It is widely observed that eukaryotic cells can polarize spontaneously in the absence of pre-established asymmetric cues. This phenomenon indicates that the principle of self-organization may be central to the establishment of cell polarity. Modelling work, as well as recent experimental data from several organisms, suggests that a combination of local positive feedback loops and global inhibitors could result in robust cell symmetry breaking through amplification of minute, stochastic variations.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
Coupling of melanocyte signaling and mechanics by caveolae is required for human skin pigmentation
Nature Communications Open Access 12 June 2020
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
References
Arkowitz, R.A. Responding to attraction: chemotaxis and chemotropism in Dictyostelium and yeast. Trends Cell Biol. 9, 20–27 (1999).
Drubin, D.G. & Nelson, W.J. Origins of cell polarity. Cell 84, 335–344 (1996).
Chung, C.Y., Funamoto, S. & Firtel, R.A. Signaling pathways controlling cell polarity and chemotaxis. Trends Biochem. Sci. 26, 557–566 (2001).
Kirschner, M., Gerhart, J. & Mitchison, T. Molecular 'vitalism'. Cell 100, 79–88 (2000).
Parent, C.A. & Devreotes, P.N. A cell's sense of direction. Science 284, 765–770 (1999).
Firtel, R.A. & Chung, C.Y. The molecular genetics of chemotaxis: sensing and responding to chemoattractant gradients. Bioessays 22, 603–615 (2000).
Devreotes, P.N. & Zigmond, S.H. Chemotaxis in eukaryotic cells: a focus on leukocytes and Dictyostelium. Annu. Rev. Cell Biol. 4, 649–686 (1988).
Brownlee, C. & Bouget, F.Y. Polarity determination in Fucus: from zygote to multicellular embryo. Semin. Cell Dev. Biol. 9, 179–185 (1998).
Robinson, K.R., Wozniak, M., Pu, R. & Messerli, M. Symmetry breaking in the zygotes of the fucoid algae: controversies and recent progress. Curr. Top. Dev. Biol. 44, 101–125 (1999).
Hable, W.E. & Kropf, D.L. Roles of secretion and the cytoskeleton in cell adhesion and polarity establishment in Pelvetia compressa zygotes. Dev. Biol. 198, 45–56 (1998).
Vincent, J.P., Oster, G.F. & Gerhart, J.C. Kinematics of gray crescent formation in Xenopus eggs: the displacement of subcortical cytoplasm relative to the egg surface. Dev. Biol. 113, 484–500 (1986).
Gerhart, J. et al. Cortical rotation of the Xenopus egg: consequences for the anteroposterior pattern of embryonic dorsal development. Development 107, 37–51 (1989).
Drubin, D.G. Development of cell polarity in budding yeast. Cell 65, 1093–1096 (1991).
Casamayor, A. & Snyder, M. Bud-site selection and cell polarity in budding yeast. Curr. Opin. Microbiol. 5, 179–186 (2002).
Park, H.O., Kang, P.J. & Rachfal, A.W. Localization of the Rsr1/Bud1 GTPase involved in selection of a proper growth site in yeast. J. Biol. Chem. 277, 26721–26724 (2002).
Pruyne, D. & Bretscher, A. Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J. Cell Sci. 113, 365–375 (2000).
Johnson, D.I. Cdc42: An essential Rho-type GTPase controlling eukaryotic cell polarity. Microbiol. Mol. Biol. Rev. 63, 54–105 (1999).
Chant, J. & Herskowitz, I. Genetic control of bud site selection in yeast by a set of gene products that constitute a morphogenetic pathway. Cell 65, 1203–1212 (1991).
Gulli, M.P. et al. Phosphorylation of the Cdc42 exchange factor Cdc24 by the PAK-like kinase Cla4 may regulate polarized growth in yeast. Mol. Cell 6, 1155–1167 (2000).
Lechler, T., Jonsdottir, G.A., Klee, S.K., Pellman, D. & Li, R. A two-tiered mechanism by which Cdc42 controls the localization and activation of an Arp2/3-activating motor complex in yeast. J. Cell Biol. 155, 261–270 (2001).
Wedlich-Soldner, R., Altschuler, S., Wu, L. & Li, R. Spontaneous cell polarization through actomyosin-based delivery of the Cdc42 GTPase. Science 299, 1231–1235 (2003).
Seeley, T.D. When is self-organization used in biological systems? Biol. Bull. 202, 314–318 (2002).
Misteli, T. The concept of self-organization in cellular architecture. J. Cell Biol. 155, 181–185 (2001).
