Home LiteratureArticle Details
PMID: 8413260 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Overproduction of Rb protein after the G1/S boundary causes G2 arrest.

Molecular and cellular biology ·Vol. 13 ·No. 11 ·1993-11-00 ·Pages 6640-52

Karantza V, Maroo A, Fay D, Sedivy JM

Abstract

The Rb protein is known to exert its activity at decision points in the G1 phase of the cell cycle. To investigate whether it may also play some role(s) at later points in the cell cycle, we used a system of rapid inducible gene amplification to conditionally overexpress Rb protein during G2 phase. A cell line expressing a temperature-sensitive simian virus 40 large T antigen (T-Ag) was stably transfected with plasmids containing the Rb cDNA linked to the simian virus 40 origin of replication: pRB-wt, pRB-fs, and pRB-Dra, carrying wild-type murine Rb cDNA, a frameshift mutation close to the beginning of the Rb coding region, and a single-amino-acid deletion in the E1A/T-Ag binding pocket, respectively. Numerous independent cell lines were isolated at the nonpermissive temperature; cell lines displaying a high level of episomal amplification of an intact Rb expression cassette following shiftdown to the permissive temperature were chosen for further analysis. Plasmid pRB-fs did not express detectable Rb antigen, while pRB-Dra expressed full-length Rb protein. The Dra mutation has previously been shown to abrogate phosphorylation as well as T-Ag binding. Fluorescence-activated cell sorting (FACS) analysis revealed that cultures induced to overexpress either wild-type or Dra mutant Rb proteins were significantly enriched for cells with a G2 DNA content. Cultures that amplified pRB-fs or rearranged pRB-wt and did not express Rb protein had normal cell cycle profiles. Double-label FACS analysis showed that cells overexpressing Rb or Rb-Dra proteins were uniformly accumulating in G2, whereas cells expressing endogenous levels of Rb were found throughout the cell cycle. These results indicate that Rb protein is interacting with some component(s) of the cell cycle-regulatory machinery during G2 phase.

Related Genes
MeSH Terms
Animals Cell Cycle/physiology Cell Line DNA/analysis,biosynthesis DNA Replication Fluorescent Antibody Technique G1 Phase G2 Phase Genes, Retinoblastoma Haplorhini Kinetics Mice Plasmids Restriction Mapping Retinoblastoma Protein/analysis,biosynthesis,metabolism S Phase Simian virus 40/genetics Time Factors Transfection
Chemicals
Retinoblastoma Protein DNA
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Karantza V
Department of Molecular Biophysics and Biochemistry, Yale University School of Medicine, New Haven, Connecticut 06510.
Maroo A
Fay D
Sedivy J M
References (86)
86 references, click to expand
  1. Association of adenovirus early-region 1A proteins with cellular polypeptides.
    Mol Cell Biol. 1986 May;6(5):1579-89 PMID: 2431282
  2. Human retinoblastoma susceptibility gene: cloning, identification, and sequence.
    Science. 1987 Mar 13;235(4794):1394-9 PMID: 3823889
  3. Structural evidence for the authenticity of the human retinoblastoma gene.
    Science. 1987 Jun 26;236(4809):1657-61 PMID: 2885916
  4. Association between an oncogene and an anti-oncogene: the adenovirus E1A proteins bind to the retinoblastoma gene product.
    Nature. 1988 Jul 14;334(6178):124-9 PMID: 2968522
  5. SV40 large tumor antigen forms a specific complex with the product of the retinoblastoma susceptibility gene.
    Cell. 1988 Jul 15;54(2):275-83 PMID: 2839300
  6. Suppression of the neoplastic phenotype by replacement of the RB gene in human cancer cells.
    Science. 1988 Dec 16;242(4885):1563-6 PMID: 3201247
  7. Simian virus 40 deoxyribonucleic acid synthesis: the viral replicon.
    J Virol. 1972 Oct;10(4):591-8 PMID: 4343541
  8. SV40 large T antigen binds preferentially to an underphosphorylated member of the retinoblastoma susceptibility gene product family.
    Cell. 1989 Jan 13;56(1):57-65 PMID: 2910497
  9. Cellular targets for transformation by the adenovirus E1A proteins.
    Cell. 1989 Jan 13;56(1):67-75 PMID: 2521301
  10. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product.
    Science. 1989 Feb 17;243(4893):934-7 PMID: 2537532
  11. Cell lines established by a temperature-sensitive simian virus 40 large-T-antigen gene are growth restricted at the nonpermissive temperature.
