Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1997 Sep;17(9):5077–5086. doi: 10.1128/mcb.17.9.5077

RRB1 and RRB2 encode maize retinoblastoma-related proteins that interact with a plant D-type cyclin and geminivirus replication protein.

R A Ach 1, T Durfee 1, A B Miller 1, P Taranto 1, L Hanley-Bowdoin 1, P C Zambryski 1, W Gruissem 1
PMCID: PMC232358  PMID: 9271385

Abstract

Unlike mammalian and yeast cells, little is known about how plants regulate G1 progression and entry into the S phase of the cell cycle. In mammalian cells, a key regulator of this process is the retinoblastoma tumor suppressor protein (RB). In contrast, G1 control in Saccharomyces cerevisiae does not utilize an RB-like protein. We report here the cloning of cDNAs from two Zea mays genes, RRB1 and RRB2, that encode RB-related proteins. Further, RRB2 transcripts are alternatively spliced to yield two proteins with different C termini. At least one RRB gene is expressed in all the tissues examined, with the highest levels seen in the shoot apex. RRB1 is a 96-kDa nuclear protein that can physically interact with two mammalian DNA tumor virus oncoproteins, simian virus 40 large-T antigen and adenovirus E1A, and with a plant D-type cyclin. These associations are abolished by mutation of a conserved cysteine residue in RRB1 that is also essential for RB function. RRB1 binding potential is also sensitive to deletions in the conserved A and B domains, although differences exist in these effects compared to those of human RB. RRB1 can also bind to the AL1 protein from tomato golden mosaic virus (TGMV), a protein which is essential for TGMV DNA replication. These results suggest that G1 regulation in plant cells is controlled by a mechanism which is much more similar to that found in mammalian cells than that in yeast.

Full Text

The Full Text of this article is available as a PDF (1.5 MB).