Meinhardt, H. & Gierer, A. Pattern formation by local self-activation and lateral inhibition. Bioessays 22, 753–760 (2000).
Gierer, A. & Meinhardt, H. A theory of biological pattern formation. Kybernetik 12, 30–39 (1972).
Niggli, V. A membrane-permeant ester of phosphatidylinositol 3,4,5-trisphosphate (PIP(3)) is an activator of human neutrophil migration. FEBS Lett. 473, 217–221 (2000).
Weiner, O.D. et al. A PtdInsP(3)- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity. Nature Cell Biol. 4, 509–513 (2002).
Bourne, H.R. & Weiner, O. Cell polarity: A chemical compass. Nature 419, 21 (2002).
Weiner, O.D. Regulation of cell polarity during eukaryotic chemotaxis: the chemotactic compass. Curr. Opin. Cell Biol. 14, 196–202 (2002).
Wang, F. et al. Lipid products of PI(3)Ks maintain persistent cell polarity and directed motility in neutrophils. Nature Cell Biol. 4, 513–518 (2002).
Comer, F.I. & Parent, C.A. PI 3-kinases and PTEN: how opposites chemoattract. Cell 109, 541–544 (2002).
Pruyne, D. et al. Role of formins in actin assembly: nucleation and barbed-end association. Science 297, 612–615 (2002).
Sagot, I., Rodal, A.A., Moseley, J., Goode, B.L. & Pellman, D. An actin nucleation mechanism mediated by Bni1 and profilin. Nature Cell Biol. 4, 626–631 (2002).
Pu, R., Wozniak, M. & Robinson, K.R. Cortical actin filaments form rapidly during photopolarization and are required for the development of calcium gradients in Pelvetia compressa zygotes. Dev. Biol. 222, 440–449 (2000).
Thompson, C.R. & Bretscher, M.S. Cell polarity and locomotion, as well as endocytosis, depend on NSF. Development 129, 4185–4192 (2002).
Houliston, E. & Elinson, R.P. Patterns of microtubule polymerization relating to cortical rotation in Xenopus laevis eggs. Development 112, 107–117 (1991).
Houliston, E. & Elinson, R.P. Evidence for the involvement of microtubules, ER, and kinesin in the cortical rotation of fertilized frog eggs. J. Cell Biol. 114, 1017–1028 (1991).
Larabell, C.A., Rowning, B.A., Wells, J., Wu, M. & Gerhart, J.C. Confocal microscopy analysis of living Xenopus eggs and the mechanism of cortical rotation. Development 122, 1281–1289 (1996).
Nedelec, F.J., Surrey, T., Maggs, A.C. & Leibler, S. Self-organization of microtubules and motors. Nature 389, 305–308 (1997).
Surrey, T., Nedelec, F., Leibler, S. & Karsenti, E. Physical properties determining self-organization of motors and microtubules. Science 292, 1167–1171 (2001).
Miller, J.R. et al. Establishment of the dorsal-ventral axis in Xenopus embryos coincides with the dorsal enrichment of dishevelled that is dependent on cortical rotation. J. Cell Biol. 146, 427–437 (1999).
Meinhardt, H. Orientation of chemotactic cells and growth cones: models and mechanisms. J. Cell Sci. 112, 2867–2874 (1999).
Acknowledgements
We would like to thank O. Weiner, S. Wedlich, S. Altschuler and L. Wu for critical comments on the manuscript. This work was supported by an EMBO fellowship to R.W.S and a grant from the National Institute of Health (GM057063) to R.L.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wedlich-Soldner, R., Li, R. Spontaneous cell polarization: undermining determinism. Nat Cell Biol 5, 267–270 (2003). https://doi.org/10.1038/ncb0403-267
Issue Date:
DOI: https://doi.org/10.1038/ncb0403-267
This article is cited by
-
Coupling of melanocyte signaling and mechanics by caveolae is required for human skin pigmentation
Nature Communications (2020)
-
Functional interaction between Cdc42 and the stress MAPK signaling pathway during the regulation of fission yeast polarized growth
International Microbiology (2020)
-
Minimal model for spontaneous cell polarization and edge activity in oscillating, rotating and migrating cells
Nature Physics (2016)
-
Mathematical Analysis of Spontaneous Emergence of Cell Polarity
Bulletin of Mathematical Biology (2014)
-
How B cells capture, process and present antigens: a crucial role for cell polarity
Nature Reviews Immunology (2013)