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Guiding self-organized pattern formation in cell polarity establishment

Gross, Peter and Kumar, K. Vijay and Goehring, Nathan W. and Bois, Justin S. and Hoege, Carsten and Jülicher, Frank and Grill, Stephan W. (2019) Guiding self-organized pattern formation in cell polarity establishment. Nature Physics, 15 (3). pp. 293-300. ISSN 1745-2473. http://resolver.caltech.edu/CaltechAUTHORS:20181016-130641267

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41567-018-0358-7DOIArticle
https://rdcu.be/bcBmxPublisherFree ReadCube access
ORCID:
AuthorORCID
Kumar, K. Vijay0000-0002-2963-7588
Goehring, Nathan W.0000-0001-8710-4467
Bois, Justin S.0000-0001-7137-8746
Grill, Stephan W.0000-0002-2290-5826
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.
Funders:
Funding AgencyGrant Number
European Molecular Biology Organization (EMBO)UNSPECIFIED
Department of Biotechnology (India)UNSPECIFIED
Max Planck SocietyUNSPECIFIED
Francis Crick InstituteUNSPECIFIED
Medical Research Council (UK)FC001086
Wellcome TrustUNSPECIFIED
COST ActionBM1408
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 ProgramRGP0023/2014
Record Number:CaltechAUTHORS:20181016-130641267
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20181016-130641267
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:90276
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:05 Dec 2018 19:09
Last Modified:06 Mar 2019 16:19

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