    Mol Cell Biol. 1989 Apr;9(4):1672-81 PMID: 2542774
  12. Structure of the human retinoblastoma gene.
    Proc Natl Acad Sci U S A. 1989 Jul;86(14):5502-6 PMID: 2748600
  13. The cellular 107K protein that binds to adenovirus E1A also associates with the large T antigens of SV40 and JC virus.
    Cell. 1989 Jul 28;58(2):249-55 PMID: 2546678
  14. An N-terminal transformation-governing sequence of SV40 large T antigen contributes to the binding of both p110Rb and a second cellular protein, p120.
    Cell. 1989 Jul 28;58(2):257-67 PMID: 2526683
  15. 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):6474-8 PMID: 2671991
  16. The product of the retinoblastoma susceptibility gene has properties of a cell cycle regulatory element.
    Cell. 1989 Sep 22;58(6):1085-95 PMID: 2673542
  17. The retinoblastoma protein is phosphorylated during specific phases of the cell cycle.
    Cell. 1989 Sep 22;58(6):1097-105 PMID: 2673543
  18. Phosphorylation of the retinoblastoma gene product is modulated during the cell cycle and cellular differentiation.
    Cell. 1989 Sep 22;58(6):1193-8 PMID: 2673546
  19. In vitro phosphorylation of the tumor suppressor gene RB protein by mitosis-specific histone H1 kinase.
    Biochem Biophys Res Commun. 1989 Oct 16;164(1):580-6 PMID: 2553023
  20. Cell cycle-dependent regulation of phosphorylation of the human retinoblastoma gene product.
    Science. 1989 Dec 8;246(4935):1300-3 PMID: 2588006
  21. Suppression of tumorigenicity of human prostate carcinoma cells by replacing a mutated RB gene.
    Science. 1990 Feb 9;247(4943):712-5 PMID: 2300823
  22. The retinoblastoma susceptibility gene product undergoes cell cycle-dependent dephosphorylation and binding to and release from SV40 large T.
    Cell. 1990 Feb 9;60(3):387-96 PMID: 2154332
  23. An inducible mammalian amber suppressor: propagation of a poliovirus mutant.
    Cell. 1987 Jul 31;50(3):379-89 PMID: 3038332
  24. The retinoblastoma susceptibility gene encodes a nuclear phosphoprotein associated with DNA binding activity.
    Nature. 1987 Oct 15-21;329(6140):642-5 PMID: 3657987
  25. Simian virus 40 compensates a cellular mutational defect of a serum-dependent function controlling cell cycle progression in the G2 phase.
    Virology. 1988 May;164(1):165-70 PMID: 2834867
  26. Expression and state of phosphorylation of the retinoblastoma susceptibility gene product in cycling and noncycling human hematopoietic cells.
    Proc Natl Acad Sci U S A. 1990 Apr;87(7):2770-4 PMID: 2320588
  27. 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):1147-55 PMID: 2138977
  28. TGF-beta 1 inhibition of c-myc transcription and growth in keratinocytes is abrogated by viral transforming proteins with pRB binding domains.
    Cell. 1990 Jun 1;61(5):777-85 PMID: 2140528
  29. Two distinct and frequently mutated regions of retinoblastoma protein are required for binding to SV40 T antigen.
    EMBO J. 1990 Jun;9(6):1815-22 PMID: 2189724
  30. 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):3761-9 PMID: 2162480
  31. Negative regulation of human c-fos expression by the retinoblastoma gene product.
    Nature. 1990 Aug 16;346(6285):668-71 PMID: 2117257
  32. Human cyclin A is adenovirus E1A-associated protein p60 and behaves differently from cyclin B.
    Nature. 1990 Aug 23;346(6286):760-3 PMID: 2143810
  33. Binding of p53 and p105-RB is not sufficient for oncogenic transformation by a hybrid polyomavirus-simian virus 40 large T antigen.
    J Virol. 1990 Nov;64(11):5250-9 PMID: 2214017
  34. Hyperphosphorylation of the retinoblastoma gene product is determined by domains outside the simian virus 40 large-T-antigen-binding regions.
    Mol Cell Biol. 1990 Dec;10(12):6586-95 PMID: 2174110
  35. Identification of cellular proteins that can interact specifically with the T/E1A-binding region of the retinoblastoma gene product.
    Cell. 1991 Feb 8;64(3):521-32 PMID: 1825028
  36. Localization of p53, retinoblastoma and host replication proteins at sites of viral replication in herpes-infected cells.
    Nature. 1991 Jan 31;349(6308):429-31 PMID: 1671528
  37. p34cdc2: the S and M kinase?
    New Biol. 1990 May;2(5):389-401 PMID: 2149647
  38. A cellular protein that competes with SV40 T antigen for binding to the retinoblastoma gene product.
    Nature. 1991 Mar 14;350(6314):160-2 PMID: 2005966
  39. Retinoblastoma cancer suppressor gene product is a substrate of the cell cycle regulator cdc2 kinase.
    EMBO J. 1991 Apr;10(4):857-64 PMID: 2009861
  40. Human cyclin A and the retinoblastoma protein interact with similar but distinguishable sequences in the adenovirus E1A gene product.
    Oncogene. 1991 Mar;6(3):481-5 PMID: 1826347
  41. Nonfunctional mutants of the retinoblastoma protein are characterized by defects in phosphorylation, viral oncoprotein association, and nuclear tethering.
    Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3033-7 PMID: 1826560
  42. Regulation of transforming growth factor beta 1 gene expression by the product of the retinoblastoma-susceptibility gene.
    Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3052-6 PMID: 1901652
  43. G1/S phosphorylation of the retinoblastoma protein is associated with an altered affinity for the nuclear compartment.
    Cell. 1991 May 3;65(3):381-93 PMID: 2018973
  44. Independent transformation activity by adenovirus-5 E1A-conserved regions 1 or 2 mutants.
    Virology. 1991 Jun;182(2):553-61 PMID: 1827227
  45. Retinoblastoma protein and simian virus 40-dependent immortalization of human fibroblasts.
    J Virol. 1991 Jun;65(6):2845-52 PMID: 1851857
  46. The E2F transcription factor is a cellular target for the RB protein.
    Cell. 1991 Jun 14;65(6):1053-61 PMID: 1828392
  47. The retinoblastoma protein copurifies with E2F-I, an E1A-regulated inhibitor of the transcription factor E2F.
    Cell. 1991 Jun 14;65(6):1063-72 PMID: 1828393
  48. The T/E1A-binding domain of the retinoblastoma product can interact selectively with a sequence-specific DNA-binding protein.
    Cell. 1991 Jun 14;65(6):1073-82 PMID: 1828394
  49. Adenovirus E1a prevents the retinoblastoma gene product from complexing with a cellular transcription factor.
    Nature. 1991 Jun 6;351(6326):494-7 PMID: 1710781
  50. Differential regulation of the tumor suppressor molecules, retinoblastoma susceptibility gene product (Rb) and p53, during cell cycle progression of normal human T cells.
    J Immunol. 1991 Jul 15;147(2):698-704 PMID: 1906503
  51. E1A induces phosphorylation of the retinoblastoma protein independently of direct physical association between the E1A and retinoblastoma products.
    Mol Cell Biol. 1991 Aug;11(8):4253-65 PMID: 1830128
  52. Cyclin A and the retinoblastoma gene product complex with a common transcription factor.
    Nature. 1991 Jul 18;352(6332):249-51 PMID: 1830372
  53. Cloning of cDNAs for cellular proteins that bind to the retinoblastoma gene product.
    Nature. 1991 Jul 18;352(6332):251-4 PMID: 1857421
  54. Amino-terminal domains of c-myc and N-myc proteins mediate binding to the retinoblastoma gene product.
    Nature. 1991 Aug 8;352(6335):541-4 PMID: 1865909
  55. Isolation of the human cdk2 gene that encodes the cyclin A- and adenovirus E1A-associated p33 kinase.
    Nature. 1991 Sep 12;353(6340):174-7 PMID: 1653904
  56. The retinoblastoma gene product regulates progression through the G1 phase of the cell cycle.
    Cell. 1991 Oct 18;67(2):293-302 PMID: 1655277
  57. Antibodies specific for the human retinoblastoma protein identify a family of related polypeptides.
    Mol Cell Biol. 1991 Nov;11(11):5792-9 PMID: 1717832
  58. A developmentally regulated and tissue-dependent transcription factor complexes with the retinoblastoma gene product.
    EMBO J. 1991 Dec;10(12):3819-27 PMID: 1834460
  59. Effects of Ad5 E1A mutant viruses on the cell cycle in relation to the binding of cellular proteins including the retinoblastoma protein and cyclin A.
    Virology. 1992 Jan;186(1):15-24 PMID: 1530776
  60. The retinoblastoma protein is phosphorylated on multiple sites by human cdc2.
    EMBO J. 1991 Dec;10(13):4279-90 PMID: 1756735
  61. Independent binding of the retinoblastoma protein and p107 to the transcription factor E2F.
    Nature. 1992 Jan 9;355(6356):176-9 PMID: 1530885
  62. The transcription factor E2F interacts with the retinoblastoma product and a p107-cyclin A complex in a cell cycle-regulated manner.
    Cell. 1992 Jan 10;68(1):157-66 PMID: 1531040
  63. Regulation of synthesis of p34cdc2 and its homologues and their relationship to p110Rb phosphorylation during cell cycle progression of normal human T cells.
    J Immunol. 1992 Mar 15;148(6):1804-11 PMID: 1541821
  64. The retinoblastoma-susceptibility gene product becomes phosphorylated in multiple stages during cell cycle entry and progression.
    Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1795-8 PMID: 1531876
  65. The retinoblastoma protein physically associates with the human cdc2 kinase.
    Mol Cell Biol. 1992 Mar;12(3):971-80 PMID: 1545827
  66. Expression of the retinoblastoma gene product in bladder carcinoma cells associates with a low frequency of tumor formation.
    Cancer Res. 1992 Apr 1;52(7):1968-73 PMID: 1551125
  67. Interleukin-2-dependent phosphorylation of the retinoblastoma-susceptibility-gene product p110-115RB in human T-cells.
    Biochem J. 1992 Mar 15;282 ( Pt 3):759-64 PMID: 1554358
  68. Transformation of a continuous rat embryo fibroblast cell line requires three separate domains of simian virus 40 large T antigen.
    J Virol. 1992 May;66(5):2780-91 PMID: 1313902
  69. Thymidine kinase transcription is regulated at G1/S phase by a complex that contains retinoblastoma-like protein and a cdc2 kinase.
    Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3256-60 PMID: 1565617
  70. Cell cycle regulation of the human cdc2 gene.
    EMBO J. 1992 May;11(5):1797-804 PMID: 1582409
  71. 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):4549-53 PMID: 1316611
  72. The retinoblastoma gene product suppresses neu oncogene-induced transformation via transcriptional repression of neu.
    J Biol Chem. 1992 May 25;267(15):10203-6 PMID: 1350277
  73. The retinoblastoma gene product regulates Sp1-mediated transcription.
    Mol Cell Biol. 1992 Jun;12(6):2455-63 PMID: 1588949
  74. Adenovirus E1a prevents the retinoblastoma gene product from repressing the activity of a cellular transcription factor.
    EMBO J. 1992 Jul;11(7):2603-10 PMID: 1385776
  75. A cDNA encoding a pRB-binding protein with properties of the transcription factor E2F.
    Cell. 1992 Jul 24;70(2):337-50 PMID: 1638634
  76. Expression cloning of a cDNA encoding a retinoblastoma-binding protein with E2F-like properties.
    Cell. 1992 Jul 24;70(2):351-64 PMID: 1638635
  77. Retinoblastoma gene product activates expression of the human TGF-beta 2 gene through transcription factor ATF-2.
    Nature. 1992 Jul 23;358(6384):331-4 PMID: 1641004
  78. Phosphorylation of the retinoblastoma protein by cdk2.
    Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):7900-4 PMID: 1518810
  79. A cell culture model system for genetic analyses of the cell cycle by targeted homologous recombination.
    Oncogene. 1993 Apr;8(4):899-907 PMID: 8455944
  80. A new concept of tissue and tumor cell proliferation.
    Cancer Res. 1977 Nov;37(11):3845-62 PMID: 332341
  81. Animal cell cycle.
    Annu Rev Biochem. 1978;47:715-50 PMID: 354504
  82. Association of a murine 53,000-dalton phosphoprotein with simian virus 40 large-T antigen in transformed cells.
    J Virol. 1980 Apr;34(1):213-24 PMID: 6246255
  83. Characteristics of an SV40-plasmid recombinant and its movement into and out of the genome of a murine cell.
    Cell. 1980 Aug;21(1):127-39 PMID: 6250708
  84. Genetic analysis of control of proliferation in fibroblastic cells in culture. I. Isolation and characterization of mutants temperature-sensitive for proliferation or survival of untransformed diploid rat cell line 3Y1.
    Somat Cell Mol Genet. 1984 Jan;10(1):17-28 PMID: 6583851
  85. Detection of cellular proteins associated with human adenovirus type 5 early region 1A polypeptides.
    Virology. 1985 Nov;147(1):142-53 PMID: 2932846
  86. A human DNA segment with properties of the gene that predisposes to retinoblastoma and osteosarcoma.
    Nature. 1986 Oct 16-22;323(6089):643-6 PMID: 2877398
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1993-11-00
Pages
6640-52
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC364727
Subset
IM
Grants
NCI NIH HHS · CA-16359 · United States
NIGMS NIH HHS · GM-07223 · United States
NIGMS NIH HHS · GM-RO1-41690 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com