Europe PMC
Nothing Special   »   [go: up one dir, main page]

Europe PMC requires Javascript to function effectively.

Either your web browser doesn't support Javascript or it is currently turned off. In the latter case, please turn on Javascript support in your web browser and reload this page.

This website requires cookies, and the limited processing of your personal data in order to function. By using the site you are agreeing to this as outlined in our privacy notice and cookie policy.

Identification of a Myc-dependent step during the formation of active G1 cyclin-cdk complexes.

Author information

Affiliations

  • 1. Zentrum für Molekulare Biologie Heidelberg (ZMBH), Germany
      Authors
    • Steiner P 1
    (1 author)

ORCIDs linked to this article

The EMBO Journal, 01 Oct 1995, 14(19):4814-4826
https://doi.org/10.1002/j.1460-2075.1995.tb00163.x PMID: 7588611 PMCID: PMC394579

Free full text in Europe PMC

Abstract 

Activation of conditional alleles of Myc can induce proliferation in quiescent cells. We now report that induction of Myc in density-arrested fibroblasts triggers rapid hyperphosphorylation of the retinoblastoma protein and activation of both cyclin D1- and cyclin E-associated kinase activities in the absence of significant changes in the amounts of cyclin-cdk complexes. Kinase activation by Myc is blocked by inhibitors of transcription and requires intact DNA binding and heterodimerization domains of Myc. Activation of cyclin E-cdk2 kinase in serum-starved cells occurs in two steps. The first is induced by Myc and involves the release of a 120 kDa cyclin E-cdk2 complex from a 250 kDa inactive complex that is present in starved cells. This is necessary, but not sufficient, to generate full kinase activity, as cdc25 phosphatase activity is limiting in the absence of external growth factors. In vivo cdc25 activity can be supplied by the addition of growth factors. In vitro recombinant cdc25a strongly activates the 120 kDa, but only poorly activates the 250 kDa cyclin E-cdk2 complex. Our data show that two distinct signals, one of which is supplied by Myc, are necessary for consecutive steps during growth factor-induced formation of active cyclin E-cdk2 complexes in G(o)-arrested rodent fibroblasts.

Free full text 

Logo of embojLink to Publisher's site
EMBO J. 1995 Oct 2; 14(19): 4814–4826.
PMCID: PMC394579
PMID: 7588611

Identification of a Myc-dependent step during the formation of active G1 cyclin-cdk complexes.

P Steiner, A Philipp, J Lukas, D Godden-Kent, M Pagano, S Mittnacht, J Bartek, and M Eilers
Author information Copyright and License information Disclaimer

Abstract

Activation of conditional alleles of Myc can induce proliferation in quiescent cells. We now report that induction of Myc in density-arrested fibroblasts triggers rapid hyperphosphorylation of the retinoblastoma protein and activation of both cyclin D1- and cyclin E-associated kinase activities in the absence of significant changes in the amounts of cyclin-cdk complexes. Kinase activation by Myc is blocked by inhibitors of transcription and requires intact DNA binding and heterodimerization domains of Myc. Activation of cyclin E-cdk2 kinase in serum-starved cells occurs in two steps. The first is induced by Myc and involves the release of a 120 kDa cyclin E-cdk2 complex from a 250 kDa inactive complex that is present in starved cells. This is necessary, but not sufficient, to generate full kinase activity, as cdc25 phosphatase activity is limiting in the absence of external growth factors. In vivo cdc25 activity can be supplied by the addition of growth factors. In vitro recombinant cdc25a strongly activates the 120 kDa, but only poorly activates the 250 kDa cyclin E-cdk2 complex. Our data show that two distinct signals, one of which is supplied by Myc, are necessary for consecutive steps during growth factor-induced formation of active cyclin E-cdk2 complexes in G(o)-arrested rodent fibroblasts.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (2.8M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.
 
icon of scanned page 4814
4814
icon of scanned page 4815
4815
icon of scanned page 4816
4816
icon of scanned page 4817
4817
icon of scanned page 4818
4818
icon of scanned page 4819
4819
icon of scanned page 4820
4820
icon of scanned page 4821
4821
icon of scanned page 4822
4822
icon of scanned page 4823
4823
icon of scanned page 4824
4824
icon of scanned page 4825
4825
icon of scanned page 4826
4826
 

Images in this article

Image
Image
on p.4816
Image
Image
on p.4817
Image
Image
on p.4819
Image
Image
on p.4820
Image
Image
on p.4822
Image
Image
on p.4823
Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Amati B, Land H. Myc-Max-Mad: a transcription factor network controlling cell cycle progression, differentiation and death. Curr Opin Genet Dev. 1994 Feb;4(1):102–108. [Abstract] [Google Scholar]
  • Armelin HA, Armelin MC, Kelly K, Stewart T, Leder P, Cochran BH, Stiles CD. Functional role for c-myc in mitogenic response to platelet-derived growth factor. Nature. 1984 Aug 23;310(5979):655–660. [Abstract] [Google Scholar]
  • Ayer DE, Kretzner L, Eisenman RN. Mad: a heterodimeric partner for Max that antagonizes Myc transcriptional activity. Cell. 1993 Jan 29;72(2):211–222. [Abstract] [Google Scholar]
  • Ayer DE, Lawrence QA, Eisenman RN. Mad-Max transcriptional repression is mediated by ternary complex formation with mammalian homologs of yeast repressor Sin3. Cell. 1995 Mar 10;80(5):767–776. [Abstract] [Google Scholar]
  • Baldin V, Lukas J, Marcote MJ, Pagano M, Draetta G. Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes Dev. 1993 May;7(5):812–821. [Abstract] [Google Scholar]
  • Bello-Fernandez C, Packham G, Cleveland JL. The ornithine decarboxylase gene is a transcriptional target of c-Myc. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7804–7808. [Europe PMC free article] [Abstract] [Google Scholar]
  • Benvenisty N, Leder A, Kuo A, Leder P. An embryonically expressed gene is a target for c-Myc regulation via the c-Myc-binding sequence. Genes Dev. 1992 Dec;6(12B):2513–2523. [Abstract] [Google Scholar]
  • Berry M, Metzger D, Chambon P. Role of the two activating domains of the oestrogen receptor in the cell-type and promoter-context dependent agonistic activity of the anti-oestrogen 4-hydroxytamoxifen. EMBO J. 1990 Sep;9(9):2811–2818. [Europe PMC free article] [Abstract] [Google Scholar]
  • Blackwood EM, Eisenman RN. Max: a helix-loop-helix zipper protein that forms a sequence-specific DNA-binding complex with Myc. Science. 1991 Mar 8;251(4998):1211–1217. [Abstract] [Google Scholar]
  • Blackwood EM, Lüscher B, Eisenman RN. Myc and Max associate in vivo. Genes Dev. 1992 Jan;6(1):71–80. [Abstract] [Google Scholar]
  • Castellazzi M, Spyrou G, La Vista N, Dangy JP, Piu F, Yaniv M, Brun G. Overexpression of c-jun, junB, or junD affects cell growth differently. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):8890–8894. [Europe PMC free article] [Abstract] [Google Scholar]
  • Daksis JI, Lu RY, Facchini LM, Marhin WW, Penn LJ. Myc induces cyclin D1 expression in the absence of de novo protein synthesis and links mitogen-stimulated signal transduction to the cell cycle. Oncogene. 1994 Dec;9(12):3635–3645. [Abstract] [Google Scholar]
  • Danielian PS, White R, Hoare SA, Fawell SE, Parker MG. Identification of residues in the estrogen receptor that confer differential sensitivity to estrogen and hydroxytamoxifen. Mol Endocrinol. 1993 Feb;7(2):232–240. [Abstract] [Google Scholar]
  • Davis AC, Wims M, Spotts GD, Hann SR, Bradley A. A null c-myc mutation causes lethality before 10.5 days of gestation in homozygotes and reduced fertility in heterozygous female mice. Genes Dev. 1993 Apr;7(4):671–682. [Abstract] [Google Scholar]
  • Dulić V, Lees E, Reed SI. Association of human cyclin E with a periodic G1-S phase protein kinase. Science. 1992 Sep 25;257(5078):1958–1961. [Abstract] [Google Scholar]
  • Eilers M, Picard D, Yamamoto KR, Bishop JM. Chimaeras of myc oncoprotein and steroid receptors cause hormone-dependent transformation of cells. Nature. 1989 Jul 6;340(6228):66–68. [Abstract] [Google Scholar]
  • Eilers M, Schirm S, Bishop JM. The MYC protein activates transcription of the alpha-prothymosin gene. EMBO J. 1991 Jan;10(1):133–141. [Europe PMC free article] [Abstract] [Google Scholar]
  • el-Deiry WS, Harper JW, O'Connor PM, Velculescu VE, Canman CE, Jackman J, Pietenpol JA, Burrell M, Hill DE, Wang Y, et al. WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res. 1994 Mar 1;54(5):1169–1174. [Abstract] [Google Scholar]
  • Evan GI, Lewis GK, Ramsay G, Bishop JM. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol Cell Biol. 1985 Dec;5(12):3610–3616. [Europe PMC free article] [Abstract] [Google Scholar]
  • Evan GI, Wyllie AH, Gilbert CS, Littlewood TD, Land H, Brooks M, Waters CM, Penn LZ, Hancock DC. Induction of apoptosis in fibroblasts by c-myc protein. Cell. 1992 Apr 3;69(1):119–128. [Abstract] [Google Scholar]
  • Fisher RP, Morgan DO. A novel cyclin associates with MO15/CDK7 to form the CDK-activating kinase. Cell. 1994 Aug 26;78(4):713–724. [Abstract] [Google Scholar]
  • Galaktionov K, Jessus C, Beach D. Raf1 interaction with Cdc25 phosphatase ties mitogenic signal transduction to cell cycle activation. Genes Dev. 1995 May 1;9(9):1046–1058. [Abstract] [Google Scholar]
  • Gaubatz S, Meichle A, Eilers M. An E-box element localized in the first intron mediates regulation of the prothymosin alpha gene by c-myc. Mol Cell Biol. 1994 Jun;14(6):3853–3862. [Europe PMC free article] [Abstract] [Google Scholar]
  • Gu W, Cechova K, Tassi V, Dalla-Favera R. Opposite regulation of gene transcription and cell proliferation by c-Myc and Max. Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2935–2939. [Europe PMC free article] [Abstract] [Google Scholar]
  • Gu Y, Rosenblatt J, Morgan DO. Cell cycle regulation of CDK2 activity by phosphorylation of Thr160 and Tyr15. EMBO J. 1992 Nov;11(11):3995–4005. [Europe PMC free article] [Abstract] [Google Scholar]
  • Gu Y, Turck CW, Morgan DO. Inhibition of CDK2 activity in vivo by an associated 20K regulatory subunit. Nature. 1993 Dec 16;366(6456):707–710. [Abstract] [Google Scholar]
  • Hannon GJ, Beach D. p15INK4B is a potential effector of TGF-beta-induced cell cycle arrest. Nature. 1994 Sep 15;371(6494):257–261. [Abstract] [Google Scholar]
  • Hanson KD, Shichiri M, Follansbee MR, Sedivy JM. Effects of c-myc expression on cell cycle progression. Mol Cell Biol. 1994 Sep;14(9):5748–5755. [Europe PMC free article] [Abstract] [Google Scholar]
  • Harper JW, Adami GR, Wei N, Keyomarsi K, Elledge SJ. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell. 1993 Nov 19;75(4):805–816. [Abstract] [Google Scholar]
  • Hatakeyama M, Brill JA, Fink GR, Weinberg RA. Collaboration of G1 cyclins in the functional inactivation of the retinoblastoma protein. Genes Dev. 1994 Aug 1;8(15):1759–1771. [Abstract] [Google Scholar]
  • Heikkila R, Schwab G, Wickstrom E, Loke SL, Pluznik DH, Watt R, Neckers LM. A c-myc antisense oligodeoxynucleotide inhibits entry into S phase but not progress from G0 to G1. Nature. 328(6129):445–449. [Abstract] [Google Scholar]
  • Herber B, Truss M, Beato M, Müller R. Inducible regulatory elements in the human cyclin D1 promoter. Oncogene. 1994 Apr;9(4):1295–1304. [Abstract] [Google Scholar]
  • Herrlich P, Ponta H. 'Nuclear' oncogenes convert extracellular stimuli into changes in the genetic program. Trends Genet. 1989 Apr;5(4):112–115. [Abstract] [Google Scholar]
  • Hoang AT, Cohen KJ, Barrett JF, Bergstrom DA, Dang CV. Participation of cyclin A in Myc-induced apoptosis. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6875–6879. [Europe PMC free article] [Abstract] [Google Scholar]
  • Hoffmann I, Draetta G, Karsenti E. Activation of the phosphatase activity of human cdc25A by a cdk2-cyclin E dependent phosphorylation at the G1/S transition. EMBO J. 1994 Sep 15;13(18):4302–4310. [Europe PMC free article] [Abstract] [Google Scholar]
  • Jansen-Dürr P, Meichle A, Steiner P, Pagano M, Finke K, Botz J, Wessbecher J, Draetta G, Eilers M. Differential modulation of cyclin gene expression by MYC. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3685–3689. [Europe PMC free article] [Abstract] [Google Scholar]
  • Jiang W, Kahn SM, Zhou P, Zhang YJ, Cacace AM, Infante AS, Doi S, Santella RM, Weinstein IB. Overexpression of cyclin D1 in rat fibroblasts causes abnormalities in growth control, cell cycle progression and gene expression. Oncogene. 1993 Dec;8(12):3447–3457. [Abstract] [Google Scholar]
  • Jinno S, Suto K, Nagata A, Igarashi M, Kanaoka Y, Nojima H, Okayama H. Cdc25A is a novel phosphatase functioning early in the cell cycle. EMBO J. 1994 Apr 1;13(7):1549–1556. [Europe PMC free article] [Abstract] [Google Scholar]
  • Kaczmarek L, Miller MR, Hammond RA, Mercer WE. A microinjected monoclonal antibody against human DNA polymerase-alpha inhibits DNA replication in human, hamster, and mouse cell lines. J Biol Chem. 1986 Aug 15;261(23):10802–10807. [Abstract] [Google Scholar]
  • Keath EJ, Caimi PG, Cole MD. Fibroblast lines expressing activated c-myc oncogenes are tumorigenic in nude mice and syngeneic animals. Cell. 1984 Dec;39(2 Pt 1):339–348. [Abstract] [Google Scholar]
  • Kelly K, Siebenlist U. The regulation and expression of c-myc in normal and malignant cells. Annu Rev Immunol. 1986;4:317–338. [Abstract] [Google Scholar]
  • Kelly K, Cochran BH, Stiles CD, Leder P. Cell-specific regulation of the c-myc gene by lymphocyte mitogens and platelet-derived growth factor. Cell. 1983 Dec;35(3 Pt 2):603–610. [Abstract] [Google Scholar]
  • Kirschmeier PT, Housey GM, Johnson MD, Perkins AS, Weinstein IB. Construction and characterization of a retroviral vector demonstrating efficient expression of cloned cDNA sequences. DNA. 1988 Apr;7(3):219–225. [Abstract] [Google Scholar]
  • Kumar V, Green S, Staub A, Chambon P. Localisation of the oestradiol-binding and putative DNA-binding domains of the human oestrogen receptor. EMBO J. 1986 Sep;5(9):2231–2236. [Europe PMC free article] [Abstract] [Google Scholar]
  • Land H, Chen AC, Morgenstern JP, Parada LF, Weinberg RA. Behavior of myc and ras oncogenes in transformation of rat embryo fibroblasts. Mol Cell Biol. 1986 Jun;6(6):1917–1925. [Europe PMC free article] [Abstract] [Google Scholar]
  • Langdon WY, Harris AW, Cory S, Adams JM. The c-myc oncogene perturbs B lymphocyte development in E-mu-myc transgenic mice. Cell. 1986 Oct 10;47(1):11–18. [Abstract] [Google Scholar]
  • Littlewood TD, Hancock DC, Danielian PS, Parker MG, Evan GI. A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res. 1995 May 25;23(10):1686–1690. [Europe PMC free article] [Abstract] [Google Scholar]
  • Lovec H, Sewing A, Lucibello FC, Müller R, Möröy T. Oncogenic activity of cyclin D1 revealed through cooperation with Ha-ras: link between cell cycle control and malignant transformation. Oncogene. 1994 Jan;9(1):323–326. [Abstract] [Google Scholar]
  • Lukas J, Müller H, Bartkova J, Spitkovsky D, Kjerulff AA, Jansen-Dürr P, Strauss M, Bartek J. DNA tumor virus oncoproteins and retinoblastoma gene mutations share the ability to relieve the cell's requirement for cyclin D1 function in G1. J Cell Biol. 1994 May;125(3):625–638. [Europe PMC free article] [Abstract] [Google Scholar]
  • Lukas J, Pagano M, Staskova Z, Draetta G, Bartek J. Cyclin D1 protein oscillates and is essential for cell cycle progression in human tumour cell lines. Oncogene. 1994 Mar;9(3):707–718. [Abstract] [Google Scholar]
  • Markowitz D, Goff S, Bank A. A safe packaging line for gene transfer: separating viral genes on two different plasmids. J Virol. 1988 Apr;62(4):1120–1124. [Europe PMC free article] [Abstract] [Google Scholar]
  • Matsuoka M, Kato JY, Fisher RP, Morgan DO, Sherr CJ. Activation of cyclin-dependent kinase 4 (cdk4) by mouse MO15-associated kinase. Mol Cell Biol. 1994 Nov;14(11):7265–7275. [Europe PMC free article] [Abstract] [Google Scholar]
  • Matsushime H, Quelle DE, Shurtleff SA, Shibuya M, Sherr CJ, Kato JY. D-type cyclin-dependent kinase activity in mammalian cells. Mol Cell Biol. 1994 Mar;14(3):2066–2076. [Europe PMC free article] [Abstract] [Google Scholar]
  • Meichle A, Philipp A, Eilers M. The functions of Myc proteins. Biochim Biophys Acta. 1992 Dec 16;1114(2-3):129–146. [Abstract] [Google Scholar]
  • Meyerson M, Harlow E. Identification of G1 kinase activity for cdk6, a novel cyclin D partner. Mol Cell Biol. 1994 Mar;14(3):2077–2086. [Europe PMC free article] [Abstract] [Google Scholar]
  • Morgan DO. Principles of CDK regulation. Nature. 1995 Mar 9;374(6518):131–134. [Abstract] [Google Scholar]
  • Müller R, Mumberg D, Lucibello FC. Signals and genes in the control of cell-cycle progression. Biochim Biophys Acta. 1993 Aug 23;1155(2):151–179. [Abstract] [Google Scholar]
  • Nakabeppu Y, Oda S, Sekiguchi M. Proliferative activation of quiescent Rat-1A cells by delta FosB. Mol Cell Biol. 1993 Jul;13(7):4157–4166. [Europe PMC free article] [Abstract] [Google Scholar]
  • Nourse J, Firpo E, Flanagan WM, Coats S, Polyak K, Lee MH, Massague J, Crabtree GR, Roberts JM. Interleukin-2-mediated elimination of the p27Kip1 cyclin-dependent kinase inhibitor prevented by rapamycin. Nature. 1994 Dec 8;372(6506):570–573. [Abstract] [Google Scholar]
  • Oswald F, Lovec H, Möröy T, Lipp M. E2F-dependent regulation of human MYC: trans-activation by cyclins D1 and A overrides tumour suppressor protein functions. Oncogene. 1994 Jul;9(7):2029–2036. [Abstract] [Google Scholar]
  • Pagano M, Pepperkok R, Lukas J, Baldin V, Ansorge W, Bartek J, Draetta G. Regulation of the cell cycle by the cdk2 protein kinase in cultured human fibroblasts. J Cell Biol. 1993 Apr;121(1):101–111. [Europe PMC free article] [Abstract] [Google Scholar]
  • Pagano M, Tam SW, Theodoras AM, Beer-Romero P, Del Sal G, Chau V, Yew PR, Draetta GF, Rolfe M. Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science. 1995 Aug 4;269(5224):682–685. [Abstract] [Google Scholar]
  • Philipp A, Schneider A, Väsrik I, Finke K, Xiong Y, Beach D, Alitalo K, Eilers M. Repression of cyclin D1: a novel function of MYC. Mol Cell Biol. 1994 Jun;14(6):4032–4043. [Europe PMC free article] [Abstract] [Google Scholar]
  • Polyak K, Kato JY, Solomon MJ, Sherr CJ, Massague J, Roberts JM, Koff A. p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Dev. 1994 Jan;8(1):9–22. [Abstract] [Google Scholar]
  • Polyak K, Lee MH, Erdjument-Bromage H, Koff A, Roberts JM, Tempst P, Massagué J. Cloning of p27Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell. 1994 Jul 15;78(1):59–66. [Abstract] [Google Scholar]
  • Prendergast GC, Lawe D, Ziff EB. Association of Myn, the murine homolog of max, with c-Myc stimulates methylation-sensitive DNA binding and ras cotransformation. Cell. 1991 May 3;65(3):395–407. [Abstract] [Google Scholar]
  • Prochownik EV, Kukowska J, Rodgers C. c-myc antisense transcripts accelerate differentiation and inhibit G1 progression in murine erythroleukemia cells. Mol Cell Biol. 1988 Sep;8(9):3683–3695. [Europe PMC free article] [Abstract] [Google Scholar]
  • Quelle DE, Ashmun RA, Shurtleff SA, Kato JY, Bar-Sagi D, Roussel MF, Sherr CJ. Overexpression of mouse D-type cyclins accelerates G1 phase in rodent fibroblasts. Genes Dev. 1993 Aug;7(8):1559–1571. [Abstract] [Google Scholar]
