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Patchwork organization of the yeast plasma membrane into numerous coexisting domains

Nature Cell Biology volume 14, pages 640–648 (2012)Cite this article

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An Addendum to this article was published on 01 August 2012

Abstract

The plasma membrane is made up of lipids and proteins, and serves as an active interface between the cell and its environment. Many plasma-membrane proteins are laterally segregated in the plane of the membrane, but the underlying mechanisms remain controversial. Here we investigate the distribution and dynamics of a representative set of plasma-membrane-associated proteins in yeast cells. These proteins were distributed non-homogeneously in patterns ranging from distinct patches to nearly continuous networks, and these patterns were in turn strongly influenced by the lipid composition of the plasma membrane. Most proteins segregated into distinct domains. However, proteins with similar or identical transmembrane sequences (TMSs) showed a marked tendency to co-localize. Indeed we could predictably relocate proteins by swapping their TMSs. Finally, we found that the domain association of plasma-membrane proteins has an impact on their function. Our results are consistent with self-organization of biological membranes into a patchwork of coexisting domains.

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Figure 1: Test set of plasma-membrane proteins and imaging approach.
Figure 2: Localization patterns of plasma-membrane proteins.
Figure 3: Dynamics of plasma-membrane proteins.
Figure 4: Coexistence of multiple plasma-membrane protein domains.
Figure 5: Real and random overlap value.
Figure 6: Changing localization patterns of plasma-membrane proteins.
Figure 7: Influence of TMSs on protein localization.
Figure 8: Artificial re-targeting of plasma-membrane proteins.

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Acknowledgements

We are indebted to A. Rohrbach for providing access to the TIRF-SIM microscope and analysis. We thank N. Johnsson (Institute for Molecular Genetics and Cell Biology, Ulm University, Germany) for providing the plasmid ACP–Sag1 and P. Hardy for editorial assistance. This work was financially supported by the Max Planck Society.

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  1. Felix Spira and Nikola S. Mueller: These authors contributed equally to this work

Authors and Affiliations

  1. Cellular Dynamics and Cell Patterning, Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, Germany

    Felix Spira, Nikola S. Mueller, Gisela Beck, Joachim Beig & Roland Wedlich-Söldner

  2. Department of Microsystems Engineering-IMTEK, Laboratory for Bio- and Nano-Photonics, University of Freiburg, Freiburg 79110, Germany

    Philipp von Olshausen

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Contributions

R.W-S., F.S. and N.S.M. designed all experiments. F.S. performed all microscopy and experiments with help from G.B. N.S.M., F.S., J.B. and R.W-S. analysed the data. P.v.O. and F.S. performed the TIRF-SIM experiments. F.S., N.S.M. and R.W-S. wrote the paper.

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Correspondence to Roland Wedlich-Söldner.

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Spira, F., Mueller, N., Beck, G. et al. Patchwork organization of the yeast plasma membrane into numerous coexisting domains. Nat Cell Biol 14, 640–648 (2012). https://doi.org/10.1038/ncb2487

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