Guiding self-organized pattern formation in cell polarity establishment
Abstract
Spontaneous pattern formation in Turing systems relies on feedback. But patterns in cells and tissues seldom form spontaneously—instead they are controlled by regulatory biochemical interactions that provide molecular guiding cues. The relationship between these guiding cues and feedback in controlled biological pattern formation remains unclear. Here, we explore this relationship during cell-polarity establishment in the one-cell-stage Caenorhabditis elegans embryo. We quantify the strength of two feedback systems that operate during polarity establishment: feedback between polarity proteins and the actomyosin cortex, and mutual antagonism among polarity proteins. We characterize how these feedback systems are modulated by guiding cues from the centrosome, an organelle regulating cell cycle progression. By coupling a mass-conserved Turing-like reaction–diffusion system for polarity proteins to an active-gel description of the actomyosin cortex, we reveal a transition point beyond which feedback ensures self-organized polarization, even when cues are removed. Notably, the system switches from a guide-dominated to a feedback-dominated regime well beyond this transition point, which ensures robustness. Together, these results reveal a general criterion for controlling biological pattern-forming systems: feedback remains subcritical to avoid unstable behaviour, and molecular guiding cues drive the system beyond a transition point for pattern formation.
Additional Information
© 2018 Springer Nature Publishing AG. Received 17 July 2018; Accepted 23 October 2018; Published 03 December 2018. Code availability: Code to analyse the data and perform numeric simulations is available upon request. Data availability: All data generated or analysed in this study are available from the corresponding author upon request. P.G. acknowledges a EMBO Long-Term Fellowship for funding. The research of K.V.K. is supported by the Department of Biotechnology, India through a Ramalingaswami Re-entry Fellowship, and the Max Planck Society and the Department of Science and Technology, India through a Max Planck Partner Group at ICTS-TIFR. N.W.G. was supported by the Francis Crick Institute, which receives its core funding from Cancer Research UK (FC001086), the UK Medical Research Council (FC001086) and the Wellcome Trust (FC001086), and is a member of the GENiE network supported by COST Action BM1408 and EMBO. S.W.G was supported by the DFG (SPP 1782, GSC 97, GR 3271/2, GR 3271/3, GR 3271/4), the European Research Council (grants 281903 and 742712), ITN grants 281903 and 641639 from the EU, the Max-Planck-Society as a Max-Planck-Fellow, and the Human Frontier Science Program (RGP0023/2014). J.S.B. acknowledges the Human Frontier Science Program for funding. We thank D. Dickinson, B. Goldstein, F. Motegi and G. Seydoux for sharing C. elegans strains. We thank P. Gönczy, L. Hubatsch, T. Hyman, K. Kruse and M. Labouesse for discussion and insightful comments on the manuscript. Author Contributions: P.G. performed experiments and K.V.K. developed the theory, with help from all authors. Data were analysed together with input from all authors. P.G., K.V.K., F.J. and S.W.G. wrote the manuscript. The authors declare no competing interests.Attached Files
Accepted Version - EMS83581.pdf
Supplemental Material - 41567_2018_358_MOESM1_ESM.pdf
Supplemental Material - 41567_2018_358_MOESM2_ESM.pdf
Supplemental Material - 41567_2018_358_MOESM3_ESM.mov
Supplemental Material - 41567_2018_358_MOESM4_ESM.mov
Supplemental Material - 41567_2018_358_MOESM5_ESM.mov
Supplemental Material - 41567_2018_358_MOESM6_ESM.mov
Supplemental Material - 41567_2018_358_MOESM7_ESM.mov
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Additional details
- PMCID
- PMC6640039
- Eprint ID
- 90276
- DOI
- 10.1038/s41567-018-0358-7
- Resolver ID
- CaltechAUTHORS:20181016-130641267
- European Molecular Biology Organization (EMBO)
- Department of Biotechnology (India)
- Max Planck Society
- Francis Crick Institute
- Medical Research Council (UK)
- FC001086
- Wellcome Trust
- COST Action
- BM1408
- Deutsche Forschungsgemeinschaft (DFG)
- SPP 1782
- Deutsche Forschungsgemeinschaft (DFG)
- GSC 97
- Deutsche Forschungsgemeinschaft (DFG)
- GR 3271/2
- Deutsche Forschungsgemeinschaft (DFG)
- GR 3271/3
- Deutsche Forschungsgemeinschaft (DFG)
- GR 3271/4
- European Research Council (ERC)
- 281903
- European Research Council (ERC)
- 742712
- European Research Council (ERC)
- 281903
- European Research Council (ERC)
- 641639
- Human Frontier Science Program
- RGP0023/2014
- Created
-
2018-12-05Created from EPrint's datestamp field
- Updated
-
2021-11-16Created from EPrint's last_modified field