Selected References

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

  1. Ach R. A., Gruissem W. A small nuclear GTP-binding protein from tomato suppresses a Schizosaccharomyces pombe cell-cycle mutant. Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):5863–5867. doi: 10.1073/pnas.91.13.5863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barkan A., Miles D., Taylor W. C. Chloroplast gene expression in nuclear, photosynthetic mutants of maize. EMBO J. 1986 Jul;5(7):1421–1427. doi: 10.1002/j.1460-2075.1986.tb04378.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bernards R., Shackleford G. M., Schackleford G. M., Gerber M. R., Horowitz J. M., Friend S. H., Schartl M., Bogenmann E., Rapaport J. M., McGee T. Structure and expression of the murine retinoblastoma gene and characterization of its encoded protein. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6474–6478. doi: 10.1073/pnas.86.17.6474. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bignon Y. J., Shew J. Y., Rappolee D., Naylor S. L., Lee E. Y., Schnier J., Lee W. H. A single Cys706 to Phe substitution in the retinoblastoma protein causes the loss of binding to SV40 T antigen. Cell Growth Differ. 1990 Dec;1(12):647–651. [PubMed] [Google Scholar]
  5. Chellappan S., Kraus V. B., Kroger B., Munger K., Howley P. M., Phelps W. C., Nevins J. R. Adenovirus E1A, simian virus 40 tumor antigen, and human papillomavirus E7 protein share the capacity to disrupt the interaction between transcription factor E2F and the retinoblastoma gene product. Proc Natl Acad Sci U S A. 1992 May 15;89(10):4549–4553. doi: 10.1073/pnas.89.10.4549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chen P. L., Riley D. J., Lee W. H. The retinoblastoma protein as a fundamental mediator of growth and differentiation signals. Crit Rev Eukaryot Gene Expr. 1995;5(1):79–95. [PubMed] [Google Scholar]
  7. Clarke A. R., Maandag E. R., van Roon M., van der Lugt N. M., van der Valk M., Hooper M. L., Berns A., te Riele H. Requirement for a functional Rb-1 gene in murine development. Nature. 1992 Sep 24;359(6393):328–330. doi: 10.1038/359328a0. [DOI] [PubMed] [Google Scholar]
  8. Collin S., Fernández-Lobato M., Gooding P. S., Mullineaux P. M., Fenoll C. The two nonstructural proteins from wheat dwarf virus involved in viral gene expression and replication are retinoblastoma-binding proteins. Virology. 1996 May 1;219(1):324–329. doi: 10.1006/viro.1996.0256. [DOI] [PubMed] [Google Scholar]
  9. Dahl M., Meskiene I., Bögre L., Ha D. T., Swoboda I., Hubmann R., Hirt H., Heberle-Bors E. The D-type alfalfa cyclin gene cycMs4 complements G1 cyclin-deficient yeast and is induced in the G1 phase of the cell cycle. Plant Cell. 1995 Nov;7(11):1847–1857. doi: 10.1105/tpc.7.11.1847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. DeGregori J., Kowalik T., Nevins J. R. Cellular targets for activation by the E2F1 transcription factor include DNA synthesis- and G1/S-regulatory genes. Mol Cell Biol. 1995 Aug;15(8):4215–4224. doi: 10.1128/mcb.15.8.4215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dirick L., Böhm T., Nasmyth K. Roles and regulation of Cln-Cdc28 kinases at the start of the cell cycle of Saccharomyces cerevisiae. EMBO J. 1995 Oct 2;14(19):4803–4813. doi: 10.1002/j.1460-2075.1995.tb00162.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Doerner P. W. Cell Cycle Regulation in Plants. Plant Physiol. 1994 Nov;106(3):823–827. doi: 10.1104/pp.106.3.823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Doerner P., Jørgensen J. E., You R., Steppuhn J., Lamb C. Control of root growth and development by cyclin expression. Nature. 1996 Apr 11;380(6574):520–523. doi: 10.1038/380520a0. [DOI] [PubMed] [Google Scholar]
  14. Doonan J., Hunt T. Cell cycle. Why don't plants get cancer? Nature. 1996 Apr 11;380(6574):481–482. doi: 10.1038/380481a0. [DOI] [PubMed] [Google Scholar]
  15. Dowdy S. F., Hinds P. W., Louie K., Reed S. I., Arnold A., Weinberg R. A. Physical interaction of the retinoblastoma protein with human D cyclins. Cell. 1993 May 7;73(3):499–511. doi: 10.1016/0092-8674(93)90137-f. [DOI] [PubMed] [Google Scholar]
  16. Du W., Vidal M., Xie J. E., Dyson N. RBF, a novel RB-related gene that regulates E2F activity and interacts with cyclin E in Drosophila. Genes Dev. 1996 May 15;10(10):1206–1218. doi: 10.1101/gad.10.10.1206. [DOI] [PubMed] [Google Scholar]
  17. Durfee T., Becherer K., Chen P. L., Yeh S. H., Yang Y., Kilburn A. E., Lee W. H., Elledge S. J. The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev. 1993 Apr;7(4):555–569. doi: 10.1101/gad.7.4.555. [DOI] [PubMed] [Google Scholar]
