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Tubulin Nanorings

Published online by Cambridge University Press:  01 February 2016

Hacène Boukari  and
Dan L. Sackett
Hacène Boukari*
Affiliation:
Department of Physics and Engineering, OSCAR Center, Delaware State University, 1200 N. Dupont Hwy, Dover, DE 19901, U.S.A.
Dan L. Sackett
Affiliation:
Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, 9200 Rockville Pike, Bethesda, MD 20892, U.S.A.
*
*(Email: [email protected])
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Abstract

Biological systems routinely produce nanoscopic molecular structures withconsiderably less dispersion in size and shape than encountered in mostmanufactured materials. Indeed, Biological structures are frequently andessentially monodisperse. An example of this uniformity, combined with anintriguing geometry, is the nanometer-scale protein nanorings produced byinteraction of the protein tubulin with certain hydrophobic tri-, tetra- andpentapeptides originally extracted as natural products from marine biosystems.Different peptides produce different sized nanorings, but we focus on thoseproduced by binding to tubulin of the cyclic depsipeptide cryptophycin. Thenanorings that form upon binding of this ligand show a sharp mass distributionindicating that the nanorings are made of 8 tubulin dimers of 100 kDa.

In this submission, we demonstrate how a combination of fluorescence correlationspectroscopy, dynamic light scattering, electron microscopy, analyticalultracentrifugation, small-angle neutron scattering, and modeling is applied toreveal interactions of tubulin and cryptophycin in solution and to characterizetheir structures. We find that the cryptophycin-tubulin nanorings(∼25 nm diameter) are single-walled, appear rigid, are composed of 8tubulin dimers in a single closed ring, and are stable upon dilution tonanomolar concentrations.

Similar studies with a different peptide, the linear pentapeptide dolastatin 10,demonstrated that binding of this peptide to tubulin produces larger nanorings(14 tubulin dimers, ∼45 nm diameter rings), with slightly differentproperties. The ability to adjust the ring size with different peptides, andproduce uniform nanorings with properties that differ slightly between sizeclasses, makes the tubulin-peptide ring structures an appealing structuralsystem.

Keywords

macromolecular structurenanostructurepolymer
Type
Articles
Information
MRS Advances , Volume 1 , Issue 8: Biomaterials and Soft Materials , 2016 , pp. 553 - 558
Copyright
Copyright © Materials Research Society 2016 

