Not much is known about how organelles organize into patterns. In ciliates, the cortical pattern is propagated during “tandem duplication,” a cell division that remodels the parental cell into two daughter cells. A key step is the formation of the division boundary along the cell’s equator. In Tetrahymena thermophila, the cdaA alleles prevent the formation of the division boundary. We find that the CDAA gene encodes a cyclin E that accumulates in the posterior cell half, concurrently with accumulation of CdaI, a Hippo/Mst kinase, in the anterior cell half. The division boundary forms between the margins of expression of CdaI and CdaA, which exclude each other from their own cortical domains. The activities of CdaA and CdaI must be balanced to initiate the division boundary and to position it along the cell’s equator. CdaA and CdaI cooperate to position organelles near the new cell ends. Our data point to an intracellular positioning mechanism involving antagonistic Hippo signaling and cyclin E.
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7 September 2020
Article|
July 06 2020
Mutual antagonism between Hippo signaling and cyclin E drives intracellular pattern formation
Yu-Yang Jiang
,
1
Department of Cellular Biology, University of Georgia, Athens, GA
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Wolfgang Maier
,
2
Bioinformatics, University of Freiburg, Freiburg, Germany
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Uzoamaka N. Chukka
,
Uzoamaka N. Chukka
1
Department of Cellular Biology, University of Georgia, Athens, GA
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Michael Choromanski
,
Michael Choromanski
1
Department of Cellular Biology, University of Georgia, Athens, GA
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Chinkyu Lee
,
Chinkyu Lee
1
Department of Cellular Biology, University of Georgia, Athens, GA
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Ewa Joachimiak
,
Ewa Joachimiak
3
Laboratory of Cytoskeleton and Cilia Biology, Nencki Institute of Experimental Biology of Polish Academy of Sciences, Warsaw, Poland
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Dorota Wloga
,
Dorota Wloga
3
Laboratory of Cytoskeleton and Cilia Biology, Nencki Institute of Experimental Biology of Polish Academy of Sciences, Warsaw, Poland
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Wayland Yeung
,
Wayland Yeung
4
Institute of Bioinformatics, University of Georgia, Athens, GA
5
Department of Biochemistry and Molecular Biology, University of Georgia, Athens, GA
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Natarajan Kannan
,
Natarajan Kannan
4
Institute of Bioinformatics, University of Georgia, Athens, GA
5
Department of Biochemistry and Molecular Biology, University of Georgia, Athens, GA
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Joseph Frankel
,
Joseph Frankel
6
Department of Biology, University of Iowa, Iowa City, IA
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Jacek Gaertig
1
Department of Cellular Biology, University of Georgia, Athens, GA
Correspondence to Jacek Gaertig: jgaertig@uga.edu
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Yu-Yang Jiang
1
Department of Cellular Biology, University of Georgia, Athens, GA
Wolfgang Maier
2
Bioinformatics, University of Freiburg, Freiburg, Germany
Uzoamaka N. Chukka
1
Department of Cellular Biology, University of Georgia, Athens, GA
Michael Choromanski
1
Department of Cellular Biology, University of Georgia, Athens, GA
Chinkyu Lee
1
Department of Cellular Biology, University of Georgia, Athens, GA
Ewa Joachimiak
3
Laboratory of Cytoskeleton and Cilia Biology, Nencki Institute of Experimental Biology of Polish Academy of Sciences, Warsaw, Poland
Dorota Wloga
3
Laboratory of Cytoskeleton and Cilia Biology, Nencki Institute of Experimental Biology of Polish Academy of Sciences, Warsaw, Poland
Wayland Yeung
4
Institute of Bioinformatics, University of Georgia, Athens, GA
5
Department of Biochemistry and Molecular Biology, University of Georgia, Athens, GA
Natarajan Kannan
4
Institute of Bioinformatics, University of Georgia, Athens, GA
5
Department of Biochemistry and Molecular Biology, University of Georgia, Athens, GA
Joseph Frankel
6
Department of Biology, University of Iowa, Iowa City, IA
Jacek Gaertig
1
Department of Cellular Biology, University of Georgia, Athens, GA
*
Y.-Y. Jiang and W. Maier contributed equally to this paper.
Correspondence to Jacek Gaertig: jgaertig@uga.edu
Received:
February 17 2020
Revision Received:
May 11 2020
Accepted:
June 04 2020
Online Issn: 1540-8140
Print Issn: 0021-9525
Funding:
Bundesministerium für Bildung und Forschung
(031L0101C de.NBI-epi)
Narodowym Centrum Nauki
(Opus13, 2017/25/B/NZ3/01609, Opus15, 2018/29/B/NZ3/02443)
National Institutes of Health
(R21HD092809, 5RO1GM114409)
© 2020 Jiang et al.
2020
This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
J Cell Biol (2020) 219 (9): e202002077.
Article history
Received:
February 17 2020
Revision Received:
May 11 2020
Accepted:
June 04 2020
Citation
Yu-Yang Jiang, Wolfgang Maier, Uzoamaka N. Chukka, Michael Choromanski, Chinkyu Lee, Ewa Joachimiak, Dorota Wloga, Wayland Yeung, Natarajan Kannan, Joseph Frankel, Jacek Gaertig; Mutual antagonism between Hippo signaling and cyclin E drives intracellular pattern formation. J Cell Biol 7 September 2020; 219 (9): e202002077. doi: https://doi.org/10.1083/jcb.202002077
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