. B., Goldfinger N., Rotter V. Spot-1, a novel NLS-binding protein that interacts with p53 through a domain encoded by p(CA)n repeats. Oncogene. 1995 Sep 7;11(5):841–851. [PubMed] [Google Scholar]
  19. Franza B. R., Jr, Maruyama K., Garrels J. I., Ruley H. E. In vitro establishment is not a sufficient prerequisite for transformation by activated ras oncogenes. Cell. 1986 Feb 14;44(3):409–418. doi: 10.1016/0092-8674(86)90462-9. [DOI] [PubMed] [Google Scholar]
  20. Friedman M. P., Lyons M. J., Ginsberg H. S. Biochemical consequences of type 2 adenovirus and Simian virus 40 double infections of African green monkey kidney cells. J Virol. 1970 May;5(5):586–597. doi: 10.1128/jvi.5.5.586-597.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Fuerst T. R., Niles E. G., Studier F. W., Moss B. Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc Natl Acad Sci U S A. 1986 Nov;83(21):8122–8126. doi: 10.1073/pnas.83.21.8122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. GOLDSTEIN L. Localization of nucleusspecific protein as shown by transplantation experiments in Amoeba proteus. Exp Cell Res. 1958 Dec;15(3):635–637. doi: 10.1016/0014-4827(58)90118-6. [DOI] [PubMed] [Google Scholar]
  23. Ganchi P. A., Sun S. C., Greene W. C., Ballard D. W. I kappa B/MAD-3 masks the nuclear localization signal of NF-kappa B p65 and requires the transactivation domain to inhibit NF-kappa B p65 DNA binding. Mol Biol Cell. 1992 Dec;3(12):1339–1352. doi: 10.1091/mbc.3.12.1339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gluzman Y. SV40-transformed simian cells support the replication of early SV40 mutants. Cell. 1981 Jan;23(1):175–182. doi: 10.1016/0092-8674(81)90282-8. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Grand R. J., Grant M. L., Gallimore P. H. Enhanced expression of p53 in human cells infected with mutant adenoviruses. Virology. 1994 Sep;203(2):229–240. doi: 10.1006/viro.1994.1480. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Hightower M. J., Fairfield F. R., Lucas J. J. A staining procedure for identifying viable cell hybrids constructed by somatic cell fusion, cybridization, or nuclear transplantation. Somatic Cell Genet. 1981 May;7(3):321–329. doi: 10.1007/BF01538857. [DOI] [PubMed] [Google Scholar]
  29. Huang M. M., Hearing P. Adenovirus early region 4 encodes two gene products with redundant effects in lytic infection. J Virol. 1989 Jun;63(6):2605–2615. doi: 10.1128/jvi.63.6.2605-2615.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Jones N., Shenk T. Isolation of adenovirus type 5 host range deletion mutants defective for transformation of rat embryo cells. Cell. 1979 Jul;17(3):683–689. doi: 10.1016/0092-8674(79)90275-7. [DOI] [PubMed] [Google Scholar]
  31. Jones N., Shenk T. Isolation of deletion and substitution mutants of adenovirus type 5. Cell. 1978 Jan;13(1):181–188. doi: 10.1016/0092-8674(78)90148-4. [DOI] [PubMed] [Google Scholar]
  32. Kalland K. H., Szilvay A. M., Brokstad K. A., Saetrevik W., Haukenes G. The human immunodeficiency virus type 1 Rev protein shuttles between the cytoplasm and nuclear compartments. Mol Cell Biol. 1994 Nov;14(11):7436–7444. doi: 10.1128/mcb.14.11.7436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kang K. I., Devin J., Cadepond F., Jibard N., Guiochon-Mantel A., Baulieu E. E., Catelli M. G. In vivo functional protein-protein interaction: nuclear targeted hsp90 shifts cytoplasmic steroid receptor mutants into the nucleus. Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):340–344. doi: 10.1073/pnas.91.1.340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Katz D. A., Theodorakis N. G., Cleveland D. W., Lindsten T., Thompson C. B. AU-A, an RNA-binding activity distinct from hnRNP A1, is selective for AUUUA repeats and shuttles between the nucleus and the cytoplasm. Nucleic Acids Res. 1994 Jan 25;22(2):238–246. doi: 10.1093/nar/22.2.238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Klessig D. F., Anderson C. W. Block to multiplication of adenovirus serotype 2 in monkey cells. J Virol. 1975 Dec;16(6):1650–1668. doi: 10.1128/jvi.16.6.1650-1668.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Knipe D. M., Smith J. L. A mutant herpesvirus protein leads to a block in nuclear localization of other viral proteins. Mol Cell Biol. 1986 Jul;6(7):2371–2381. doi: 10.1128/mcb.6.7.2371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Laskey R. A., Mills A. D. Quantitative film detection of 3H and 14C in polyacrylamide gels by fluorography. Eur J Biochem. 1975 Aug 15;56(2):335–341. doi: 10.1111/j.1432-1033.1975.tb02238.x. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. 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]