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References

REFERENCES

Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K., and Watson, J. D., Molecular Biology of the Cell 3rd Edition (Garland Publishing Inc., NY, USA, 1994).Google Scholar
Boukari, H., Nossal, R., Sackett, D., and Schuck, P., Phys. Rev. Lett. 93 98106 (2004).CrossRefGoogle Scholar
Boukari, H., Schuck, P., Sackett, D. L., Nossal, R., Biopolymers 86, 424 (2007).CrossRefGoogle Scholar
Boukari, H., Nossal, R., Sackett, D. L., Biochemistry 42 1292–1300 (2003).CrossRefGoogle Scholar
Watts, N. R., Cheng, N., West, W., Steven, A. C., Sackett, D. L., Biochemistry 41, 12662 (2002).CrossRefGoogle Scholar
Nogales, E., Whittaker, M., Milligan, R. A., Downing, K. H., Cell 96, 79 (1999).CrossRefGoogle Scholar
Bordas, J., Mandelkow, E. M., Mandelkow, E., J. Mol. Biol. 164, 89 (1983).CrossRefGoogle Scholar
Diaz, J. F., Pantos, E., Bordas, J., Andreu, J. M., J. Mol. Biol. 238, 214 (1994).CrossRefGoogle Scholar
Nordlander, P., ACS Nano 3, 488 (2009).CrossRefGoogle Scholar
Carlson, J. C. T., Sidhartha, S. J., Flenniken, M., Chou, T., Siegel, R. A., and Wagner, C. R., J. Am Chem. Soc. 128, 7630 (2006).CrossRefGoogle Scholar
Seo, S., Kim, H. C., Ko, H., and Cheng, M., J. Vac. Sci. Technol. B 25, 2271 (2007).CrossRefGoogle Scholar
Steele, J. M., Liu, Z., Wang, Y., and Zhang, X., Opt. Express 14, 5664 (2006).CrossRefGoogle Scholar
Bozhevolnyi, S.I., Volkov, V. S., Devaux, E., Laluet, J. Y., and Ebbesen, T. W., Nature 440, 508 (2006).CrossRefGoogle Scholar
Wang, B. and Wang, G. P., Appl. Phys. Lett. 89, 133106 (2006).CrossRefGoogle Scholar
Jung, K. Y., Teixeira, F. L., and Reano, R. M., J. Lightwave Technol. 25, 2757 (2007).CrossRefGoogle Scholar
Suarez, M. A., Grosjean, T., Charraut, D., and Courjon, D., Opt. Commun. 270, 447 (2007).CrossRefGoogle Scholar
Larsson, E. M., Alegret, J., Käll, M., and Sutherland, D. S., Nano Lett. 7, 1256 (2007).CrossRefGoogle Scholar
Stewart, M. E., Anderton, C. R., Thompson, L. B., Maria, J., Gray, S. K., Rogers, J. A., and Nuzzo, P. G., Chem. Rev. 108, 494 (2008).CrossRefGoogle Scholar
Aizpurua, J., Hanarp, P., Sutherland, D. S., Käll, M., Bryant, G. W., de Abajo, F. J. G., Phys. Rev. Lett. 90, 057401 (2003).CrossRefGoogle Scholar
Laurent, G., Félidj, N., Grand, J., Aubard, J., and Lévi, G., Phys. Rev. B 73, 245417 (2006).CrossRefGoogle Scholar
Wang, S., Pile, D. F. P., Sun, C., and Zhang, X., Nano Lett. 7, 1076 (2007).CrossRefGoogle Scholar
Hao, F., Nordlander, P., Burnett, M. T., and Maier, S. A., Phys. Rev. B 76, 245417 (2007).CrossRefGoogle Scholar
Clark, A. W., Glidle, A., Cumming, D. R. S., and Cooper, J. M., Appl. Phys. Lett. 93, 023121 (2008).CrossRefGoogle Scholar
Liu, G. L., Lu, Y., Kim, J., Doll, J. C., and Lee, L. P., Adv. Mater. 17, 2683 (2005).CrossRefGoogle Scholar
Lu, Y., Liu, G. L., Kim, J., Mejia, Y. X., and Lee, L. P., Nano Lett. 5, 119 (2005).CrossRefGoogle Scholar
Chou, T. F., So, C., White, B. F., Carlson, J. C. T., Sarikaya, M., Wagner, C. R., ACS Nano 2, 2519 (2008).CrossRefGoogle Scholar
Zhang, S., Marini, D. M., Hwang, W., and Santoso, S., Cur. Opin. Chem. Biol. 6, 865 (2002).CrossRefGoogle Scholar
O’Sullivan, M. C., Sprafke, J. K., Kondratuk, D. V., Rinfray, C., Claridge, T. D. W., Saywell, A., Blunt, M. O., O’Shea, J. N., Beton, P. H., Malfois, M., Anderson, H. L., Nature 469, 72 (2011).CrossRefGoogle Scholar
Behrens, S., Habicht, W., Wagner, K., and Unger, E., Adv. Mater. 18, 264 (2006).CrossRefGoogle Scholar
Boukari, H. and Sackett, D. L. in Biophysical Tools for Biologists: Vol 1, Edited by Correia, J. J. and Detrich, H. W., III (ELSEVIER ACADEMIC PRESS INC, California; 2008).Google Scholar
Rigler, R. and Elson, E. S. Fluorescence Correlation Spectroscopy: Theory and Applications (Springer Series in Chemical Physics, Springer-Verlag, New York, 2001).CrossRefGoogle Scholar
Kostorz, G. Neutron Scattering (Academic Press, NY, 1979).Google Scholar
Goldstein, J., Newbury, D. E., Joy, D. C., Lyman, C. E., Echlin, P., Lifshin, E., Sawyer, L., and Michael, J. R. Scanning Electron Microscopy and X-ray Microanalysis (Springer; 3rd Edition, 2007).Google Scholar
Berne, B. J. and Pecora, R. Dynamic Light Scattering (Wiley-Interscience, John Wiley and Sons, Inc., New York, NY, USA, 1976).Google Scholar
www.analyticalultracentrifugation.com/references.htm (accessed on 11/18/2015).Google Scholar
Svedberg, T., and Pederson, K. O. The Ultracentrifuge (Oxford Univ. Press, London, 1940).Google Scholar
Watts, N.R., Sackett, D.L., Ward, R.D., Miller, M.W., Wingfield, P.T., Stahl, S.S., Steven, A.C., J Cell Biol. 150 349–60 (2000).CrossRefGoogle Scholar
de La Torre, J. G. and Bloomfield, V. A. Q. Rev. Biophys. 14, 81 (1981).CrossRefGoogle Scholar
http://leonardo.inf.um.es/macromol/programs/hydropro/hydropro.htm (accessed on 11/18/2015)Google Scholar
Mitra, A. and Sept, D., Biochemistry 43, 13955 (2004).CrossRefGoogle Scholar