  18. Durfee T., Mancini M. A., Jones D., Elledge S. J., Lee W. H. The amino-terminal region of the retinoblastoma gene product binds a novel nuclear matrix protein that co-localizes to centers for RNA processing. J Cell Biol. 1994 Nov;127(3):609–622. doi: 10.1083/jcb.127.3.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Elmer J. S., Brand L., Sunter G., Gardiner W. E., Bisaro D. M., Rogers S. G. Genetic analysis of the tomato golden mosaic virus. II. The product of the AL1 coding sequence is required for replication. Nucleic Acids Res. 1988 Jul 25;16(14B):7043–7060. doi: 10.1093/nar/16.14.7043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ewen M. E., Sluss H. K., Sherr C. J., Matsushime H., Kato J., Livingston D. M. Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell. 1993 May 7;73(3):487–497. doi: 10.1016/0092-8674(93)90136-e. [DOI] [PubMed] [Google Scholar]
  21. Ewen M. E., Xing Y. G., Lawrence J. B., Livingston D. M. Molecular cloning, chromosomal mapping, and expression of the cDNA for p107, a retinoblastoma gene product-related protein. Cell. 1991 Sep 20;66(6):1155–1164. doi: 10.1016/0092-8674(91)90038-z. [DOI] [PubMed] [Google Scholar]
  22. Figge J., Webster T., Smith T. F., Paucha E. Prediction of similar transforming regions in simian virus 40 large T, adenovirus E1A, and myc oncoproteins. J Virol. 1988 May;62(5):1814–1818. doi: 10.1128/jvi.62.5.1814-1818.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Goodrich D. W., Wang N. P., Qian Y. W., Lee E. Y., Lee W. H. The retinoblastoma gene product regulates progression through the G1 phase of the cell cycle. Cell. 1991 Oct 18;67(2):293–302. doi: 10.1016/0092-8674(91)90181-w. [DOI] [PubMed] [Google Scholar]
  24. Grafi G., Burnett R. J., Helentjaris T., Larkins B. A., DeCaprio J. A., Sellers W. R., Kaelin W. G., Jr A maize cDNA encoding a member of the retinoblastoma protein family: involvement in endoreduplication. Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):8962–8967. doi: 10.1073/pnas.93.17.8962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gu W., Schneider J. W., Condorelli G., Kaushal S., Mahdavi V., Nadal-Ginard B. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell. 1993 Feb 12;72(3):309–324. doi: 10.1016/0092-8674(93)90110-c. [DOI] [PubMed] [Google Scholar]
  26. Hanley-Bowdoin L., Elmer J. S., Rogers S. G. Expression of functional replication protein from tomato golden mosaic virus in transgenic tobacco plants. Proc Natl Acad Sci U S A. 1990 Feb;87(4):1446–1450. doi: 10.1073/pnas.87.4.1446. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hannon G. J., Demetrick D., Beach D. Isolation of the Rb-related p130 through its interaction with CDK2 and cyclins. Genes Dev. 1993 Dec;7(12A):2378–2391. doi: 10.1101/gad.7.12a.2378. [DOI] [PubMed] [Google Scholar]
  28. Hemerly A., Bergounioux C., Van Montagu M., Inzé D., Ferreira P. Genes regulating the plant cell cycle: isolation of a mitotic-like cyclin from Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3295–3299. doi: 10.1073/pnas.89.8.3295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hemerly A., Engler J. de A., Bergounioux C., Van Montagu M., Engler G., Inzé D., Ferreira P. Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development. EMBO J. 1995 Aug 15;14(16):3925–3936. doi: 10.1002/j.1460-2075.1995.tb00064.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hiebert S. W., Chellappan S. P., Horowitz J. M., Nevins J. R. The interaction of RB with E2F coincides with an inhibition of the transcriptional activity of E2F. Genes Dev. 1992 Feb;6(2):177–185. doi: 10.1101/gad.6.2.177. [DOI] [PubMed] [Google Scholar]
  31. Hinds P. W., Mittnacht S., Dulic V., Arnold A., Reed S. I., Weinberg R. A. Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell. 1992 Sep 18;70(6):993–1006. doi: 10.1016/0092-8674(92)90249-c. [DOI] [PubMed] [Google Scholar]
  32. Howard E. A., Zupan J. R., Citovsky V., Zambryski P. C. The VirD2 protein of A. tumefaciens contains a C-terminal bipartite nuclear localization signal: implications for nuclear uptake of DNA in plant cells. Cell. 1992 Jan 10;68(1):109–118. doi: 10.1016/0092-8674(92)90210-4. [DOI] [PubMed] [Google Scholar]
  33. Hu Q. J., Dyson N., Harlow E. The regions of the retinoblastoma protein needed for binding to adenovirus E1A or SV40 large T antigen are common sites for mutations. EMBO J. 1990 Apr;9(4):1147–1155. doi: 10.1002/j.1460-2075.1990.tb08221.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Huang S., Wang N. P., Tseng B. Y., Lee W. H., Lee E. H. Two distinct and frequently mutated regions of retinoblastoma protein are required for binding to SV40 T antigen. EMBO J. 1990 Jun;9(6):1815–1822. doi: 10.1002/j.1460-2075.1990.tb08306.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Jacks T., Fazeli A., Schmitt E. M., Bronson R. T., Goodell M. A., Weinberg R. A. Effects of an Rb mutation in the mouse. Nature. 1992 Sep 24;359(6393):295–300. doi: 10.1038/359295a0. [DOI] [PubMed] [Google Scholar]
  36. Kaelin W. G., Jr, Ewen M. E., Livingston D. M. Definition of the minimal simian virus 40 large T antigen- and adenovirus E1A-binding domain in the retinoblastoma gene product. Mol Cell Biol. 1990 Jul;10(7):3761–3769. doi: 10.1128/mcb.10.7.3761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kato J., Matsushime H., Hiebert S. W., Ewen M. E., Sherr C. J. Direct binding of cyclin D to the retinoblastoma gene product (pRb) and pRb phosphorylation by the cyclin D-dependent kinase CDK4. Genes Dev. 1993 Mar;7(3):331–342. doi: 10.1101/gad.7.3.331. [DOI] [PubMed] [Google Scholar]
  38. Kaye F. J., Kratzke R. A., Gerster J. L., Horowitz J. M. A single amino acid substitution results in a retinoblastoma protein defective in phosphorylation and oncoprotein binding. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6922–6926. doi: 10.1073/pnas.87.17.6922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Koch C., Schleiffer A., Ammerer G., Nasmyth K. Switching transcription on and off during the yeast cell cycle: Cln/Cdc28 kinases activate bound transcription factor SBF (Swi4/Swi6) at start, whereas Clb/Cdc28 kinases displace it from the promoter in G2. Genes Dev. 1996 Jan 15;10(2):129–141. doi: 10.1101/gad.10.2.129. [DOI] [PubMed] [Google Scholar]
  40. Lam E. W., La Thangue N. B. DP and E2F proteins: coordinating transcription with cell cycle progression. Curr Opin Cell Biol. 1994 Dec;6(6):859–866. doi: 10.1016/0955-0674(94)90057-4. [DOI] [PubMed] [Google Scholar]
  41. Lee E. Y., Chang C. Y., Hu N., Wang Y. C., Lai C. C., Herrup K., Lee W. H., Bradley A. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature. 1992 Sep 24;359(6393):288–294. doi: 10.1038/359288a0. [DOI] [PubMed] [Google Scholar]
  42. Luckow V. A., Lee S. C., Barry G. F., Olins P. O. Efficient generation of infectious recombinant baculoviruses by site-specific transposon-mediated insertion of foreign genes into a baculovirus genome propagated in Escherichia coli. J Virol. 1993 Aug;67(8):4566–4579. doi: 10.1128/jvi.67.8.4566-4579.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Ludlow J. W., Skuse G. R. Viral oncoprotein binding to pRB, p107, p130, and p300. Virus Res. 1995 Feb;35(2):113–121. doi: 10.1016/0168-1702(94)00094-s. [DOI] [PubMed] [Google Scholar]
  44. Matsuoka S., Edwards M. C., Bai C., Parker S., Zhang P., Baldini A., Harper J. W., Elledge S. J. p57KIP2, a structurally distinct member of the p21CIP1 Cdk inhibitor family, is a candidate tumor suppressor gene. Genes Dev. 1995 Mar 15;9(6):650–662. doi: 10.1101/gad.9.6.650. [DOI] [PubMed] [Google Scholar]
  45. McLean B. G., Zupan J., Zambryski P. C. Tobacco mosaic virus movement protein associates with the cytoskeleton in tobacco cells. Plant Cell. 1995 Dec;7(12):2101–2114. doi: 10.1105/tpc.7.12.2101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Nagar S., Pedersen T. J., Carrick K. M., Hanley-Bowdoin L., Robertson D. A geminivirus induces expression of a host DNA synthesis protein in terminally differentiated plant cells. Plant Cell. 1995 Jun;7(6):705–719. doi: 10.1105/tpc.7.6.705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Narita J. O., Gruissem W. Tomato hydroxymethylglutaryl-CoA reductase is required early in fruit development but not during ripening. Plant Cell. 1989 Feb;1(2):181–190. doi: 10.1105/tpc.1.2.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Nasmyth K. Control of the yeast cell cycle by the Cdc28 protein kinase. Curr Opin Cell Biol. 1993 Apr;5(2):166–179. doi: 10.1016/0955-0674(93)90099-c. [DOI] [PubMed] [Google Scholar]
  49. Nevins J. R. E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science. 1992 Oct 16;258(5081):424–429. doi: 10.1126/science.1411535. [DOI] [PubMed] [Google Scholar]
  50. Orozco B. M., Hanley-Bowdoin L. A DNA structure is required for geminivirus replication origin function. J Virol. 1996 Jan;70(1):148–158. doi: 10.1128/jvi.70.1.148-158.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Qian Y., Luckey C., Horton L., Esser M., Templeton D. J. Biological function of the retinoblastoma protein requires distinct domains for hyperphosphorylation and transcription factor binding. Mol Cell Biol. 1992 Dec;12(12):5363–5372. doi: 10.1128/mcb.12.12.5363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Qin X. Q., Chittenden T., Livingston D. M., Kaelin W. G., Jr Identification of a growth suppression domain within the retinoblastoma gene product. Genes Dev. 1992 Jun;6(6):953–964. doi: 10.1101/gad.6.6.953. [DOI] [PubMed] [Google Scholar]