  40. Liang S., Hitomi M., Tartakoff A. M. Adenoviral E1B-55kDa protein inhibits yeast mRNA export and perturbs nuclear structure. Proc Natl Acad Sci U S A. 1995 Aug 1;92(16):7372–7375. doi: 10.1073/pnas.92.16.7372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Marton M. J., Baim S. B., Ornelles D. A., Shenk T. The adenovirus E4 17-kilodalton protein complexes with the cellular transcription factor E2F, altering its DNA-binding properties and stimulating E1A-independent accumulation of E2 mRNA. J Virol. 1990 May;64(5):2345–2359. doi: 10.1128/jvi.64.5.2345-2359.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Meier U. T., Blobel G. Nopp140 shuttles on tracks between nucleolus and cytoplasm. Cell. 1992 Jul 10;70(1):127–138. doi: 10.1016/0092-8674(92)90539-o. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. Mullen M. A., Gerstberger S., Ciufo D. M., Mosca J. D., Hayward G. S. Evaluation of colocalization interactions between the IE110, IE175, and IE63 transactivator proteins of herpes simplex virus within subcellular punctate structures. J Virol. 1995 Jan;69(1):476–491. doi: 10.1128/jvi.69.1.476-491.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Nakayasu H., Berezney R. Nuclear matrins: identification of the major nuclear matrix proteins. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10312–10316. doi: 10.1073/pnas.88.22.10312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Newmeyer D. D., Forbes D. J. Nuclear import can be separated into distinct steps in vitro: nuclear pore binding and translocation. Cell. 1988 Mar 11;52(5):641–653. doi: 10.1016/0092-8674(88)90402-3. [DOI] [PubMed] [Google Scholar]
  47. Newmeyer D. D. The nuclear pore complex and nucleocytoplasmic transport. Curr Opin Cell Biol. 1993 Jun;5(3):395–407. doi: 10.1016/0955-0674(93)90003-9. [DOI] [PubMed] [Google Scholar]
  48. Nieto A., de la Luna S., Bárcena J., Portela A., Valcárcel J., Melero J. A., Ortín J. Nuclear transport of influenza virus polymerase PA protein. Virus Res. 1992 Jun;24(1):65–75. doi: 10.1016/0168-1702(92)90031-4. [DOI] [PubMed] [Google Scholar]
  49. 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]
  50. Parnaik V. K., Kennady P. K. Nuclear transport of proteins translated in vitro from SP6 plasmid-generated mRNAs. Mol Cell Biol. 1990 Mar;10(3):1287–1292. doi: 10.1128/mcb.10.3.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. 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]
  52. Pines J., Hunter T. Human cyclins A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport. J Cell Biol. 1991 Oct;115(1):1–17. doi: 10.1083/jcb.115.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Pines J., Hunter T. The differential localization of human cyclins A and B is due to a cytoplasmic retention signal in cyclin B. EMBO J. 1994 Aug 15;13(16):3772–3781. doi: 10.1002/j.1460-2075.1994.tb06688.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Piñol-Roma S., Dreyfuss G. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature. 1992 Feb 20;355(6362):730–732. doi: 10.1038/355730a0. [DOI] [PubMed] [Google Scholar]
  55. Radna R. L., Foellmer B., Feldman L. A., Francke U., Ozer H. L. Restriction of human adenovirus replication in Chinese hamster cell lines and their hybrids with human cells. Virus Res. 1987 Nov;8(4):277–299. doi: 10.1016/0168-1702(87)90001-3. [DOI] [PubMed] [Google Scholar]
  56. Ross S. R., Levine A. J., Galos R. S., Williams J., Shenk T. Early viral proteins in HeLa cells infected with adenovirus type 5 host range mutants. Virology. 1980 Jun;103(2):475–492. doi: 10.1016/0042-6822(80)90205-6. [DOI] [PubMed] [Google Scholar]
  57. Rowe D. T., Graham F. L. Complementation of adenovirus type 5 host range mutants by adenovirus type 12 in coinfected HeLa and BHK-21 cells. J Virol. 1981 Apr;38(1):191–197. doi: 10.1128/jvi.38.1.191-197.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Sandler A. B., Ketner G. Adenovirus early region 4 is essential for normal stability of late nuclear RNAs. J Virol. 1989 Feb;63(2):624–630. doi: 10.1128/jvi.63.2.624-630.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Sandler A. B., Ketner G. The metabolism of host RNAs in cells infected by an adenovirus E4 mutant. Virology. 1991 Mar;181(1):319–326. doi: 10.1016/0042-6822(91)90498-z. [DOI] [PubMed] [Google Scholar]
