Ablation of the Retinoblastoma gene family deregulates G1 control causing immortalization and increased cell turnover under growth-restricting conditions

Dannenberg, Jan-Hermen; van Rossum, Agnes; Schuijff, Leontine; te Riele, Hein

doi:10.1101/gad.847700

Cited by 413Cancer-related Molecular PathwaysTelomeres, Telomerase, and SenescenceRetinal Development and Disorders

Ablation of the Retinoblastoma gene family deregulates G1 control causing immortalization and increased cell turnover under growth-restricting conditions

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Dannenberg, Jan-Hermen, van Rossum, Agnes, Schuijff, Leontine, te Riele, Hein·2000·Genes & Development

DOI 10.1101/gad.847700PMC PMC317114

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Abstract

The retinoblastoma suppressor pRB belongs to the family of so-called pocket proteins, which also includes p107 and p130. These proteins may functionally overlap in cell cycle control and tumor suppression. We have generated an isogenic set of embryonic stem (ES) cell lines carrying single or compound loss-of-function mutations in the Rb gene family, including a cell line completely devoid of all three pocket proteins. None of the knockout combinations affected the growth characteristics of ES cells; however, concomitant ablation of all three pocket proteins strongly impaired their differentiation capacity. For the generated genotypes, primary mouse embryonic fibroblasts (MEFs) also were obtained. While inactivation of Rb alone did not alleviate the senescence response of MEFs, pRB/p107-deficient MEFs, after having adapted to in vitro culturing, continued to proliferate at modest rate. Additional ablation of p130 rendered MEFs completely insensitive to senescence-inducing signals and strongly increased their proliferation rate. Although triple-knockout MEFs retained anchorage dependence, they lacked proper G 1 control and showed increased cell turnover under growth-inhibiting conditions.

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In ES cells, ablation of RB, p107, and p130 impairs differentiation and increases cell turnover under growth arrest.
“In ES cells, ablation of all three RB family members (RB, p107 and p130) results in impaired differentiation and an increase in cell turnover under growth arrest conditions69.”
From Molecular regulation of stem cell quiescence (2013) · cites this paper as [69]

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The serial cultivation of human diploid cell strains
Hayflick, L., & Moorhead, P. S. (1961) · Experimental Cell Research · doi:10.1016/0014-4827(61)90192-6 · Cited by 8,508 · see citing works
Cancer Cell Cycles
Sherr, C. J. (1996) · Science · doi:10.1126/science.274.5293.1672 · Cited by 5,379 · see citing works
Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a
Serrano, M., Lin, A. W., McCurrach, M. E., Beach, D., & Lowe, S. W. (1997) · Cell · doi:10.1016/s0092-8674(00)81902-9 · Cited by 5,178 · cited 1× · see citing works
“Thus, inactivation of Ink4a, p19Arf, or p53 has been shown to result in immortalization of MEFs (Serrano et al. 1996, 1997; Kamijo et al. 1997).”
Background
The retinoblastoma protein and cell cycle control
Weinberg, R. A. (1995) · Cell · doi:10.1016/0092-8674(95)90385-2 · Cited by 4,862 · see citing works
A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4.
Serrano, M., Hannon, G. J., & Beach, D. (1993) · Nature · doi:10.1038/366704a0 · Cited by 3,650 · see citing works
The human papilloma virus-16 E7-oncoprotein is able to bind to the retinoblastoma gene product
Dyson, N., Howley, P. M., Münger, K., & Harlow, E. (1989) · Science · doi:10.1126/science.2537532 · Cited by 3,017 · see citing works
Induction of apoptosis in fibroblasts by c-myc protein
Evan, G. I., Wyllie, A. H., Gilbert, C. S., Littlewood, T. D., Land, H., Brooks, M. W., Waters, C. M., Penn, L. Z., & Hancock, D. C. (1992) · Cell · doi:10.1016/0092-8674(92)90123-t · Cited by 2,941 · see citing works
A cell cycle regulator potentially involved in genesis of many tumor types
Kamb, A., Gruis, N. A., Weaver-Feldhaus, J., Liu, Q., Harshman, K., Tavtigian, S. V., Stockert, E., Day, R. S., Johnson, B. E., & Skolnick, M. H. (1994) · Science · doi:10.1126/science.8153634 · Cited by 2,751 · see citing works
QUANTITATIVE STUDIES OF THE GROWTH OF MOUSE EMBRYO CELLS IN CULTURE AND THEIR DEVELOPMENT INTO ESTABLISHED LINES
Todaro, G. J., & Green, H. (1963) · The Journal of Cell Biology · doi:10.1083/jcb.17.2.299 · Cited by 2,725 · see citing works
The regulation of E2F by pRB-family proteins.
Dyson, N. (1998) · Genes & Development · doi:10.1101/gad.12.15.2245 · Cited by 2,317 · see citing works
p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest.Preprint
Polyak, K., Kato, J., Solomon, M., Sherr, C., Massagué, J., Roberts, J., & Koff, A. (1994) · Genes & Development · doi:10.1101/gad.8.1.9 · Cited by 1,949 · see citing works
Effects of an Rb mutation in the mouse
Jacks, T., Fazeli, A., Schmitt, E. M., Bronson, R. T., Goodell, M. A., & Weinberg, R. A. (1992) · Nature · doi:10.1038/359295a0 · Cited by 1,755 · see citing works
Deletions of the cyclin-dependent kinase-4 inhibitor gene in multiple human cancers
Nobori, T., Miura, K., Wu, D. J., Lois, A., Takabayashi, K., & Carson, D. A. (1994) · Nature · doi:10.1038/368753a0 · Cited by 1,742 · see citing works
ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppression pathways
Zhang, Y., Xiong, Y., & Yarbrough, W. G. (1998) · Cell · doi:10.1016/s0092-8674(00)81401-4 · Cited by 1,626 · see citing works
Role of the INK4a Locus in Tumor Suppression and Cell Mortality
Serrano, M., Lee, H.-W., Chin, L., Cordon-Cardo, C., Beach, D., & DePinho, R. A. (1996) · Cell · doi:10.1016/s0092-8674(00)81079-x · Cited by 1,585 · see citing works
Tumor Suppression at the Mouse INK4a Locus Mediated by the Alternative Reading Frame Product p19
Kamijo, T., Zindy, F., Roussel, M. F., Quelle, D. E., Downing, J. R., Ashmun, R. A., Grosveld, G., & Sherr, C. J. (1997) · Cell · doi:10.1016/s0092-8674(00)80452-3 · Cited by 1,566 · see citing works
The Ink4a tumor suppressor gene product, p19Arf, interacts with MDM2 and neutralizes MDM2’s inhibition of p53
Pomerantz, J., Schreiber-Agus, N., Liégeois, N. J., Silverman, A., Alland, L., Chin, L., Potes, J., Chen, K., Orlow, I., Lee, H.-W., et al. (1998) · Cell · doi:10.1016/s0092-8674(00)81400-2 · Cited by 1,521 · see citing works
Alternative reading frames of the INK4a tumor suppressor gene encode two unrelated proteins capable of inducing cell cycle arrest
Ouelle, D. E., Zindy, F., Ashmun, R. A., & Sherr, C. J. (1995) · Cell · doi:10.1016/0092-8674(95)90214-7 · Cited by 1,485 · see citing works
SV40 large tumor antigen forms a specific complex with the product of the retinoblastoma susceptibility gene
DeCaprio, J. A., Ludlow, J. W., Figge, J., Shew, J.-Y., Huang, C.-M., Lee, W.-H., Marsilio, E., Paucha, E., & Livingston, D. M. (1988) · Cell · doi:10.1016/0092-8674(88)90559-4 · Cited by 1,459 · see citing works
Promoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mice.Preprint
Friedrich, G., & Soriano, P. M. (1991) · Genes & Development · doi:10.1101/gad.5.9.1513 · Cited by 1,403 · see citing works
Association between an oncogene and an anti-oncogene: the adenovirus E1A proteins bind to the retinoblastoma gene product
Whyte, P., Buchkovich, K. J., Horowitz, J. M., Friend, S. H., Raybuck, M., Weinberg, R. A., & Harlow, E. (1988) · Nature · doi:10.1038/334124a0 · Cited by 1,403 · see citing works
Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis
Lee, E. Y.-H. P., Chang, C.-Y., Hu, N., Wang, Y.-C. J., Lai, C., Herrup, K., Lee, W., & Bradley, A. (1992) · Nature · doi:10.1038/359288a0 · Cited by 1,264 · see citing works
Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization
Zindy, F., Eischen, C. M., Randle, D. H., Kamijo, T., Cleveland, J. L., Sherr, C. J., & Roussel, M. F. (1998) · Genes & Development · doi:10.1101/gad.12.15.2424 · Cited by 1,245 · see citing works
Radiation-induced cell cycle arrest compromised by p21 deficiency
Brugarolas, J., Chandrasekaran, C., Gordon, J. I., Beach, D., Jacks, T., & Hannon, G. J. (1995) · Nature · doi:10.1038/377552a0 · Cited by 1,242 · cited 2× · see citing works
“…was determined by incubating MEFs with 5-Bromodeoxyuridine (0.3 µg/mL) plus 5-Fluoro-5deoxyuridine (0.03 µg/mL) for 5 h. Cells were collected and resuspended in 70% alcohol at 4°C, stained with DAKO mouse anti-BrdU antibody, and prepared for FACS analysis as described in Brugarolas et al. (1995).”
BackgroundMethodInfluential
Distinct Roles for Cyclin-Dependent Kinases in Cell Cycle Control
van den Heuvel, S., & Harlow, E. (1993) · Science · doi:10.1126/science.8266103 · Cited by 1,092 · see citing works
Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells.
Kanda, T., Sullivan, K., & Wahl, G. (1998) · Current Biology · doi:10.1016/s0960-9822(98)70156-3 · Cited by 1,040 · see citing works
Requirement for a functional Rb-1 gene in murine development
Clarke, A. R., Maandag, E. R., van ROON, M. A., van der Lugt, N. M. T., van der Valk, M., Hooper, M., Berns, A. J. M., & Rielef, H. T. (1992) · Nature · doi:10.1038/359328a0 · Cited by 1,006 · see citing works
p14ARF links the tumour suppressors RB and p53
Bates, S., Phillips, A. C., Clark, P. A., Stott, F., Peters, G., Ludwig, R. L., & Vousden, K. H. (1998) · Nature · doi:10.1038/25867 · Cited by 918 · see citing works
Abnormalities in Structure and Expression of the Human Retinoblastoma Gene in SCLC
Harbour, J. W., Lai, S.-L., Whang‐Peng, J., Gazdar, A. F., Minna, J. D., & Kaye, F. J. (1988) · Science · doi:10.1126/science.2838909 · Cited by 900 · see citing works
Functional and physical interactions of the ARF tumor suppressor with p53 and Mdm2
