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Long-range interlayer alignment of intralayer domains in stacked lipid bilayers

Nature Materials volume 11, pages 1074–1080 (2012)Cite this article

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Abstract

Liquid-crystalline phases of stacked lipid bilayers represent a pervasive motif in biomolecular assemblies. Here we report that, in addition to the usual smectic order, multicomponent multilayer membranes can exhibit columnar order arising from the coupling of two-dimensional intralayer phase separation and interlayer smectic ordering. This coupling propagates across hundreds of membrane lamellae, producing long-range alignment of phase-separated domains. Quantitative analysis of real-time dynamical experiments reveals that there is an interplay between intralayer domain growth and interlayer coupling, suggesting the existence of cooperative multilayer epitaxy. We postulate that such long-range epitaxy is solvent-assisted, and that it originates from the surface tension associated with differences in the network of hydrogen-bonded water molecules at the hydrated interfaces between the domains and the surrounding phase. Our findings might inspire the development of self-assembly-based strategies for the long-range alignment of functional lipid domains.

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Figure 1: Composition-dependent phase separation in stacked lipid bilayers.
Figure 2: Depth-resolved confocal fluorescence microscopy of aligned and unaligned stacked lipid bilayers.
Figure 3: Domain evolution and coarsening.
Figure 4: Dependence of domain size on the number of lamellae.
Figure 5: Proposed molecular explanation of interlamellar coupling of domains in stacked lipid bilayers.
Figure 6: X-ray diffraction analysis.

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Acknowledgements

This work is supported by a grant from the Biomolecular Materials Program, Division of Materials Science and Engineering, Basic Energy Sciences, US Department of Energy under Award no. DE-FG02-04ER46173.

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Author notes

  1. Yicong Ma and Daryoosh Vashaee: These authors contributed equally to this work

Authors and Affiliations

  1. Department of Applied Science, University of California, Davis, California 95616, USA

    Lobat Tayebi & Atul N. Parikh

  2. Helmerich Advanced Technology Research Center, School of Material Science and Engineering, Oklahoma State University, Tulsa, Oklahoma 74106, USA

    Lobat Tayebi

  3. Physics Department, University of California, San Diego, California 92093, USA

    Yicong Ma, Gang Chen & Sunil K. Sinha

  4. Helmerich Advanced Technology Research Center, School of Electrical and Computer Engineering, Oklahoma State University, Tulsa, Oklahoma 74106, USA

    Daryoosh Vashaee

  5. Department of Biomedical Engineering, University of California, Davis, California 95616, USA

    Atul N. Parikh

  6. Department of Chemical Engineering and Materials Science, University of California, Davis, California 95616, USA

    Atul N. Parikh

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Contributions

L.T., Y. M. and G.C. performed experiments, analysed data and wrote initial drafts of the manuscript. D.V. contributed extensively to all experimental data analyses and helped L.T. with the theoretical model. A.N.P. and S.K.S. conceived the overall project, provided intellectual and technical guidance, performed final edits of the manuscript and are principal investigators of the supporting grant. All authors contributed to writing and revising the manuscript, and agreed on its final content.

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Correspondence to Sunil K. Sinha or Atul N. Parikh.

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Tayebi, L., Ma, Y., Vashaee, D. et al. Long-range interlayer alignment of intralayer domains in stacked lipid bilayers. Nature Mater 11, 1074–1080 (2012). https://doi.org/10.1038/nmat3451

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