  60. 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]
  61. Sarnow P., Sullivan C. A., Levine A. J. A monoclonal antibody detecting the adenovirus type 5-E1b-58Kd tumor antigen: characterization of the E1b-58Kd tumor antigen in adenovirus-infected and -transformed cells. Virology. 1982 Jul 30;120(2):510–517. doi: 10.1016/0042-6822(82)90054-x. [DOI] [PubMed] [Google Scholar]
  62. Schmidt-Zachmann M. S., Dargemont C., Kühn L. C., Nigg E. A. Nuclear export of proteins: the role of nuclear retention. Cell. 1993 Aug 13;74(3):493–504. doi: 10.1016/0092-8674(93)80051-f. [DOI] [PubMed] [Google Scholar]
  63. Silverstein G., Strohl W. A. Restricted replication of adenovirus type 2 in mouse Balb/3T3 cells. Arch Virol. 1986;87(3-4):241–264. doi: 10.1007/BF01315303. [DOI] [PubMed] [Google Scholar]
  64. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Trono D., Baltimore D. A human cell factor is essential for HIV-1 Rev action. EMBO J. 1990 Dec;9(12):4155–4160. doi: 10.1002/j.1460-2075.1990.tb07638.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. White E., Spector D., Welch W. Differential distribution of the adenovirus E1A proteins and colocalization of E1A with the 70-kilodalton cellular heat shock protein in infected cells. J Virol. 1988 Nov;62(11):4153–4166. doi: 10.1128/jvi.62.11.4153-4166.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Winslow B. J., Trono D. The blocks to human immunodeficiency virus type 1 Tat and Rev functions in mouse cell lines are independent. J Virol. 1993 Apr;67(4):2349–2354. doi: 10.1128/jvi.67.4.2349-2354.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Wolff B., Cohen G., Hauber J., Meshcheryakova D., Rabeck C. Nucleocytoplasmic transport of the Rev protein of human immunodeficiency virus type 1 is dependent on the activation domain of the protein. Exp Cell Res. 1995 Mar;217(1):31–41. doi: 10.1006/excr.1995.1060. [DOI] [PubMed] [Google Scholar]
  69. Yang J., DeFranco D. B. Differential roles of heat shock protein 70 in the in vitro nuclear import of glucocorticoid receptor and simian virus 40 large tumor antigen. Mol Cell Biol. 1994 Aug;14(8):5088–5098. doi: 10.1128/mcb.14.8.5088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Zantema A., Fransen J. A., Davis-Olivier A., Ramaekers F. C., Vooijs G. P., DeLeys B., Van der Eb A. J. Localization of the E1B proteins of adenovirus 5 in transformed cells, as revealed by interaction with monoclonal antibodies. Virology. 1985 Apr 15;142(1):44–58. doi: 10.1016/0042-6822(85)90421-0. [DOI] [PubMed] [Google Scholar]
  71. Zantema A., Schrier P. I., Davis-Olivier A., van Laar T., Vaessen R. T., van der EB A. J. Adenovirus serotype determines association and localization of the large E1B tumor antigen with cellular tumor antigen p53 in transformed cells. Mol Cell Biol. 1985 Nov;5(11):3084–3091. doi: 10.1128/mcb.5.11.3084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Zhao L. J., Padmanabhan R. Nuclear transport of adenovirus DNA polymerase is facilitated by interaction with preterminal protein. Cell. 1988 Dec 23;55(6):1005–1015. doi: 10.1016/0092-8674(88)90245-0. [DOI] [PubMed] [Google Scholar]
  73. Zhu Z., Cai W., Schaffer P. A. Cooperativity among herpes simplex virus type 1 immediate-early regulatory proteins: ICP4 and ICP27 affect the intracellular localization of ICP0. J Virol. 1994 May;68(5):3027–3040. doi: 10.1128/jvi.68.5.3027-3040.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Zhu Z., Schaffer P. A. Intracellular localization of the herpes simplex virus type 1 major transcriptional regulatory protein, ICP4, is affected by ICP27. J Virol. 1995 Jan;69(1):49–59. doi: 10.1128/jvi.69.1.49-59.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Zucker M. L., Flint S. J. Infection and transformation of mouse cells by human adenovirus type 2. Virology. 1985 Nov;147(1):126–141. doi: 10.1016/0042-6822(85)90233-8. [DOI] [PubMed] [Google Scholar]
  76. van den Heuvel S. J., van Laar T., Kast W. M., Melief C. J., Zantema A., van der Eb A. J. Association between the cellular p53 and the adenovirus 5 E1B-55kd proteins reduces the oncogenicity of Ad-transformed cells. EMBO J. 1990 Aug;9(8):2621–2629. doi: 10.1002/j.1460-2075.1990.tb07444.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES