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Atypical E2F activity restrains APC/C-CCS52A2 function obligatory for endocycle onset

Tim Lammens UGent, Véronique Boudolf UGent, Leila Kheibarshekan Asl UGent, L Panagiotis Zalmas, Tarik Gaamouche UGent, Sara Maes UGent, Marleen Vanstraelen, Eva Kondorosi, Nicholas B La Thangue and Willy Govaerts UGent, et al. (2008) PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 105(38). p.14721-14726
abstract
The endocycle represents an alternative cell cycle that is activated in various developmental processes, including placental formation, Drosophila oogenesis, and leaf development. In endocycling cells, mitotic cell cycle exit is followed by successive doublings of the DNA content, resulting in polyploidy. The timing of endocycle onset is crucial for correct development, because polyploidization is linked with cessation of cell division and initiation of terminal differentiation. The anaphase-promoting complex/cyclosome (APC/C) activator genes CDH1, FZR, and CCS52 are known to promote endocycle onset in human, Drosophila, and Medicago species cells, respectively; however, the genetic pathways governing development-dependent ApC/C-CDH1/FZR/CCS52 activity remain unknown. We report that the atypical E2F transcription factor E2Fe/DEL1 controls the expression of the CDH1/FZR orthologous CCS52A2 gene from Arabidopsis thaliana. E2Fe/DEL1 misregulation resulted in untimely CCS52A2 transcription, affecting the timing of endocycle onset. Correspondingly, ectopic CCS52A2 expression drove cells into the endocycle prematurely. Dynamic simulation illustrated that E2Fe/DEL1 accounted for the onset of the endocycle by regulating the temporal expression of CCS52A2 during the cell cycle in a development-dependent manner. Analogously, the atypical mammalian E2F7 protein was associated with the promoter of the APC/C-activating CDH1 gene, indicating that the transcriptional control of APC/C activator genes by atypical E2Fs might be evolutionarily conserved.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
DEL1, CDH1, E2F7, endoreduplication, ANAPHASE-PROMOTING COMPLEX, CYCLIN-DEPENDENT KINASE, ARABIDOPSIS-THALIANA, TRANSCRIPTION FACTOR, DROSOPHILA ENDOCYCLE, CELL ENLARGEMENT, GENE-EXPRESSION, ENDOREDUPLICATION, DIFFERENTIATION, PLANTS
journal title
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Proc. Natl. Acad. Sci. USA
volume
105
issue
38
pages
14721 - 14726
Web of Science type
Article
Web of Science id
000259592400088
ISSN
0027-8424
DOI
10.1073/pnas.0806510105
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
433538
handle
http://hdl.handle.net/1854/LU-433538
date created
2008-10-28 13:37:00
date last changed
2012-12-05 13:20:21
@article{433538,
  abstract     = {The endocycle represents an alternative cell cycle that is activated in various developmental processes, including placental formation, Drosophila oogenesis, and leaf development. In endocycling cells, mitotic cell cycle exit is followed by successive doublings of the DNA content, resulting in polyploidy. The timing of endocycle onset is crucial for correct development, because polyploidization is linked with cessation of cell division and initiation of terminal differentiation. The anaphase-promoting complex/cyclosome (APC/C) activator genes CDH1, FZR, and CCS52 are known to promote endocycle onset in human, Drosophila, and Medicago species cells, respectively; however, the genetic pathways governing development-dependent ApC/C-CDH1/FZR/CCS52 activity remain unknown. We report that the atypical E2F transcription factor E2Fe/DEL1 controls the expression of the CDH1/FZR orthologous CCS52A2 gene from Arabidopsis thaliana. E2Fe/DEL1 misregulation resulted in untimely CCS52A2 transcription, affecting the timing of endocycle onset. Correspondingly, ectopic CCS52A2 expression drove cells into the endocycle prematurely. Dynamic simulation illustrated that E2Fe/DEL1 accounted for the onset of the endocycle by regulating the temporal expression of CCS52A2 during the cell cycle in a development-dependent manner. Analogously, the atypical mammalian E2F7 protein was associated with the promoter of the APC/C-activating CDH1 gene, indicating that the transcriptional control of APC/C activator genes by atypical E2Fs might be evolutionarily conserved.},
  author       = {Lammens, Tim and Boudolf, V{\'e}ronique and Kheibarshekan Asl, Leila and Zalmas, L Panagiotis and Gaamouche, Tarik and Maes, Sara and Vanstraelen, Marleen and Kondorosi, Eva and La Thangue, Nicholas B and Govaerts, Willy and Inz{\'e}, Dirk and De Veylder, Lieven},
  issn         = {0027-8424},
  journal      = {PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA},
  keyword      = {DEL1,CDH1,E2F7,endoreduplication,ANAPHASE-PROMOTING COMPLEX,CYCLIN-DEPENDENT KINASE,ARABIDOPSIS-THALIANA,TRANSCRIPTION FACTOR,DROSOPHILA ENDOCYCLE,CELL ENLARGEMENT,GENE-EXPRESSION,ENDOREDUPLICATION,DIFFERENTIATION,PLANTS},
  language     = {eng},
  number       = {38},
  pages        = {14721--14726},
  title        = {Atypical E2F activity restrains APC/C-CCS52A2 function obligatory for endocycle onset},
  url          = {http://dx.doi.org/10.1073/pnas.0806510105},
  volume       = {105},
  year         = {2008},
}

Chicago
Lammens, Tim, Véronique Boudolf, Leila Kheibarshekan Asl, L Panagiotis Zalmas, Tarik Gaamouche, Sara Maes, Marleen Vanstraelen, et al. 2008. “Atypical E2F Activity Restrains APC/C-CCS52A2 Function Obligatory for Endocycle Onset.” Proceedings of the National Academy of Sciences of the United States of America 105 (38): 14721–14726.
APA
Lammens, T., Boudolf, V., Kheibarshekan Asl, L., Zalmas, L. P., Gaamouche, T., Maes, S., Vanstraelen, M., et al. (2008). Atypical E2F activity restrains APC/C-CCS52A2 function obligatory for endocycle onset. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 105(38), 14721–14726.
Vancouver
1.
Lammens T, Boudolf V, Kheibarshekan Asl L, Zalmas LP, Gaamouche T, Maes S, et al. Atypical E2F activity restrains APC/C-CCS52A2 function obligatory for endocycle onset. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2008;105(38):14721–6.
MLA
Lammens, Tim, Véronique Boudolf, Leila Kheibarshekan Asl, et al. “Atypical E2F Activity Restrains APC/C-CCS52A2 Function Obligatory for Endocycle Onset.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 105.38 (2008): 14721–14726. Print.