  • Reisman D, Elkind NB, Roy B, Beamon J, Rotter V. c-Myc trans-activates the p53 promoter through a required downstream CACGTG motif. Cell Growth Differ. 1993 Feb;4(2):57–65. [Abstract] [Google Scholar]
  • Rustgi AK, Dyson N, Bernards R. Amino-terminal domains of c-myc and N-myc proteins mediate binding to the retinoblastoma gene product. Nature. 1991 Aug 8;352(6335):541–544. [Abstract] [Google Scholar]
  • Schreiber-Agus N, Chin L, Chen K, Torres R, Rao G, Guida P, Skoultchi AI, DePinho RA. An amino-terminal domain of Mxi1 mediates anti-Myc oncogenic activity and interacts with a homolog of the yeast transcriptional repressor SIN3. Cell. 1995 Mar 10;80(5):777–786. [Abstract] [Google Scholar]
  • Sebastian B, Kakizuka A, Hunter T. Cdc25M2 activation of cyclin-dependent kinases by dephosphorylation of threonine-14 and tyrosine-15. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3521–3524. [Europe PMC free article] [Abstract] [Google Scholar]
  • Serrano M, Hannon GJ, Beach D. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature. 1993 Dec 16;366(6456):704–707. [Abstract] [Google Scholar]
  • Sherr CJ. G1 phase progression: cycling on cue. Cell. 1994 Nov 18;79(4):551–555. [Abstract] [Google Scholar]
  • Toyoshima H, Hunter T. p27, a novel inhibitor of G1 cyclin-Cdk protein kinase activity, is related to p21. Cell. 1994 Jul 15;78(1):67–74. [Abstract] [Google Scholar]
  • van den Heuvel S, Harlow E. Distinct roles for cyclin-dependent kinases in cell cycle control. Science. 1993 Dec 24;262(5142):2050–2054. [Abstract] [Google Scholar]
  • Weinberg RA. The retinoblastoma protein and cell cycle control. Cell. 1995 May 5;81(3):323–330. [Abstract] [Google Scholar]
  • Westin EH, Gallo RC, Arya SK, Eva A, Souza LM, Baluda MA, Aaronson SA, Wong-Staal F. Differential expression of the amv gene in human hematopoietic cells. Proc Natl Acad Sci U S A. 1982 Apr;79(7):2194–2198. [Europe PMC free article] [Abstract] [Google Scholar]
  • Westin EH, Wong-Staal F, Gelmann EP, Dalla-Favera R, Papas TS, Lautenberger JA, Eva A, Reddy EP, Tronick SR, Aaronson SA, et al. Expression of cellular homologues of retroviral onc genes in human hematopoietic cells. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2490–2494. [Europe PMC free article] [Abstract] [Google Scholar]
  • Won KA, Xiong Y, Beach D, Gilman MZ. Growth-regulated expression of D-type cyclin genes in human diploid fibroblasts. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9910–9914. [Europe PMC free article] [Abstract] [Google Scholar]
  • Xiong Y, Hannon GJ, Zhang H, Casso D, Kobayashi R, Beach D. p21 is a universal inhibitor of cyclin kinases. Nature. 1993 Dec 16;366(6456):701–704. [Abstract] [Google Scholar]
  • Zervos AS, Gyuris J, Brent R. Mxi1, a protein that specifically interacts with Max to bind Myc-Max recognition sites. Cell. 1993 Jan 29;72(2):223–232. [Abstract] [Google Scholar]
Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

Full text links 

Read article at publisher's site: https://doi.org/10.1002/j.1460-2075.1995.tb00163.x

Read article for free, from open access legal sources, via Unpaywall: https://onlinelibrary.wiley.com/doi/pdfdirect/10.1002/j.1460-2075.1995.tb00163.xUnpaywall

Citations & impact 

Impact metrics

132
Citations
Jump to Citations

Citations of article over time

Alternative metrics

Altmetric item for https://www.altmetric.com/details/80395329
Altmetric
Discover the attention surrounding your research
https://www.altmetric.com/details/80395329

Article citations

Go to all (132) article citations

Similar Articles 

To arrive at the top five similar articles we use a word-weighted algorithm to compare words from the Title and Abstract of each citation.