Kamijo, T., Weber, J. D., Zambetti, G., Zindy, F., Roussel, M. F., & Sherr, C. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.14.8292 · Cited by 899 · see citing works
p53 controls both the G2/M and the G1 cell cycle checkpoints and mediates reversible growth arrest in human fibroblasts.
Agarwal, M. L., Agarwal, A., Taylor, W. R., & Stark, G. R. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.18.8493 · Cited by 858 · see citing works
Cyclin-Dependent Regulation of G 1 in Mammalian Fibroblasts
Ohtsubo, M., & Roberts, J. M. (1993) · Science · doi:10.1126/science.8384376 · Cited by 767 · see citing works
Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis.
Qin, X. Q., Livingston, D. M., Kaelin, W. G., & Adams, P. D. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.23.10918 · Cited by 753 · see citing works
Genetic alterations of cyclins, cyclin-dependent kinases, and Cdk inhibitors in human cancer
(1996) · Advances in cancer research · doi:10.1016/s0065-230x(08)60352-8 · Cited by 752 · see citing works
Mediation of c-Myc-Induced Apoptosis by p53
Hermeking, H., & Eick, D. (1994) · Science · doi:10.1126/science.8091232 · Cited by 738 · see citing works
Stabilization of the p53 tumor suppressor is induced by adenovirus 5 E1A and accompanies apoptosis.Preprint
Lowe, S. W., & Ruley, H. E. (1993) · Genes & Development · doi:10.1101/gad.7.4.535 · Cited by 662 · see citing works
Bax suppresses tumorigenesis and stimulates apoptosis in vivo
Yin, C., Knudson, C. M., Korsmeyer, S. J., & Dyke, T. V. (1997) · Nature · doi:10.1038/385637a0 · Cited by 650 · see citing works
p19ARF links the tumour suppressor p53 to Ras
Palmero, I., Pantoja, C., & Serrano, M. (1998) · Nature · doi:10.1038/25870 · Cited by 617 · see citing works
p53-dependent apoptosis produced by Rb-deficiency in the developing mouse lens
Morgenbesser, S. D., Williams, B. O., Jacks, T., & DePinho, R. A. (1994) · Nature · doi:10.1038/371072a0 · Cited by 607 · see citing works
E1A signaling to p53 involves the p19ARFtumor suppressorPreprint
de Stanchina, E., McCurrach, M. E., Zindy, F., Shieh, S.-Y., Ferbeyre, G., Samuelson, A. V., Prives, C. L., Roussel, M. F., Sherr, C. J., & Lowe, S. W. (1998) · Genes & Development · doi:10.1101/gad.12.15.2434 · Cited by 607 · see citing works
Interaction between the retinoblastoma protein and the oncoprotein MDM2
Xiao, Z.-X., Chen, J., Levine, A. J., Modjtahedi, N., Xing, J. W., Sellers, W. R., & Livingston, D. M. (1995) · Nature · doi:10.1038/375694a0 · Cited by 586 · see citing works
Inactivation of the Retinoblastoma Susceptibility Gene in Human Breast Cancers
Lee, E. Y.-H. P., To, H., Shew, J.-Y., Bookstein, R., Scully, P., & Lee, W. (1988) · Science · doi:10.1126/science.3388033 · Cited by 581 · see citing works
Expression of the p16INK4a tumor suppressor versus other INK4 family members during mouse development and aging
Zindy, F., Quelle, D. E., Roussel, M. F., & Sherr, C. J. (1997) · Oncogene · doi:10.1038/sj.onc.1201178 · Cited by 574 · see citing works
Myc-mediated apoptosis requires wild-type p53 in a manner independent of cell cycle arrest and the ability of p53 to induce p21waf1/cip1.Preprint
Wagner, A. J., Kokontis, J. M., & Hay, N. (1994) · Genes & Development · doi:10.1101/gad.8.23.2817 · Cited by 540 · see citing works
The biology of replicative senescence
Campisi, J. (1997) · European Journal of Cancer · doi:10.1016/s0959-8049(96)00058-5 · Cited by 538 · see citing works
Frequent inactivation of the retinoblastoma anti-oncogene is restricted to a subset of human tumor cells.
Horowitz, J. M., Park, S. H., Bogenmann, E., Cheng, J., Yandell, D. W., Kaye, F. J., Minna, J. D., Dryja, T. P., & Weinberg, R. A. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.7.2775 · Cited by 532 · see citing works
Toward an understanding of the functional complexity of the E2F and retinoblastoma families.
Nevins, J. R. (1998) · PubMed · Cited by 514 · see citing works
Id2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins
Lasorella, A., Noseda, M., Beyna, M., & Iavarone, A. (2000) · Nature · doi:10.1038/35036504 · Cited by 497 · see citing works
Untitled work
(1993) · PubMed · Cited by 469 · see citing works
p53 alteration is a common event in the spontaneous immortalization of primary BALB/c murine embryo fibroblasts.
Harvey, D. M., & Levine, A. J. (1991) · Genes & Development · doi:10.1101/gad.5.12b.2375 · Cited by 453 · see citing works
E-Cadherin–dependent Growth Suppression is Mediated by the Cyclin-dependent Kinase Inhibitor p27KIP1
Croix, B. S., Sheehan, C., Rak, J. W., Flørenes, V. A., Slingerland, J. M., & Kerbel, R. S. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.142.2.557 · Cited by 450 · see citing works
Highly efficient gene targeting in embryonic stem cells through homologous recombination with isogenic DNA constructs.
Riele, H. T., Maandag, E. R., & Berns, A. J. M. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.11.5128 · Cited by 446 · see citing works
pRB and p107/p130 are required for the regulated expression of different sets of E2F responsive genes
Hurford, R. K., Cobrinik, D., Lee, M. H., & Dyson, N. (1997) · Genes & Development · doi:10.1101/gad.11.11.1447 · Cited by 431 · see citing works
Shared role of the pRB-related p130 and p107 proteins in limb development.Preprint
Cobrinik, D. E., Lee, M. H., Hannon, G. J., Mulligan, G., Bronson, R. T., Dyson, N. J., Harlow, E. E., Beach, D., Weinberg, R. A., & Jacks, T. (1996) · Genes & Development · doi:10.1101/gad.10.13.1633 · Cited by 426 · see citing works
The retinoblastoma gene family in differentiation and development
Lipinski, M. M., & Jacks, T. (1999) · Oncogene · doi:10.1038/sj.onc.1203244 · Cited by 404 · see citing works
A Link Between Cyclin A Expression and Adhesion-Dependent Cell Cycle Progression
Guadagno, T. M., Ohtsubo, M., Roberts, J. M., & Assoian, R. K. (1993) · Science · doi:10.1126/science.8248807 · Cited by 393 · see citing works
Mutation of E2f-1 Suppresses Apoptosis and Inappropriate S Phase Entry and Extends Survival of Rb-Deficient Mouse Embryos
Tsai, K. Y., Hu, Y., Macleod, K. F., Crowley, D., Yamasaki, L., & Jacks, T. (1998) · Molecular Cell · doi:10.1016/s1097-2765(00)80274-9 · Cited by 372 · see citing works
Dependence of Cyclin E-CDK2 Kinase Activity on Cell Anchorage
Fang, F., Orend, G., Watanabe, N., Hunter, T. R., & Ruoslahti, E. I. (1996) · Science · doi:10.1126/science.271.5248.499 · Cited by 361 · see citing works
Active Transcriptional Repression by the Rb–E2F Complex Mediates G1 Arrest Triggered by p16INK4a, TGFβ, and Contact Inhibition
Zhang, H. S., Postigo, A. A., & Dean, D. C. (1999) · Cell · doi:10.1016/s0092-8674(00)80714-x · Cited by 349 · see citing works
Targeted disruption of p107: functional overlap between p107 and Rb.Preprint
Lee, M. H., Williams, B. O., Mulligan, G., Mukai, S., Bronson, R. T., Dyson, N. J., Harlow, E., & Jacks, T. (1996) · Genes & Development · doi:10.1101/gad.10.13.1621 · Cited by 335 · see citing works
The retinoblastoma gene family: cousins with overlapping interests
Mulligan, G. (1998) · Trends in Genetics · doi:10.1016/s0168-9525(98)01470-x · Cited by 334 · see citing works
p107 is a suppressor of retinoblastoma development in pRb-deficient micePreprint
Robanus-Maandag, E. C., Dekker, M., van der Valk, M., Carrozza, M. L., Jeanny, J., Dannenberg, J., Berns, A. J. M., & Riele, H. T. (1998) · Genes & Development · doi:10.1101/gad.12.11.1599 · Cited by 319 · see citing works
Self-citation
Altered Cell Cycle Kinetics, Gene Expression, and G 1 Restriction Point Regulation in Rb -Deficient Fibroblasts
Herrera, R. E., Sah, V. P., Williams, B. O., Mäkelä, T. P., Weinberg, R. A., & Jacks, T. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.5.2402 · Cited by 302 · see citing works
Abrogation of oncogene-associated apoptosis allows transformation of p53-deficient cells.
Lowe, S. W., Jacks, T., Housman, D. E., & Ruley, H. E. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.6.2026 · Cited by 286 · see citing works
p16INK4A and p19ARF act in overlapping pathways in cellular immortalization
Carnero, A., Hudson, J. D., Price, C. M., & Beach, D. (2000) · Nature Cell Biology · doi:10.1038/35004020 · Cited by 278 · see citing works
Heterozygous Rb-1 delta 20/+mice are predisposed to tumors of the pituitary gland with a nearly complete penetrance.
Hu, N., Gutsmann, A., Herbert, D. C., Bradley, A., Lee, W., & Lee, E. Y. (1994) · PubMed · Cited by 266 · see citing works
Withdrawal of differentiation inhibitory activity/leukemia inhibitory factor up-regulates D-type cyclins and cyclin-dependent kinase inhibitors in mouse embryonic stem cells.
Savatier, P., Lapillonne, H., van Grunsven, L. A., Rudkin, B. B., & Samarut, J. (1996) · PubMed · Cited by 260 · see citing works
Developmental rescue of an embryonic‐lethal mutation in the retinoblastoma gene in chimeric mice.
Robanus-Maandag, E. C., van der Valk, M., Vlaar, M., Feltkamp, C. A., O’Brien, J. M., van ROON, M. A., van der Lugt, N. M. T., Berns, A. J. M., & Riele, H. T. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06746.x · Cited by 248 · see citing works
Contrasting patterns of retinoblastoma protein expression in mouse embryonic stem cells and embryonic fibroblasts.
Savatier, P., Huang, S., Székely, L., Wiman, K. G., & Samarut, J. (1994) · PubMed · Cited by 245 · see citing works
pRB plays an essential role in cell cycle arrest induced by DNA damage
Harrington, E. A., Bruce, J. L., Harlow, E., & Dyson, N. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.20.11945 · Cited by 242 · see citing works
Cooperating oncogenes converge to regulate cyclin/cdk complexes.Preprint
Lloyd, A. C., Obermüller, F., Staddon, S., Barth, C. F., McMahon, M., & Land, H. (1997) · Genes & Development · doi:10.1101/gad.11.5.663 · Cited by 224 · see citing works
Murine fibroblasts lacking p21 undergo senescence and are resistant to transformation by oncogenic Ras.
Pantoja, C., & Serrano, M. (1999) · Oncogene · doi:10.1038/sj.onc.1202880 · Cited by 201 · cited 1× · see citing works
“This phenomenon, known as contact inhibition, was shown to be accompanied by increased p27KIP1 and decreased cyclin D1 levels (Polyak et al. 1994; St. Croix et al. 1998).”
Background
Reversible arrest of growth in G1 of an established fibroblast line (3T3)
Nilausen, K., & Green, H. (1965) · Experimental Cell Research · doi:10.1016/0014-4827(65)90306-x · Cited by 187 · see citing works
Strain-dependent embryonic lethality in mice lacking the retinoblastoma-related p130 gene
LeCouter, J. E., Kablar, B., Whyte, P., Ying, C., & Rudnicki, M. A. (1998) · Development · doi:10.1242/dev.125.23.4669 · Cited by 181 · see citing works
p21 Is a Critical CDK2 Regulator Essential for Proliferation Control in Rb-deficient Cells
Brugarolas, J., Bronson, R. T., & Jacks, T. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.141.2.503 · Cited by 153 · see citing works
Schwann cell differentiation
Zorick, T. S., & Lemke, G. (1996) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(96)80090-1 · Cited by 150 · see citing works
Cdkn2a , the cyclin-dependent kinase inhibitor encoding p16 INK4a and p19 ARF , is a candidate for the plasmacytoma susceptibility locus, Pctr1
Zhang, S., Ramsay, E. S., & Mock, B. A. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.5.2429 · Cited by 147 · see citing works
Strain-Dependent Myeloid Hyperplasia, Growth Deficiency, and Accelerated Cell Cycle in Mice Lacking the Rb-Related p107 Gene
LeCouter, J. E., Kablar, B., Hardy, W. R., Ying, C., Megeney, L. A., May, L. L., & Rudnicki, M. A. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.12.7455 · Cited by 141 · see citing works
Flp-mediated tissue-specific inactivation of the retinoblastoma tumor suppressor gene in the mouse
Vooijs, M., van der Valk, M., Riele, H. T., & Berns, A. J. M. (1998) · Oncogene · doi:10.1038/sj.onc.1202169 · Cited by 140 · see citing works
Anchorage-Dependent Transcription of the Cyclin A Gene
Schulze, A., Zerfass, K., Bergès, J., Middendorp, S., Jansen‐Dürr, P., & Henglein, B. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.9.4632 · Cited by 138 · see citing works
p19 Arf induces p53-dependent apoptosis during Abelson virus-mediated pre-B cell transformation
Radfar, A., Unnikrishnan, I., Lee, H., DePinho, R. A., & Rosenberg, N. E. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.22.13194 · Cited by 138 · see citing works
Accumulation of p16INK4a in mouse fibroblasts as a function of replicative senescence and not of retinoblastoma gene status
Palmero, I., McConnell, B. B., Parry, D., Brookes, S., Hara, E., Bates, S., Jat, P., & Peters, G. G. (1997) · Oncogene · doi:10.1038/sj.onc.1201212 · Cited by 123 · see citing works
Accumulation of p53 induced by the adenovirus E1A protein requires regions involved in the stimulation of DNA synthesis
Querido, E., Teodoro, J. G., & Branton, P. E. (1997) · Journal of Virology · doi:10.1128/jvi.71.5.3526-3533.1997 · Cited by 99 · see citing works
Oncogenic Ras Induces p19ARF and Growth Arrest in Mouse Embryo Fibroblasts Lacking p21Cip1 and p27Kip1 without Activating Cyclin D-dependent Kinases
Groth, A., Weber, J. D., Willumsen, B. M., Sherr, C. J., & Roussel, M. F. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m003417200 · Cited by 92 · see citing works
Ice Rhythms—Core Reveals a Plethora of Climate Cycles
Kerr, R. A. (1996) · Science · doi:10.1126/science.274.5287.499 · Cited by 80 · see citing works
p130 Is Dispensable in Peripheral T Lymphocytes: Evidence for Functional Compensation by p107 and pRB
Mulligan, G., Wong, J., & Jacks, T. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.1.206 · Cited by 72 · see citing works
E2F: a nodal point in cell cycle regulation
Bernards, R. (1997) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/s0304-419x(97)00027-9 · Cited by 47 · see citing works
p53 mutations in spontaneously immortalized 3T12 but not 3T3 mouse embryo cells.
Rittling, S. R., & Denhardt, D. T. (1992) · PubMed · Cited by 41 · see citing works
p27kip1-independent cell cycle regulation by MYC
Berns, K., Martins, C. P., Dannenberg, J., Berns, A. J. M., Riele, H. T., & Bernards, R. (2000) · Oncogene · doi:10.1038/sj.onc.1203879 · Cited by 30 · see citing works
Self-citation
Cloning and expression of the Rb-related mouse p130 mRNA.
LeCouter, J. E., Whyte, P., & Rudnicki, M. A. (1996) · PubMed · Cited by 29 · see citing works
Role of first exon/intron sequences in the regulation of myc family oncogenic potency.
Xu, L., Wallen, R., Patel, V., & DePinho, R. A. (1993) · PubMed · Cited by 16 · see citing works
Sequences and Factors Required for the F9 Embryonal Carcinoma Stem Cell E1a-Like Activity
Murray, E. J., Stott, D., & Rigby, P. W. J. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.11.5534 · Cited by 6 · see citing works

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Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence
Narita, M., Nuñez, S., Heard, E., Narita, M., Lin, A. W., Hearn, S. A., Spector, D. L., Hannon, G. J., & Lowe, S. W. (2003) · Cell · doi:10.1016/s0092-8674(03)00401-x · Cited by 2,278 · see citing works
The essence of senescence: Figure 1.
Kuilman, T., Michaloglou, C., Mooi, W. J., & Peeper, D. S. (2010) · Genes & Development · doi:10.1101/gad.1971610 · Cited by 2,038 · see citing works
The RB and p53 pathways in cancer
Sherr, C. J., & McCormick, F. (2002) · Cancer Cell · doi:10.1016/s1535-6108(02)00102-2 · Cited by 1,690 · see citing works
To cycle or not to cycle: a critical decision in cancer
Malumbres, M., & Barbacid, M. (2001) · Nature reviews. Cancer · doi:10.1038/35106065 · Cited by 1,475 · see citing works
Mammalian cyclin-dependent kinases
Malumbres, M., & Barbacid, M. (2005) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2005.09.005 · Cited by 1,294 · see citing works
Molecular regulation of stem cell quiescence
Cheung, T. H., & Rando, T. A. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3591 · Cited by 1,148 · see citing works
E2F integrates cell cycle progression with DNA repair, replication, and G 2 /M checkpoints
Ren, B., Cam, H., Takahashi, Y., Volkert, T., Terragni, J., Young, R. A., & Dynlacht, B. D. (2002) · Genes & Development · doi:10.1101/gad.949802 · Cited by 1,125 · see citing works
The signals and pathways activating cellular senescence
Ben-Porath, I., & Weinberg, R. A. (2005) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2004.10.013 · Cited by 1,046 · see citing works
The INK4a/ARF network in tumour suppression
Sherr, C. J. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35096061 · Cited by 984 · see citing works
Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation
Orford, K. W., & Scadden, D. T. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2269 · Cited by 851 · see citing works
Loss of p16Ink4a with retention of p19Arf predisposes mice to tumorigenesis
Sharpless, N. E., Bardeesy, N., Lee, K.-H., Carrasco, D., Castrillon, D. H., Aguirre, A. J., Wu, E. A., Horner, J. W., & DePinho, R. A. (2001) · Nature · doi:10.1038/35092592 · Cited by 848 · see citing works
FoxM1 is required for execution of the mitotic programme and chromosome stability
Laoukili, J., Kooistra, M. R. H., Brás, A., Kauw, J. J. W., Kerkhoven, R. M., Morrison, A. J., Clevers, H. C., & Medema, R. H. (2005) · Nature Cell Biology · doi:10.1038/ncb1217 · Cited by 808 · see citing works
Cyclin D-dependent kinases, INK4 inhibitors and cancer
Ortega, S., Malumbres, M., & Barbacid, M. (2002) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/s0304-419x(02)00037-9 · Cited by 774 · see citing works
The retinoblastoma tumour suppressor in development and cancer
Classon, M., & Harlow, E. (2002) · Nature Reviews Cancer · doi:10.1038/nrc950 · Cited by 738 · see citing works
Signalling, cell cycle and pluripotency in embryonic stem cells
Burdon, T., Smith, A. T., & Savatier, P. (2002) · Trends in Cell Biology · doi:10.1016/s0962-8924(02)02352-8 · Cited by 710 · see citing works
Tumor suppression by Ink4a-Arf: progress and puzzles.
Lowe, S. W., & Sherr, C. J. (2003) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(02)00013-8 · Cited by 699 · see citing works
Induction of small cell lung cancer by somatic inactivation of both Trp53 and Rb1 in a conditional mouse model
Meuwissen, R., Linn, S. C., Linnoila, R. I., Zevenhoven, J., Mooi, W. J., & Berns, A. (2003) · Cancer Cell · doi:10.1016/s1535-6108(03)00220-4 · Cited by 643 · see citing works
Plasminogen activator inhibitor-1 is a critical downstream target of p53 in the induction of replicative senescence
Kortlever, R. M., Higgins, P. J., & Bernards, R. (2006) · Nature Cell Biology · doi:10.1038/ncb1448 · Cited by 637 · see citing works
Pocket proteins and cell cycle control
Cobrinik, D. (2005) · Oncogene · doi:10.1038/sj.onc.1208619 · Cited by 601 · see citing works
Targeted disruption of the three Rb-related genes leads to loss of G 1 control and immortalization
Sage, J., Mulligan, G. J., Attardi, L. D., Miller, A., Chen, S., Williams, B., Theodorou, E., & Jacks, T. (2000) · Genes & Development · doi:10.1101/gad.843200 · Cited by 582 · see citing works
Comparative biology of mouse versus human cells: modelling human cancer in mice
Rangarajan, A., & Weinberg, R. A. (2003) · Nature reviews. Cancer · doi:10.1038/nrc1235 · Cited by 567 · see citing works
Molecular mechanisms underlying RB protein function
Dick, F. A., & Rubin, S. M. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3567 · Cited by 570 · see citing works
Loss of p16Ink4a confers susceptibility to metastatic melanoma in mice
Krimpenfort, P., Quon, K. C., Mooi, W. J., Loonstra, A., & Berns, A. (2001) · Nature · doi:10.1038/35092584 · Cited by 568 · see citing works
Cell Cycle Inhibition by FoxO Forkhead Transcription Factors Involves Downregulation of Cyclin D
Schmidt, M., de Mattos, S. F., van der Horst, A., Klompmaker, R., Kops, G. J. P. L., Lam, E. W. ‐., Burgering, B. M. T., & Medema, R. H. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.22.7842-7852.2002 · Cited by 566 · see citing works
Acute mutation of retinoblastoma gene function is sufficient for cell cycle re-entry
Sage, J., Miller, A. L., Pérez-Mancera, P. A., Wysocki, J. M., & Jacks, T. (2003) · Nature · doi:10.1038/nature01764 · Cited by 538 · see citing works
p53 and E2f: partners in life and death
Polager, S., & Ginsberg, D. (2009) · Nature Reviews Cancer · doi:10.1038/nrc2718 · Cited by 498 · see citing works
Fibronectin, integrins, and growth control
Danen, E. H. J., & Yamada, K. M. (2001) · Journal of Cellular Physiology · doi:10.1002/jcp.1137 · Cited by 456 · see citing works
Control of Cell Cycle Exit and Entry by Protein Kinase B-Regulated Forkhead Transcription Factors
Kops, G. J. P. L., Medema, R. H., Glassford, J., Essers, M. A. G., Dijkers, P. F., Coffer, P. J., Lam, E. W. ‐., & Burgering, B. M. T. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.7.2025-2036.2002 · Cited by 442 · see citing works
CDK Activity Antagonizes Whi5, an Inhibitor of G1/S Transcription in Yeast
Costanzo, M., Nishikawa, J. L., Tang, X., Millman, J. S., Schub, O., Breitkreuz, K. E., Dewar, D., Rupeš, I., Andrews, B., & Tyers, M. (2004) · Cell · doi:10.1016/j.cell.2004.05.024 · Cited by 428 · see citing works
A revised picture of the E2F transcriptional network and RB function
Nolan-Stevaux, O., & Dyson, N. J. (2002) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(02)00388-5 · Cited by 423 · see citing works
A bistable Rb–E2F switch underlies the restriction point
Yao, G., Lee, T. J., Mori, S., Nevins, J. R., & You, L. (2008) · Nature Cell Biology · doi:10.1038/ncb1711 · Cited by 422 · see citing works
Loss of the Lkb1 tumour suppressor provokes intestinal polyposis but resistance to transformation
Bardeesy, N. M., Sinha, M., Hezel, A. F., Signoretti, S., Hathaway, N. A., Sharpless, N. E., Loda, M. F., Carrasco, D. R., & DePinho, R. A. (2002) · Nature · doi:10.1038/nature01045 · Cited by 418 · see citing works
Putting the stress on senescence
Serrano, M., & Blasco, M. A. (2001) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(00)00278-7 · Cited by 413 · see citing works
The DNA damage signaling pathway is a critical mediator of oncogene-induced senescence
Mallette, F. A., Gaumont-Leclerc, M.-F., & Ferbeyre, G. (2007) · Genes & Development · doi:10.1101/gad.1487307 · Cited by 406 · see citing works
Oncogene-Induced Cell Senescence — Halting on the Road to Cancer
Mooi, W. J., & Peeper, D. S. (2006) · New England Journal of Medicine · doi:10.1056/nejmra062285 · Cited by 371 · see citing works
Role of the RB1 family in stabilizing histone methylation at constitutive heterochromatin
Gonzalo, S., García-Cao, M., Fraga, M. F., Schotta, G., Peters, A. H. F. M., Cotter, S. E., Eguía, R., Dean, D. C., Esteller, M., Jenuwein, T., et al. (2005) · Nature Cell Biology · doi:10.1038/ncb1235 · Cited by 343 · see citing works
Mechanisms of cellular senescence in human and mouse cells.
Itahana, K., Campisi, J., & Dimri, G. P. (2004) · Biogerontology · doi:10.1023/b:bgen.0000017682.96395.10 · Cited by 338 · see citing works
Selective Evolution of Stromal Mesenchyme with p53 Loss in Response to Epithelial Tumorigenesis
Hill, R., Song, Y., Cardiff, R. D., & Van Dyke, T. (2005) · Cell · doi:10.1016/j.cell.2005.09.030 · Cited by 324 · see citing works
A Common Set of Gene Regulatory Networks Links Metabolism and Growth Inhibition
Cam, H., Balciunaite, E., Blais, A., Spektor, A., Scarpulla, R. C., Young, R., Kluger, Y., & Dynlacht, B. D. (2004) · Molecular Cell · doi:10.1016/j.molcel.2004.09.037 · Cited by 322 · see citing works
Transcriptional control at regulatory checkpoints by histone deacetylases: molecular connections between cancer and chromatin
Wade, P. A. (2001) · Human Molecular Genetics · doi:10.1093/hmg/10.7.693 · Cited by 319 · see citing works
Cell Cycle Control of Embryonic Stem Cells
White, J., & Dalton, S. (2005) · Stem Cell Reviews and Reports · doi:10.1385/scr:1:2:131 · Cited by 313 · see citing works
Mouse models for human lung cancerPreprint
Meuwissen, R. L. J., & Berns, A. J. M. (2005) · Genes & Development · doi:10.1101/gad.1284505 · Cited by 301 · see citing works
The genetics of the E2F family of transcription factors: shared functions and unique roles
DeGregori, J. V. (2002) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/s0304-419x(02)00051-3 · Cited by 295 · see citing works
p38 MAP Kinase's Emerging Role as a Tumor Suppressor
Bulavin, D. V., & Fornace, A. J. (2004) · Advances in cancer research · doi:10.1016/s0065-230x(04)92005-2 · Cited by 290 · see citing works
Pancreatic Cancer: Basic and Clinical Aspects
Schneider, G., Siveke, J. T., Eckel, F., & Schmid, R. M. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.04.001 · Cited by 285 · see citing works
Molecular stop signs: regulation of cell-cycle arrest by C/EBP transcription factors
Johnson, P. F. (2005) · Journal of Cell Science · doi:10.1242/jcs.02459 · Cited by 288 · see citing works
E2F mediates cell cycle-dependent transcriptional repression in vivo by recruitment of an HDAC1/mSin3B corepressor complex
Rayman, J. B., Takahashi, Y., Indjeian, V. B., Dannenberg, J.-H., Catchpole, S., Watson, R. J., te Riele, H., & Dynlacht, B. D. (2002) · Genes & Development · doi:10.1101/gad.969202 · Cited by 288 · see citing works
Self-citation
Retinoblastoma protein functions as a molecular switch determining white versus brown adipocyte differentiation
Hansen, J. B., Jørgensen, C., Petersen, R. K., Hallenborg, P., De Matteis, R., Bøye, H. A., Petrovic, N., Enerbäck, S., Nedergaard, J., Cinti, S., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0301964101 · Cited by 287 · see citing works
The retinoblastoma family of proteins and their regulatory functions in the mammalian cell division cycle
Henley, S. A., & Dick, F. A. (2012) · Cell Division · doi:10.1186/1747-1028-7-10 · Cited by 279 · see citing works
Id proteins in cell cycle control and cellular senescence
Zebedee, Z., & Hara, E. (2001) · Oncogene · doi:10.1038/sj.onc.1205092 · Cited by 277 · see citing works
The p16INK4a-RB pathway : molecular link between cellular senescence and tumor suppression
Ohtani, N., Yamakoshi, K., Takahashi, A., & Hara, E. (2004) · The Journal of Medical Investigation · doi:10.2152/jmi.51.146 · Cited by 276 · see citing works
THE CELL CYCLE AND MYC INTERSECT WITH MECHANISMS FOR PLURIPOTENCY AND REPROGRAMMING
Singh, A. M., & Dalton, S. (2009) · Cell Stem Cell · doi:10.1016/j.stem.2009.07.003 · Cited by 276 · see citing works
Mammalian SIRT1 limits replicative life span in response to chronic genotoxic stress
Chua, K. F., Mostoslavsky, R., Lombard, D. B., Pang, W. W., Saito, S., Franco, S., Kaushal, D., Cheng, H.-L., Fischer, M. R., Stokes, N., et al. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.06.007 · Cited by 257 · see citing works
Reversal of Senescence in Mouse Fibroblasts through Lentiviral Suppression of p53
Dirac, A. M. G., & Bernards, R. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.c300023200 · Cited by 254 · see citing works
Cell cycle transcription control: DREAM/MuvB and RB-E2F complexes.
Fischer, M., & Müller, G. A. (2017) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2017.1360836 · Cited by 255 · see citing works
Mechanisms by which DNA tumor virus oncoproteins target the Rb family of pocket proteins
Helt, A.-M. (2003) · Carcinogenesis · doi:10.1093/carcin/24.2.159 · Cited by 250 · see citing works
p107 and p130: Versatile Proteins with Interesting Pockets
Classon, M., & Dyson, N. J. (2001) · Experimental Cell Research · doi:10.1006/excr.2000.5135 · Cited by 237 · see citing works
G1 tetraploidy checkpoint and the suppression of tumorigenesis
Margolis, R. L., Lohez, O. D., & Andreassen, P. R. (2002) · Journal of Cellular Biochemistry · doi:10.1002/jcb.10411 · Cited by 231 · see citing works
Overlapping functions of Hdac1 and Hdac2 in cell cycle regulation and haematopoiesis
Wilting, R. H., Yanover, E., Heideman, M. R., Jacobs, H., Horner, J. W., van der Torre, J., DePinho, R. A., & Dannenberg, J. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.136 · Cited by 229 · see citing works
Self-citation
mSin3A corepressor regulates diverse transcriptional networks governing normal and neoplastic growth and survivalPreprint
Dannenberg, J., David, G., Zhong, S., van der Torre, J., Wong, W. H., & DePinho, R. A. (2005) · Genes & Development · doi:10.1101/gad.1286905 · Cited by 221 · see citing works
Self-citation
Control of glutamine metabolism by the tumor suppressor Rb
Reynolds, M. R., Lane, A. N., Robertson, B., Kemp, S., Liu, Y., Hill, B. G., Dean, D. C., & Clem, B. F. (2014) · Oncogene · doi:10.1038/onc.2012.635 · Cited by 216 · see citing works
Increasing cell size remodels the proteome and promotes senescence
Lanz, M. C., Zatulovskiy, E. A., Swaffer, M. P., Zhang, L., Ilerten, I., Zhang, S., You, D. S., Marinov, G. K., McAlpine, P. L., Elias, J. E., et al. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.07.017 · Cited by 218 · see citing works
Control of cell division by a retinoblastoma protein homolog in ChlamydomonasPreprint
Umen, J., & Goodenough, U. W. (2001) · Genes & Development · doi:10.1101/gad.892101 · Cited by 215 · see citing works
Tumour suppression by p53: the importance of apoptosis and cellular senescence
Zuckerman, V., Wolyniec, K., Sionov, R. V., Haupt, S., & Haupt, Y. (2009) · The Journal of Pathology · doi:10.1002/path.2584 · Cited by 210 · see citing works
Wide spectrum of tumors in knock‐in mice carrying a Cdk4 protein insensitive to INK4 inhibitors
Sotillo, R., Dubus, P., Martn, J., de la Cueva, E., Ortega, S., Malumbres, M., & Barbacid, M. (2001) · The EMBO Journal · doi:10.1093/emboj/20.23.6637 · Cited by 208 · see citing works
Understanding the limitations of radiation-induced cell cycle checkpoints
Deckbar, D., Jeggo, P. A., & Löbrich, M. (2011) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2011.575764 · Cited by 205 · see citing works
Mechanisms controlling cell cycle exit upon terminal differentiation
Buttitta, L., & Edgar, B. A. (2007) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2007.10.004 · Cited by 196 · see citing works
Inhibition of Pluripotency Networks by the Rb Tumor Suppressor Restricts Reprogramming and Tumorigenesis
Kareta, M. S., Gorges, L. L., Hafeez, S., Benayoun, B. A., Marro, S. G., Zmoos, A., Cecchini, M. J., Spacek, D. V., Batista, L. F. Z., O’Brien, M., et al. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.10.019 · Cited by 194 · see citing works
