DOI: 10.1073/pnas.95.14.8040. Lipid nanotubes as substrates for helical crystallization of macromolecules

Lipid nanotubes as substrates for helical crystallization of macromolecules

10.1073/pnas.95.14.8040

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

A general approach for crystallization of proteins in a fast and simple manner would be of immense interest to biologists studying protein structure–function relationships. Here, we describe a method that we have developed for promoting the formation of helical arrays of proteins and macromolecular assemblies. Electron micrographs of the arrays are suitable for helical image analysis and three-dimensional reconstruction. We show that hydrated mixtures of the glycolipid galactosylceramide (GalCer) and derivatized lipids or charged lipids form unilamellar nanotubules. The tubules bind proteins in a specific manner via high affinity ligands on the polar head groups of the lipid or via electrostatic interactions. By doping the GalCer with a novel nickel-containing lipid, we have been able to form helical arrays of two histidine-tagged proteins. Similarly, doping with a biotinylated lipid allows crystallization of streptavidin. Finally, three proteins with affinity for positively or negatively charged lipid layers formed helical arrays on appropriately charged tubules. The generality of this method may allow a wide variety of proteins to be crystallized on lipid nanotubes under physiological conditions.

Bibliography

Wilson-Kubalek, E. M., Brown, R. E., Celia, H., & Milligan, R. A. (1998). Lipid nanotubes as substrates for helical crystallization of macromolecules. Proceedings of the National Academy of Sciences, 95(14), 8040â8045.

Authors 4

Elizabeth M. Wilson-Kubalek (first)
Rhoderick E. Brown (additional)
Hervé Celia (additional)
Ronald A. Milligan (additional)

References 45 Referenced 142

10.1126/science.186.4168.1036
10.1017/S0033583500004297
10.1126/science.8316858
10.1016/S0092-8674(00)80330-X
10.1038/386088a0
10.1038/386091a0
10.1083/jcb.127.2.411
10.1038/nsb0696-547
10.1038/376441a0
10.1016/S0969-2126(01)00216-7
10.1016/S0022-2836(05)80271-2
T A Ceska, R Henderson, J M Baldwin, F Zemlin, E Beckmann, K H Downing Acta Physiol Scand Suppl 607, 31–40 (1992). / Acta Physiol Scand Suppl by Ceska T A (1992)
10.1038/367614a0
10.1038/350167a0
10.1038/34465
10.1016/0304-3991(92)90019-G
10.1016/0304-3991(95)00057-8
10.1016/0022-2836(89)90379-3
10.1006/jmbi.1995.0282
10.1038/373037a0
10.1016/0304-3991(92)90007-7
10.1016/S0065-227X(97)89638-4
10.1038/301125a0
10.1016/0304-3991(91)90082-H
10.1016/S0006-3495(96)79597-8
10.1016/S0006-3495(95)80068-8
10.1074/jbc.272.7.4103
10.1073/pnas.91.9.3809
10.1016/S0021-9258(18)62016-2
10.1006/jsbi.1994.1039
10.1093/emboj/16.6.1199
10.1006/jmbi.1997.1431
10.1002/chem.19970030419
10.1016/0022-2836(88)90107-6
10.1038/340730a0
10.1016/0889-1605(85)90084-9
10.1016/1047-8477(92)90013-Z
10.1016/0092-8674(95)90114-0
10.1016/0022-2836(91)90538-H
10.1016/S0006-3495(91)82232-9
10.1002/pro.5560050909
10.1073/pnas.93.10.4937
10.1083/jcb.91.2.340
10.1016/S0962-8924(00)88948-5
10.1038/364430a0

Dates

Type	When
Created	23 years ago (July 26, 2002, 10:39 a.m.)
Deposited	3 years, 4 months ago (April 13, 2022, 4:38 p.m.)
Indexed	2 months, 1 week ago (June 10, 2025, 2:44 p.m.)
Issued	27 years, 1 month ago (July 7, 1998)
Published	27 years, 1 month ago (July 7, 1998)
Published Online	27 years, 1 month ago (July 7, 1998)
Published Print	27 years, 1 month ago (July 7, 1998)

Funders 0

None

BibTeX

@article{Wilson_Kubalek_1998, title={Lipid nanotubes as substrates for helical crystallization of macromolecules}, volume={95}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.95.14.8040}, DOI={10.1073/pnas.95.14.8040}, number={14}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Wilson-Kubalek, Elizabeth M. and Brown, Rhoderick E. and Celia, Hervé and Milligan, Ronald A.}, year={1998}, month=jul, pages={8040–8045} }

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