Online citations, reference lists, and bibliographies.
Please confirm you are human
(Sign Up for free to never see this)
← Back to Search

Cyclin F Controls Cell-Cycle Transcriptional Outputs By Directing The Degradation Of The Three Activator E2Fs.

L. Clijsters, Claire Hoencamp, Jorg J. A. Calis, Antonio Marzio, Shanna M Handgraaf, M. Cuitiño, B. Rosenberg, G. Leone, M. Pagano
Published 2019 · Biology, Medicine

Save to my Library
Download PDF
Analyze on Scholarcy
Share
E2F1, E2F2, and E2F3A, the three activators of the E2F family of transcription factors, are key regulators of the G1/S transition, promoting transcription of hundreds of genes critical for cell-cycle progression. We found that during late S and in G2, the degradation of all three activator E2Fs is controlled by cyclin F, the substrate receptor of 1 of 69 human SCF ubiquitin ligase complexes. E2F1, E2F2, and E2F3A interact with the cyclin box of cyclin F via their conserved N-terminal cyclin binding motifs. In the short term, E2F mutants unable to bind cyclin F remain stable throughout the cell cycle, induce unscheduled transcription in G2 and mitosis, and promote faster entry into the next S phase. However, in the long term, they impair cell fitness. We propose that by restricting E2F activity to the S phase, cyclin F controls one of the main and most critical transcriptional engines of the cell cycle.
This paper references
10.1038/ncomms10530
SCFCyclin F-dependent degradation of CDC6 suppresses DNA re-replication
D. Walter (2016)
10.1038/nrm4002
DNA replication origin activation in space and time
Michalis Fragkos (2015)
10.1016/j.tcb.2012.10.011
A cyclin without cyclin-dependent kinases: cyclin F controls genome stability through ubiquitin-mediated proteolysis.
Vincenzo D’Angiolella (2013)
10.1111/J.2517-6161.1995.TB02031.X
Controlling the false discovery rate: a practical and powerful approach to multiple testing
Y. Benjamini (1995)
10.1016/0092-8674(94)90582-7
Negative regulation of the growth-promoting transcription factor E2F-1 by a stably bound cyclin A-dependent protein kinase
W. Krek (1994)
10.4161/cc.9.19.13300
Coordinate regulation of histone mRNA metabolism and DNA replication
M. M. Koseoglu (2010)
10.1126/SCIENCE.1312258
Association of cdk2 kinase with the transcription factor E2F during S phase.
M. Pagano (1992)
10.1101/GAD.6.2.177
The interaction of RB with E2F coincides with an inhibition of the transcriptional activity of E2F.
S. Hiebert (1992)
10.1038/nrm3582
Mechanisms and function of substrate recruitment by F-box proteins
J. Skaar (2013)
10.1016/j.cell.2011.09.019
Global Identification of Modular Cullin-RING Ligase Substrates
Michael J. Emanuele (2011)
10.4161/cc.20402
APC/CCdh1 controls the proteasome-mediated degradation of E2F3 during cell cycle exit
Zhen Ping (2012)
10.1016/j.celrep.2019.05.004
Two Distinct E2F Transcriptional Modules Drive Cell Cycles and Differentiation.
M. Cuitiño (2019)
10.1016/j.biocel.2016.02.005
Ubiquitination-mediated degradation of cell cycle-related proteins by F-box proteins.
Nana Zheng (2016)
10.1038/nrm3567
Molecular mechanisms underlying RB protein function
F. Dick (2013)
10.1073/PNAS.90.15.6914
E2F-1-mediated transactivation is inhibited by complex formation with the retinoblastoma susceptibility gene product.
E. Flemington (1993)
10.14806/EJ.17.1.200
Cutadapt removes adapter sequences from high-throughput sequencing reads
M. Martin (2011)
10.1016/j.molcel.2015.05.006
Quantitative Proteomic Atlas of Ubiquitination and Acetylation in the DNA Damage Response.
A. E. Elia (2015)
10.1038/onc.2012.387
Increased replication initiation and conflicts with transcription underlie Cyclin E-induced replication stress
R. Jones (2013)
10.1093/bioinformatics/btu638
HTSeq—a Python framework to work with high-throughput sequencing data
S. Anders (2015)
10.1093/nar/gks461
Camera: a competitive gene set test accounting for inter-gene correlation
D. Wu (2012)
10.1038/onc.2011.550
A p27Kip1 mutant that does not inhibit CDK activity promotes centrosome amplification and micronucleation
S. S. Sharma (2012)
10.1093/nar/gkv007
limma powers differential expression analyses for RNA-sequencing and microarray studies
M. Ritchie (2015)
10.1126/science.aal4671
Mitotic transcription and waves of gene reactivation during mitotic exit
Katherine C. Palozola (2017)
10.1038/nature09140
SCFCyclin F controls centrosome homeostasis and mitotic fidelity via CP110 degradation
Vincenzo D’Angiolella (2010)
10.1016/j.celrep.2017.08.099
The E3 Ubiquitin Ligase SCF(Cyclin F) Transmits AKT Signaling to the Cell-Cycle Machinery.
Rajarshi Choudhury (2017)
10.1093/bioinformatics/bts635
STAR: ultrafast universal RNA-seq aligner
Alexander Dobin (2013)
10.1002/j.1460-2075.1993.tb06116.x
Functional synergy between DP‐1 and E2F‐1 in the cell cycle‐regulating transcription factor DRTF1/E2F.
L. R. Bandara (1993)
10.1016/j.molcel.2016.09.010
Cyclin F-Mediated Degradation of SLBP Limits H2A.X Accumulation and Apoptosis upon Genotoxic Stress in G2.
John F Dankert (2016)
10.1186/s13059-014-0550-8
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
M. Love (2014)
10.1093/bioinformatics/btp616
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data
M. Robinson (2010)
10.1038/nmeth.1318
Enzymatic assembly of DNA molecules up to several hundred kilobases
D. Gibson (2009)
10.4161/cc.9.19.13162
APC/CCdc20 targets E2F1 for degradation in prometaphase
M. Peart (2010)
10.1101/GAD.864201
E2Fs regulate the expression of genes involved in differentiation, development, proliferation, and apoptosis.
H. Mueller (2001)
10.7554/eLife.30473
Rapid DNA replication origin licensing protects stem cell pluripotency
J. Matson (2017)
10.1038/nbt.2931
Normalization of RNA-seq data using factor analysis of control genes or samples
D. Risso (2014)
10.1128/MCB.13.10.6501
Inhibition of E2F-1 transactivation by direct binding of the retinoblastoma protein.
K. Helin (1993)
10.1101/GAD.949802
E2F integrates cell cycle progression with DNA repair, replication, and G(2)/M checkpoints.
B. Ren (2002)
10.12688/f1000research.8987.2
From reads to genes to pathways: differential expression analysis of RNA-Seq experiments using Rsubread and the edgeR quasi-likelihood pipeline
Y. Chen (2016)
10.1016/0092-8674(91)90019-U
Cell cycle regulation of the E2F transcription factor involves an interaction with cyclin A
M. Mudryj (1991)
10.1038/nrm3629
Control of cell cycle transcription during G1 and S phases
C. Bertoli (2013)
10.1073/pnas.0506580102
Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles
Aravind Subramanian (2005)
10.1038/nature25507
Intragenic origins due to short G1 phases underlie oncogene-induced DNA replication stress
Morgane Macheret (2018)
10.1038/ncomms6800
Cyclin F suppresses B-Myb activity to promote cell cycle checkpoint control.
D. K. Klein (2015)
10.1016/j.redox.2013.12.020
OpenComet: An automated tool for comet assay image analysis
Benjamin M. Gyori (2014)
10.1016/j.devcel.2007.10.017
Synergistic function of E2F7 and E2F8 is essential for cell survival and embryonic development.
J. Li (2008)
10.1038/nature02082
Degradation of Cdc25A by β-TrCP during S phase and in response to DNA damage
L. Busino (2003)
10.1002/j.1460-2075.1994.tb06955.x
Human cyclin F.
C. Bai (1994)
10.1371/journal.pone.0001487
Genome-Wide and Functional Annotation of Human E3 Ubiquitin Ligases Identifies MULAN, a Mitochondrial E3 that Regulates the Organelle's Dynamics and Signaling
Wei Li (2008)
10.1242/jcs.145862
PIP-box-mediated degradation prohibits re-accumulation of Cdc6 during S phase
Linda Clijsters (2014)
10.18632/oncotarget.13636
CDH1 regulates E2F1 degradation in response to differentiation signals in keratinocytes
Randeep K. Singh (2017)
10.1101/GAD.8.15.1772
Differential regulation of E2F transactivation by cyclin/cdk2 complexes.
B. Dynlacht (1994)
10.1016/0092-8674(91)90558-G
The retinoblastoma protein copurifies with E2F-I, an E1A-regulated inhibitor of the transcription factor E2F
S. Bagchi (1991)
10.1101/GAD.14.7.804
Analysis of promoter binding by the E2F and pRB families in vivo: distinct E2F proteins mediate activation and repression.
Y. Takahashi (2000)
10.1016/J.MOLCEL.2006.03.017
Stabilizers and destabilizers controlling cell cycle oscillators.
D. Guardavaccaro (2006)
10.1016/j.celrep.2018.08.076
β-TrCP- and Casein Kinase II-Mediated Degradation of Cyclin F Controls Timely Mitotic Progression
I. Mavrommati (2018)
10.1038/nrm2469
Conserved functions of the pRB and E2F families
S. Heuvel (2008)
10.1371/journal.ppat.1003358
Colocalization of Different Influenza Viral RNA Segments in the Cytoplasm before Viral Budding as Shown by Single-molecule Sensitivity FISH Analysis
Yi-Ying Chou (2013)
10.1016/j.cell.2012.03.043
Cyclin F-Mediated Degradation of Ribonucleotide Reductase M2 Controls Genome Integrity and DNA Repair
Vincenzo D’Angiolella (2012)
10.1083/jcb.201209002
FBH1 promotes DNA double-strand breakage and apoptosis in response to DNA replication stress
Yeon-Tae Jeong (2013)
10.1038/8984
Interaction between ubiquitin–protein ligase SCFSKP2 and E2F-1 underlies the regulation of E2F-1 degradation
A. Marti (1999)
10.1093/nar/gkr1203
E2F7 represses a network of oscillating cell cycle genes to control S-phase progression
B. Westendorp (2012)
10.1093/bioinformatics/btr260
Molecular signatures database (MSigDB) 3.0
A. Liberzon (2011)



This paper is referenced by
10.1083/jcb.201909032
DNA replication and mitotic entry: A brake model for cell cycle progression
Bennie Lemmens (2019)
10.15252/embj.2018101443
E2F1 proteolysis via SCF‐cyclin F underlies synthetic lethality between cyclin F loss and Chk1 inhibition
K. Burdová (2019)
10.1038/s41418-020-00648-0
Ubiquitin signaling in cell cycle control and tumorigenesis.
Fabin Dang (2020)
10.1016/j.yexcr.2020.112212
Cyclin F and KIF20A, FOXM1 target genes, increase proliferation and invasion of ovarian cancer cells.
Yingwei Li (2020)
10.3390/ijms21082662
Pisum sativum Defensin 1 Eradicates Mouse Metastatic Lung Nodules from B16F10 Melanoma Cells
Virgínia Amaral (2020)
10.1016/j.celrep.2019.05.004
Two Distinct E2F Transcriptional Modules Drive Cell Cycles and Differentiation.
M. Cuitiño (2019)
10.1101/672964
Cell cycle oscillators underlying orderly proteolysis of E2F8
D. Wasserman (2019)
10.1038/s41598-020-61087-y
Cryptochromes modulate E2F family transcription factors
Alanna B Chan (2020)
10.1101/2020.11.17.385716
Cyclin D3 drives inertial cell cycling in dark zone germinal center B cells
Juhee Pae (2020)
10.1093/nar/gkaa1002
A unified model for the G1/S cell cycle transition
S. Hume (2020)
10.1016/j.canlet.2020.04.002
ETV4 is a theranostic target in clear cell renal cell carcinoma that promotes metastasis by activating the pro-metastatic gene FOSL1 in a PI3K-AKT dependent manner.
L. Xu (2020)
10.1038/s12276-020-00508-4
Regulation of cell cycle drivers by Cullin-RING ubiquitin ligases.
Sang-Min Jang (2020)
10.15252/embj.2019103421
E2F transcription regulation: an orphan cyclin enters the stage
Heike I Rösner (2019)
10.1093/hmg/ddz119
Pathogenic mutations in the ALS gene CCNF cause cytoplasmic mislocalization of Cyclin F and elevated VCP ATPase activity.
Yujiao Yu (2019)
10.3390/cancers12051249
F-Box Proteins and Cancer
Kanae Yumimoto (2020)
10.1091/mbc.E19-12-0725
Cell cycle oscillators underlying orderly proteolysis of E2F8
D. Wasserman (2020)
10.15252/embj.2018101430
Cyclin F‐dependent degradation of E2F7 is critical for DNA repair and G2‐phase progression
Ruixue Yuan (2019)
10.1038/s41568-019-0143-7
The broken cycle: E2F dysfunction in cancer
L. Kent (2019)
10.1016/j.tcb.2020.05.002
Complex Cartography: Regulation of E2F Transcription Factors by Cyclin F and Ubiquitin.
Michael J. Emanuele (2020)
Semantic Scholar Logo Some data provided by SemanticScholar