  53. STEWARD F. C., MAPES M. O., KENT A. E., HOLSTEN R. D. GROWTH AND DEVELOPMENT OF CULTURED PLANT CELLS. Science. 1964 Jan 3;143(3601):20–27. doi: 10.1126/science.143.3601.20. [DOI] [PubMed] [Google Scholar]
  54. Saunders K., Lucy A., Stanley J. DNA forms of the geminivirus African cassava mosaic virus consistent with a rolling circle mechanism of replication. Nucleic Acids Res. 1991 May 11;19(9):2325–2330. doi: 10.1093/nar/19.9.2325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Schiestl R. H., Gietz R. D. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr Genet. 1989 Dec;16(5-6):339–346. doi: 10.1007/BF00340712. [DOI] [PubMed] [Google Scholar]
  56. Schneider J. W., Gu W., Zhu L., Mahdavi V., Nadal-Ginard B. Reversal of terminal differentiation mediated by p107 in Rb-/- muscle cells. Science. 1994 Jun 3;264(5164):1467–1471. doi: 10.1126/science.8197461. [DOI] [PubMed] [Google Scholar]
  57. Settlage S. B., Miller A. B., Hanley-Bowdoin L. Interactions between geminivirus replication proteins. J Virol. 1996 Oct;70(10):6790–6795. doi: 10.1128/jvi.70.10.6790-6795.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Shan B., Durfee T., Lee W. H. Disruption of RB/E2F-1 interaction by single point mutations in E2F-1 enhances S-phase entry and apoptosis. Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):679–684. doi: 10.1073/pnas.93.2.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Shen B., Carneiro N., Torres-Jerez I., Stevenson B., McCreery T., Helentjaris T., Baysdorfer C., Almira E., Ferl R. J., Habben J. E. Partial sequencing and mapping of clones from two maize cDNA libraries. Plant Mol Biol. 1994 Nov;26(4):1085–1101. doi: 10.1007/BF00040691. [DOI] [PubMed] [Google Scholar]
  60. Sherr C. J. G1 phase progression: cycling on cue. Cell. 1994 Nov 18;79(4):551–555. doi: 10.1016/0092-8674(94)90540-1. [DOI] [PubMed] [Google Scholar]
  61. Soni R., Carmichael J. P., Shah Z. H., Murray J. A. A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell. 1995 Jan;7(1):85–103. doi: 10.1105/tpc.7.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Stenger D. C., Revington G. N., Stevenson M. C., Bisaro D. M. Replicational release of geminivirus genomes from tandemly repeated copies: evidence for rolling-circle replication of a plant viral DNA. Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):8029–8033. doi: 10.1073/pnas.88.18.8029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Sterner J. M., Murata Y., Kim H. G., Kennett S. B., Templeton D. J., Horowitz J. M. Detection of a novel cell cycle-regulated kinase activity that associates with the amino terminus of the retinoblastoma protein in G2/M phases. J Biol Chem. 1995 Apr 21;270(16):9281–9288. doi: 10.1074/jbc.270.16.9281. [DOI] [PubMed] [Google Scholar]
  64. Steward F. C. From cultured cells to whole plants: the induction and control of their growth and morphogenesis. Proc R Soc Lond B Biol Sci. 1970 Feb 17;175(1038):1–30. doi: 10.1098/rspb.1970.0009. [DOI] [PubMed] [Google Scholar]
  65. Sunter G., Hartitz M. D., Hormuzdi S. G., Brough C. L., Bisaro D. M. Genetic analysis of tomato golden mosaic virus: ORF AL2 is required for coat protein accumulation while ORF AL3 is necessary for efficient DNA replication. Virology. 1990 Nov;179(1):69–77. doi: 10.1016/0042-6822(90)90275-v. [DOI] [PubMed] [Google Scholar]
  66. Weinberg R. A. The retinoblastoma protein and cell cycle control. Cell. 1995 May 5;81(3):323–330. doi: 10.1016/0092-8674(95)90385-2. [DOI] [PubMed] [Google Scholar]
  67. Xie Q., Sanz-Burgos A. P., Hannon G. J., Gutiérrez C. Plant cells contain a novel member of the retinoblastoma family of growth regulatory proteins. EMBO J. 1996 Sep 16;15(18):4900–4908. [PMC free article] [PubMed] [Google Scholar]
  68. Xie Q., Suárez-López P., Gutiérrez C. Identification and analysis of a retinoblastoma binding motif in the replication protein of a plant DNA virus: requirement for efficient viral DNA replication. EMBO J. 1995 Aug 15;14(16):4073–4082. doi: 10.1002/j.1460-2075.1995.tb00079.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Zamanian M., La Thangue N. B. Adenovirus E1a prevents the retinoblastoma gene product from repressing the activity of a cellular transcription factor. EMBO J. 1992 Jul;11(7):2603–2610. doi: 10.1002/j.1460-2075.1992.tb05325.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES