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Research Article

Interchangeable Roles for E2F Transcriptional Repression by the Retinoblastoma Protein and p27KIP1–Cyclin-Dependent Kinase Regulation in Cell Cycle Control and Tumor Suppression

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Article: e00561-16 | Received 11 Oct 2016, Accepted 01 Nov 2016, Published online: 17 Mar 2023

REFERENCES

  • Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell 144:646–674. https://doi.org/10.1016/j.cell.2011.02.013.
  • Coller HA. 2007. What's taking so long? S-phase entry from quiescence versus proliferation. Nat Rev Mol Cell Biol 8:667–670.
  • Dick FA, Rubin SM. 2013. Molecular mechanisms underlying RB protein function. Nat Rev Mol Cell Biol 14:297–306. https://doi.org/10.1038/nrm3567.
  • Bertoli C, Skotheim JM, de Bruin RA. 2013. Control of cell cycle transcription during G1 and S phases. Nat Rev Mol Cell Biol 14:518–528. https://doi.org/10.1038/nrm3629.
  • Deshpande A, Sicinski P, Hinds PW. 2005. Cyclins and cdks in development and cancer: a perspective. Oncogene 24:2909–2915. https://doi.org/10.1038/sj.onc.1208618.
  • Hydbring P, Malumbres M, Sicinski P. 2016. Non-canonical functions of cell cycle cyclins and cyclin-dependent kinases. Nat Rev Mol Cell Biol 17:280–292. https://doi.org/10.1038/nrm.2016.27.
  • Sherr CJ, McCormick F. 2002. The RB and p53 pathways in cancer. Cancer Cell 2:103–112. https://doi.org/10.1016/S1535-6108(02)00102-2.
  • Vervoorts J, Luscher B. 2008. Post-translational regulation of the tumor suppressor p27(KIP1). Cell Mol Life Sci 65:3255–3264. https://doi.org/10.1007/s00018-008-8296-7.
  • Besson A, Gurian-West M, Chen X, Kelly-Spratt KS, Kemp CJ, Roberts JM. 2006. A pathway in quiescent cells that controls p27Kip1 stability, subcellular localization, and tumor suppression. Genes Dev 20:47–64. https://doi.org/10.1101/gad.1384406.
  • Malek NP, Sundberg H, McGrew S, Nakayama K, Kyriakides TR, Roberts JM. 2001. A mouse knock-in model exposes sequential proteolytic pathways that regulate p27Kip1 in G1 and S phase. Nature 413:323–327. https://doi.org/10.1038/35095083.
  • Coats S, Flanagan WM, Nourse J, Roberts JM. 1996. Requirement of p27Kip1 for restriction point control of the fibroblast cell cycle. Science 272:877–880. https://doi.org/10.1126/science.272.5263.877.
  • Georgia S, Bhushan A. 2006. p27 regulates the transition of beta-cells from quiescence to proliferation. Diabetes 55:2950–2956. https://doi.org/10.2337/db06-0249.
  • Kossatz U, Dietrich N, Zender L, Buer J, Manns MP, Malek NP. 2004. Skp2-dependent degradation of p27kip1 is essential for cell cycle progression. Genes Dev 18:2602–2607. https://doi.org/10.1101/gad.321004.
  • Sutterluty H, Chatelain E, Marti A, Wirbelauer C, Senften M, Muller U, Krek W. 1999. p45SKP2 promotes p27Kip1 degradation and induces S phase in quiescent cells. Nat Cell Biol 1:207–214. https://doi.org/10.1038/12027.
  • Viatour P, Somervaille TC, Venkatasubrahmanyam S, Kogan S, McLaughlin ME, Weissman IL, Butte AJ, Passegue E, Sage J. 2008. Hematopoietic stem cell quiescence is maintained by compound contributions of the retinoblastoma gene family. Cell Stem Cell 3:416–428. https://doi.org/10.1016/j.stem.2008.07.009.
  • Mason-Richie NA, Mistry MJ, Gettler CA, Elayyadi A, Wikenheiser-Brokamp KA. 2008. Retinoblastoma function is essential for establishing lung epithelial quiescence after injury. Cancer Res 68:4068–4076. https://doi.org/10.1158/0008-5472.CAN-07-5667.
  • Mayhew CN, Bosco EE, Fox SR, Okaya T, Tarapore P, Schwemberger SJ, Babcock GF, Lentsch AB, Fukasawa K, Knudsen ES. 2005. Liver-specific pRB loss results in ectopic cell cycle entry and aberrant ploidy. Cancer Res 65:4568–4577. https://doi.org/10.1158/0008-5472.CAN-04-4221.
  • Dyson N. 1998. The regulation of E2F by pRB-family proteins. Genes Dev 12:2245–2262. https://doi.org/10.1101/gad.12.15.2245.
  • Qin XQ, Chittenden T, Livingston DM, Kaelin WG, Jr. 1992. Identification of a growth suppression domain within the retinoblastoma gene product. Genes Dev 6:953–964. https://doi.org/10.1101/gad.6.6.953.
  • Hiebert SW, Chellappan SP, Horowitz JM, Nevins JR. 1992. The interaction of RB with E2F coincides with an inhibition of the transcriptional activity of E2F. Genes Dev 6:177–185. https://doi.org/10.1101/gad.6.2.177.
  • Qin X-Q, Livingston DM, Ewen M, Sellers WR, Arany Z, Kaelin WG. 1995. The transcription factor E2F-1 is a downstream target of RB action. Mol Cell Biol 15:742–755. https://doi.org/10.1128/MCB.15.2.742.
  • Otterson GA, Chen W, Coxon AB, Khleif SN, Kaye FJ. 1997. Incomplete penetrance of familial retinoblastoma linked to germ-line mutations that result in partial loss of RB function. Proc Natl Acad Sci U S A 94:12036–12040. https://doi.org/10.1073/pnas.94.22.12036.
  • Sellers WR, Novitch BG, Miyake S, Heith A, Otterson GA, Kaye FJ, Lassar AB, Kaelin WG, Jr. 1998. Stable binding to E2F is not required for the retinoblastoma protein to activate transcription, promote differentiation, and suppress tumor cell growth. Genes Dev 12:95–106. https://doi.org/10.1101/gad.12.1.95.
  • Whitaker LL, Su H, Baskaran R, Knudsen ES, Wang JY. 1998. Growth suppression by an E2F-binding-defective retinoblastoma protein (RB): contribution from the RB C pocket. Mol Cell Biol 18:4032–4042. https://doi.org/10.1128/MCB.18.7.4032.
  • Binne UK, Classon MK, Dick FA, Wei W, Rape M, Kaelin WG, Jr, Naar AM, Dyson NJ. 2007. Retinoblastoma protein and anaphase-promoting complex physically interact and functionally cooperate during cell-cycle exit. Nat Cell Biol 9:225–232. https://doi.org/10.1038/ncb1532.
  • Ji P, Jiang H, Rekhtman K, Bloom J, Ichetovkin M, Pagano M, Zhu L. 2004. An Rb-Skp2-p27 pathway mediates acute cell cycle inhibition by Rb and is retained in a partial-penetrance Rb mutant. Mol Cell 16:47–58. https://doi.org/10.1016/j.molcel.2004.09.029.
  • Alexander K, Hinds PW. 2001. Requirement for p27(KIP1) in retinoblastoma protein-mediated senescence. Mol Cell Biol 21:3616–3631. https://doi.org/10.1128/MCB.21.11.3616-3631.2001.
  • Wang H, Bauzon F, Ji P, Xu X, Sun D, Locker J, Sellers RS, Nakayama K, Nakayama KI, Cobrinik D, Zhu L. 2010. Skp2 is required for survival of aberrantly proliferating Rb1-deficient cells and for tumorigenesis in Rb1+/− mice. Nat Genet 42:83–88. https://doi.org/10.1038/ng.498.
  • Zhao H, Bauzon F, Fu H, Lu Z, Cui J, Nakayama K, Nakayama KI, Locker J, Zhu L. 2013. Skp2 deletion unmasks a p27 safeguard that blocks tumorigenesis in the absence of pRb and p53 tumor suppressors. Cancer Cell 24:645–659. https://doi.org/10.1016/j.ccr.2013.09.021.
  • Cecchini MJ, Thwaites M, Talluri S, Macdonald JI, Passos DT, Chong JL, Cantalupo P, Stafford P, Saenz-Robles MT, Francis SM, Pipas JM, Leone G, Welch I, Dick FA. 2014. A retinoblastoma allele that is mutated at its common E2F interaction site inhibits cell proliferation in gene targeted mice. Mol Cell Biol 34:2029–2045. https://doi.org/10.1128/MCB.01589-13.
  • Park MS, Rosai J, Nguyen HT, Capodieci P, Cordon-Cardo C, Koff A. 1999. p27 and Rb are on overlapping pathways suppressing tumorigenesis in mice. Proc Natl Acad Sci U S A 96:6382–6387. https://doi.org/10.1073/pnas.96.11.6382.
  • Buttitta LA, Edgar BA. 2007. Mechanisms controlling cell cycle exit upon terminal differentiation. Curr Opin Cell Biol 19:697–704. https://doi.org/10.1016/j.ceb.2007.10.004.
  • Busuttil RA, Rubio M, Dolle ME, Campisi J, Vijg J. 2003. Oxygen accelerates the accumulation of mutations during the senescence and immortalization of murine cells in culture. Aging Cell 2:287–294. https://doi.org/10.1046/j.1474-9728.2003.00066.x.
  • Williams BO, Remington L, Albert DM, Mukai S, Bronson RT, Jacks T. 1994. Cooperative tumorigenic effects of germline mutations in Rb and p53. Nat Genet 7:480–484. https://doi.org/10.1038/ng0894-480.
  • Harrison DJ, Hooper ML, Armstrong JF, Clarke AR. 1995. Effects of heterozygosity for the Rb-1t19neo allele in the mouse. Oncogene 10:1615–1620.
  • Bilodeau S, Roussel-Gervais A, Drouin J. 2009. Distinct developmental roles of cell cycle inhibitors p57Kip2 and p27Kip1 distinguish pituitary progenitor cell cycle exit from cell cycle reentry of differentiated cells. Mol Cell Biol 29:1895–1908. https://doi.org/10.1128/MCB.01885-08.
  • Cobrinik D. 2005. Pocket proteins and cell cycle control. Oncogene 24:2796–2809. https://doi.org/10.1038/sj.onc.1208619.
  • Morris EJ, Dyson NJ. 2001. Retinoblastoma protein partners. Adv Cancer Res 82:1–54. https://doi.org/10.1016/S0065-230X(01)82001-7.
  • Finn RS, Dering J, Conklin D, Kalous O, Cohen DJ, Desai AJ, Ginther C, Atefi M, Chen I, Fowst C, Los G, Slamon DJ. 2009. PD 0332991, a selective cyclin D kinase 4/6 inhibitor, preferentially inhibits proliferation of luminal estrogen receptor-positive human breast cancer cell lines in vitro. Breast Cancer Res 11:R77. https://doi.org/10.1186/bcr2419.
  • Rader J, Russell MR, Hart LS, Nakazawa MS, Belcastro LT, Martinez D, Li Y, Carpenter EL, Attiyeh EF, Diskin SJ, Kim S, Parasuraman S, Caponigro G, Schnepp RW, Wood AC, Pawel B, Cole KA, Maris JM. 2013. Dual CDK4/CDK6 inhibition induces cell-cycle arrest and senescence in neuroblastoma. Clin Cancer Res 19:6173–6182. https://doi.org/10.1158/1078-0432.CCR-13-1675.
  • Gelbert LM, Cai S, Lin X, Sanchez-Martinez C, Del Prado M, Lallena MJ, Torres R, Ajamie RT, Wishart GN, Flack RS, Neubauer BL, Young J, Chan EM, Iversen P, Cronier D, Kreklau E, de Dios A. 2014. Preclinical characterization of the CDK4/6 inhibitor LY2835219: in-vivo cell cycle-dependent/independent anti-tumor activities alone/in combination with gemcitabine. Investig New Drugs 32:825–837. https://doi.org/10.1007/s10637-014-0120-7.
  • Cadoo KA, Gucalp A, Traina TA. 2014. Palbociclib: an evidence-based review of its potential in the treatment of breast cancer. Breast Cancer (Dove Med Press) 6:123–133.
  • Cecchini MJ, Amiri M, Dick FA. 2012. Analysis of cell cycle position in mammalian cells. J Vis Exp 59:e3491.
  • Thwaites MJ, Cecchini MJ, Dick FA. 2014. Analyzing RB and E2F during the G1-S transition. Methods Mol Biol 1170:449–461. https://doi.org/10.1007/978-1-4939-0888-2_24.
  • Fero ML, Rivkin M, Tasch M, Porter P, Carow CE, Firpo E, Polyak K, Tsai LH, Broudy V, Perlmutter RM, Kaushansky K, Roberts JM. 1996. A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27(Kip1)-deficient mice. Cell 85:733–744. https://doi.org/10.1016/S0092-8674(00)81239-8.
  • Ritchie K, Watson LA, Davidson B, Jiang Y, Berube NG. 2014. ATRX is required for maintenance of the neuroprogenitor cell pool in the embryonic mouse brain. Biol Open 3:1158–1163. https://doi.org/10.1242/bio.20148730.

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