Multiple centrosomes arise from tetraploidy checkpoint failure and mitotic centrosome clusters in p53 and RB pocket protein-compromised cells
Borel, F., Lohez, O. D., Lacroix, F., & Margolis, R. L. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.152205299 · Cited by 193 · see citing works
Cell Cycle Features of Primate Embryonic Stem Cells
Fluckiger, A.-C., Marcy, G., Marchand, M., Négre, D., Cosset, F., Mitalipov, S. M., Wolf, D. P., Savatier, P., & Dehay, C. (2005) · Stem Cells · doi:10.1634/stemcells.2005-0194 · Cited by 186 · see citing works
Necessary and Sufficient Role for a Mitosis Skip in Senescence Induction
Johmura, Y., Shimada, M., Misaki, T., Naiki-Ito, A., Miyoshi, H., Motoyama, N., Ohtani, N., Hara, E., Nakamura, M., Morita, A., et al. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.05.003 · Cited by 182 · see citing works
Mad2 Is a Critical Mediator of the Chromosome Instability Observed upon Rb and p53 Pathway Inhibition
Schvartzman, J.-M., Duijf, P. H. G., Sotillo, R., Coker, C., & Benezra, R. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.04.017 · Cited by 181 · see citing works
Developmental Activation of the Rb–E2F Pathway and Establishment of Cell Cycle-regulated Cyclin-dependent Kinase Activity during Embryonic Stem Cell Differentiation
White, J., Stead, E., Faast, R., Conn, S. J., Cartwright, P., & Dalton, S. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-12-1056 · Cited by 173 · see citing works
Regulation of DNA Methyltransferase 1 by the pRb/E2F1 Pathway
McCabe, M. T., Davis, J. N., & Day, M. L. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-2158 · Cited by 172 · see citing works
G1 to S phase cell cycle transition in somatic and embryonic stem cells
Neganova, I. E., & Lako, M. (2008) · Journal of Anatomy · doi:10.1111/j.1469-7580.2008.00931.x · Cited by 172 · see citing works
Cell growth dilutes the cell cycle inhibitor Rb to trigger cell division
Zatulovskiy, E. A., Zhang, S., Berenson, D. F., Topacio, B. R., & Skotheim, J. M. (2020) · Science · doi:10.1126/science.aaz6213 · Cited by 164 · see citing works
Germ Line Transmission of the Cdk4R24C Mutation Facilitates Tumorigenesis and Escape from Cellular Senescence
Rane, S. G., Cosenza, S. C., Mettus, R. V., & Reddy, E. P. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.2.644-656.2002 · Cited by 167 · see citing works
The retinoblastoma tumor-suppressor gene, the exception that proves the rule
Goodrich, D. W. (2006) · Oncogene · doi:10.1038/sj.onc.1209616 · Cited by 166 · see citing works
Modelling mammalian cellular quiescence
Yao, G. (2014) · Interface Focus · doi:10.1098/rsfs.2013.0074 · Cited by 160 · see citing works
Large T Antigens of Polyomaviruses: Amazing Molecular Machines
An, P., Robles, M. T. S., & Pipas, J. M. (2012) · Annual Review of Microbiology · doi:10.1146/annurev-micro-092611-150154 · Cited by 158 · see citing works
TBX-3, the Gene Mutated in Ulnar-Mammary Syndrome, Is a Negative Regulator of p19 and Inhibits Senescence
Brummelkamp, T. R., Kortlever, R. M., Lingbeek, M., Trettel, F., MacDonald, M. E., van Lohuizen, M., & Bernards, R. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m110492200 · Cited by 154 · see citing works
Cell cycle in mouse development
Ciemerych, M. A., & Siciński, P. (2005) · Oncogene · doi:10.1038/sj.onc.1208608 · Cited by 150 · see citing works
C/EBPβ cooperates with RB:E2F to implement RasV12‐induced cellular senescence
Sebastian, T. B., Malı́k, R., Thomas, S., Sage, J., & Johnson, P. F. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600789 · Cited by 147 · see citing works
Unique and overlapping functions of pRb and p107 in the control of proliferation and differentiation in epidermis
Ruiz, S., Santos, M., Segrelles, C., Leis, H., Jorcano, J. L., Berns, A., Paramio, J. M., & Vooijs, M. (2004) · Development · doi:10.1242/dev.01148 · Cited by 147 · see citing works
Retinoblastoma family genes
Du, W., & Pogoriler, J. E. (2006) · Oncogene · doi:10.1038/sj.onc.1209651 · Cited by 145 · see citing works
Evolution of networks and sequences in eukaryotic cell cycle control
Cross, F. R., Buchler, N. E. G., & Skotheim, J. M. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0078 · Cited by 144 · see citing works
Cdk4 disruption renders primary mouse cells resistant to oncogenic transformation, leading to Arf/p53-independent senescencePreprint
Zou, X., Ray, D., Aziyu, A., Christov, K. T., Boiko, A. D., Gudkov, A. V., & Kiyokawa, H. (2002) · Genes & Development · doi:10.1101/gad.1033002 · Cited by 143 · see citing works
Cdk4 and Cdk6 Couple the Cell-Cycle Machinery to Cell Growth via mTORC1
Romero‐Pozuelo, J., Figlia, G., Kaya, O., Martín-Villalba, A., & Teleman, A. A. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.03.068 · Cited by 137 · see citing works
A senescence rescue screen identifies BCL6 as an inhibitor of anti-proliferative p19 ARF –p53 signalingPreprint
Shvarts, A., Brummelkamp, T. R., Scheeren, F., Koh, E., Daley, G. Q., Spits, H., & Bernards, R. (2002) · Genes & Development · doi:10.1101/gad.929302 · Cited by 142 · see citing works
Concise Review: Control of Cell Fate Through Cell Cycle and Pluripotency Networks
Boward, B., Wu, T., & Dalton, S. (2016) · Stem Cells · doi:10.1002/stem.2345 · Cited by 132 · see citing works
Tissue-specific tumor suppressor activity of retinoblastoma gene homologs p107 and p130
Dannenberg, J.-H., Schuijff, L., Dekker, M., van der Valk, M., & Riele, H. T. (2004) · Genes & Development · doi:10.1101/gad.322004 · Cited by 137 · see citing works
Self-citation
Update on Human Polyomaviruses and Cancer
Gjoerup, O. V., & Chang, Y. (2010) · Advances in cancer research · doi:10.1016/s0065-230x(10)06001-x · Cited by 137 · see citing works
To cell cycle, swing the APC/C
van Leuken, R. J., Clijsters, L., & Wolthuis, R. M. F. (2008) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2008.05.002 · Cited by 131 · see citing works
Rb family proteins as modulators of gene expression and new aspects regarding the interaction with chromatin remodeling enzymes
Macaluso, M., Montanari, M., & Giordano, A. (2006) · Oncogene · doi:10.1038/sj.onc.1209680 · Cited by 130 · see citing works
Co-repressor, co-activator and general transcription factor: the many faces of the Sin3 histone deacetylase (HDAC) complex
Adams, G. E., Chandru, A., & Cowley, S. M. (2018) · Biochemical Journal · doi:10.1042/bcj20170314 · Cited by 123 · see citing works
The Retinoblastoma Protein Regulates Pericentric Heterochromatin
Isaac, C. E., Francis, S. M., Martens, A. L., Julian, L. M., Seifried, L. A., Erdmann, N., Binné, U. K., Harrington, L., Sicinski, P., Bérubé, N. G., et al. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.26.9.3659-3671.2006 · Cited by 128 · see citing works
Senescence-Associated Secretory Phenotype and Its Possible Role in Chronic Obstructive Pulmonary Disease
Kumar, M., Seeger, W., & Voswinckel, R. (2014) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2013-0382ps · Cited by 129 · see citing works
Keeping things quiet: Roles of NuRD and Sin3 co-repressor complexes during mammalian development
McDonel, P. E., Costello, I., & Hendrich, B. (2008) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2008.07.022 · Cited by 127 · see citing works
Origin of bistability underlying mammalian cell cycle entry
Yao, G., Tan, C., West, M., Nevins, J. R., & You, L. (2011) · Molecular Systems Biology · doi:10.1038/msb.2011.19 · Cited by 124 · see citing works
The DNA Damage Signaling Pathway Connects Oncogenic Stress to Cellular Senescence
Mallette, F. A., & Ferbeyre, G. (2007) · Cell Cycle · doi:10.4161/cc.6.15.4516 · Cited by 125 · see citing works

Targeted disruption of the three Rb-related genes leads to loss of G 1 control and immortalization
Sage, J., Mulligan, G. J., Attardi, L. D., Miller, A., Chen, S., Williams, B., Theodorou, E., & Jacks, T. (2000) · Genes & Development · doi:10.1101/gad.843200 · Cited by 582 · see citing works
In Brief
(2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35048044
The retinoblastoma gene: role in cell cycle control and cell differentiation
Wiman, K. G. (1993) · The FASEB Journal · doi:10.1096/fasebj.7.10.8393817 · Cited by 136 · see citing works
Functional linkage of Retinoblastoma protein family turnover and potency during mouse embryonic stem cell development
Henry, R. W., Arnosti, D. N., Knott, J. G., & Sengupta, S. (2012) · The FASEB Journal · doi:10.1096/fasebj.26.1_supplement.922.14
ORIGINAL ARTICLE The Retinoblastoma Protein and Its Homolog p130 Regulate the G 1/S Transition in Pancreatic �-Cells
Harb, G., Vasavada, R. C., Cobrinik, D. E., & Stewart, A. F. (2013)

Authors: Dannenberg, J.-H., van Rossum, A., Schuijff, L., & te Riele, H.
Affiliations: The Netherlands Cancer Institute (NL)
Venue: Genes & Development
Publisher: Cold Spring Harbor Laboratory
Published: 2000-12-01
Volume: 14
Issue: 23
Pages: 3051-3064
ISSN: 0890-9369 (ISSN-L)
1549-5477
DOI: 10.1101/gad.847700
PMC: PMC317114
OpenAlex: W2001004678
Cited by: 413
References: 96
Citations by year: 2026: 1 · 2025: 1 · 2024: 5 · 2023: 8 · 2022: 6 · 2021: 8 · 2020: 12 · 2019: 3 · 2018: 12 · 2017: 8 · 2016: 9 · 2015: 10 · 2014: 11 · 2013: 21 · 2012: 17
Type: posted content
Language: en
Open access: bronze
doi.org
Locations: Genes & Development (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
Keywords: retinoblastoma protein, p107, p130, pocket proteins, cellular senescence, cell immortalization, cell turnover, embryonic stem cells, mouse embryonic fibroblasts, differentiation capacity, loss-of-function mutations, tumor suppression
MeSH terms: Animals, Cell Adhesion, Cell Differentiation, Cell Division, Cell Line, Mice, Inbred C57BL, Mice, Nude, Nuclear Proteins, Phosphoproteins, Proteins, Stem Cells, Tumor Suppressor Protein p53, Retinoblastoma Protein, G1 Phase, Teratocarcinoma, Mice, Knockout, Tumor Suppressor Protein p14ARF, Retinoblastoma-Like Protein p130, Retinoblastoma-Like Protein p107, Mice

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Ablation of the Retinoblastoma gene family deregulates G1 control causing immortalization and increased cell turnover under growth-restricting conditions

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