Four Different Mechanisms for Switching Cell Polarity

Overview

Journal PLoS Comput Biol

Specialty Biology

Date 2021 Jan 19

PMID 33465073

Citations 1

Authors

Filipe Tostevin

Manon Wigbers

Lotte Sogaard-Andersen

Ulrich Gerland

Affiliations

Soon will be listed here.

Abstract

The mechanisms and design principles of regulatory systems establishing stable polarized protein patterns within cells are well studied. However, cells can also dynamically control their cell polarity. Here, we ask how an upstream signaling system can switch the orientation of a polarized pattern. We use a mathematical model of a core polarity system based on three proteins as the basis to study different mechanisms of signal-induced polarity switching. The analysis of this model reveals four general classes of switching mechanisms with qualitatively distinct behaviors: the transient oscillator switch, the reset switch, the prime-release switch, and the push switch. Each of these regulatory mechanisms effectively implements the function of a spatial toggle switch, however with different characteristics in their nonlinear and stochastic dynamics. We identify these characteristics and also discuss experimental signatures of each type of switching mechanism.

Citing Articles

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References

Chou C, Bardwell L, Nie Q, Yi T . Noise filtering tradeoffs in spatial gradient sensing and cell polarization response. BMC Syst Biol. 2011; 5:196. PMC: 3268761. DOI: 10.1186/1752-0509-5-196. View

Lou C, Liu X, Ni M, Huang Y, Huang Q, Huang L . Synthesizing a novel genetic sequential logic circuit: a push-on push-off switch. Mol Syst Biol. 2010; 6:350. PMC: 2858441. DOI: 10.1038/msb.2010.2. View

Hu Z, Lutkenhaus J . Topological regulation of cell division in Escherichia coli involves rapid pole to pole oscillation of the division inhibitor MinC under the control of MinD and MinE. Mol Microbiol. 1999; 34(1):82-90. DOI: 10.1046/j.1365-2958.1999.01575.x. View

Dworkin J . Cellular polarity in prokaryotic organisms. Cold Spring Harb Perspect Biol. 2010; 1(6):a003368. PMC: 2882128. DOI: 10.1101/cshperspect.a003368. View

Wedlich-Soldner R, Li R . Spontaneous cell polarization: undermining determinism. Nat Cell Biol. 2003; 5(4):267-70. DOI: 10.1038/ncb0403-267. View

Schumacher D, Sogaard-Andersen L . Regulation of Cell Polarity in Motility and Cell Division in Myxococcus xanthus. Annu Rev Microbiol. 2017; 71:61-78. DOI: 10.1146/annurev-micro-102215-095415. View

Campanale J, Sun T, Montell D . Development and dynamics of cell polarity at a glance. J Cell Sci. 2017; 130(7):1201-1207. PMC: 5399778. DOI: 10.1242/jcs.188599. View

Drubin D, Nelson W . Origins of cell polarity. Cell. 1996; 84(3):335-44. DOI: 10.1016/s0092-8674(00)81278-7. View

Park J, Holmes W, Lee S, Kim H, Kim D, Kwak M . Mechanochemical feedback underlies coexistence of qualitatively distinct cell polarity patterns within diverse cell populations. Proc Natl Acad Sci U S A. 2017; 114(28):E5750-E5759. PMC: 5514712. DOI: 10.1073/pnas.1700054114. View

10.

Fritz G, Buchler N, Hwa T, Gerland U . Designing sequential transcription logic: a simple genetic circuit for conditional memory. Syst Synth Biol. 2008; 1(2):89-98. PMC: 2533522. DOI: 10.1007/s11693-007-9006-8. View

11.

Lugagne J, Sosa Carrillo S, Kirch M, Kohler A, Batt G, Hersen P . Balancing a genetic toggle switch by real-time feedback control and periodic forcing. Nat Commun. 2017; 8(1):1671. PMC: 5693866. DOI: 10.1038/s41467-017-01498-0. View

12.

Chau A, Walter J, Gerardin J, Tang C, Lim W . Designing synthetic regulatory networks capable of self-organizing cell polarization. Cell. 2012; 151(2):320-32. PMC: 3498761. DOI: 10.1016/j.cell.2012.08.040. View

13.

Lawson M, Drawert B, Khammash M, Petzold L, Yi T . Spatial stochastic dynamics enable robust cell polarization. PLoS Comput Biol. 2013; 9(7):e1003139. PMC: 3723497. DOI: 10.1371/journal.pcbi.1003139. View

14.

Zusman D, Scott A, Yang Z, Kirby J . Chemosensory pathways, motility and development in Myxococcus xanthus. Nat Rev Microbiol. 2007; 5(11):862-72. DOI: 10.1038/nrmicro1770. View

15.

Loose M, Fischer-Friedrich E, Herold C, Kruse K, Schwille P . Min protein patterns emerge from rapid rebinding and membrane interaction of MinE. Nat Struct Mol Biol. 2011; 18(5):577-83. DOI: 10.1038/nsmb.2037. View

16.

Gross P, Kumar K, Goehring N, Bois J, Hoege C, Julicher F . Guiding self-organized pattern formation in cell polarity establishment. Nat Phys. 2019; 15(3):293-300. PMC: 6640039. DOI: 10.1038/s41567-018-0358-7. View

17.

Etienne-Manneville S . Cdc42--the centre of polarity. J Cell Sci. 2004; 117(Pt 8):1291-300. DOI: 10.1242/jcs.01115. View

18.

Kaiser D, Yu R . Reversing cell polarity: evidence and hypothesis. Curr Opin Microbiol. 2005; 8(2):216-21. DOI: 10.1016/j.mib.2005.02.002. View

19.

Goehring N, Hoege C, Grill S, Hyman A . PAR proteins diffuse freely across the anterior-posterior boundary in polarized C. elegans embryos. J Cell Biol. 2011; 193(3):583-94. PMC: 3087016. DOI: 10.1083/jcb.201011094. View

20.

Szadkowski D, Harms A, Carreira L, Wigbers M, Potapova A, Wuichet K . Spatial control of the GTPase MglA by localized RomR-RomX GEF and MglB GAP activities enables Myxococcus xanthus motility. Nat Microbiol. 2019; 4(8):1344-1355. DOI: 10.1038/s41564-019-0451-4. View