Measuring similarity between dynamic ensembles of biomolecules

ABSTRACT We present a simple and general approach termed REsemble for quantifying population overlap and structural similarity between ensembles. This approach captures improvements in the

quality of ensembles determined using increasing input experimental data—improvements that go undetected when conventional methods for comparing ensembles are used—and reveals unexpected

similarities between RNA ensembles determined using NMR and molecular dynamics simulations. Access through your institution Buy or subscribe This is a preview of subscription content, access

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Log in * Learn about institutional subscriptions * Read our FAQs * Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS LOCOHD: A METRIC FOR COMPARING LOCAL ENVIRONMENTS OF

PROTEINS Article Open access 13 May 2024 RAPID AND ACCURATE DETERMINATION OF ATOMISTIC RNA DYNAMIC ENSEMBLE MODELS USING NMR AND STRUCTURE PREDICTION Article Open access 02 November 2020

CONVERGENCE AND EQUILIBRIUM IN MOLECULAR DYNAMICS SIMULATIONS Article Open access 07 February 2024 REFERENCES * Jensen, M.R. et al. _Structure_ 17, 1169–1185 (2009). Article  CAS  PubMed 

Google Scholar  * Clore, G.M. & Schwieters, C.D. _Biochemistry_ 43, 10678–10691 (2004). Article  CAS  PubMed  Google Scholar  * Salmon, L., Yang, S. & Al-Hashimi, H.M. _Annu. Rev.

Phys. Chem._ 10.1146/annurev-physchem-040412-110059 (16 December 2013). * Boehr, D.D., Nussinov, R. & Wright, P.E. _Nat. Chem. Biol._ 5, 789–796 (2009). Article  CAS  PubMed  PubMed

Central  Google Scholar  * Wand, A.J. _Curr. Opin. Struct. Biol._ 23, 75–81 (2013). Article  CAS  PubMed  Google Scholar  * Stelzer, A.C. et al. _Nat. Chem. Biol._ 7, 553–559 (2011). CAS 

PubMed  PubMed Central  Google Scholar  * Richardson, J.S. & Richardson, D.C. _Annu. Rev. Biophys._ 42, 1–28 (2013). Article  CAS  PubMed  PubMed Central  Google Scholar  *

Lindorff-Larsen, K. & Ferkinghoff-Borg, J. _PLoS ONE_ 4, e4203 (2009). Article  PubMed  PubMed Central  Google Scholar  * Fisher, C.K., Huang, A. & Stultz, C.M. _J. Am. Chem. Soc._

132, 14919–14927 (2010). Article  CAS  PubMed  PubMed Central  Google Scholar  * De Simone, A., Richter, B., Salvatella, X. & Vendruscolo, M. _J. Am. Chem. Soc._ 131, 3810–3811 (2009).

Article  CAS  PubMed  Google Scholar  * Cha, S.-H. _Int. J. Math. Models Methods Appl. Sci._ 1, 300–307 (2007). Google Scholar  * Brüschweiler, R. _Curr. Opin. Struct. Biol._ 13, 175–183

(2003). Article  PubMed  Google Scholar  * Frank, A.T., Stelzer, A.C., Al-Hashimi, H.M. & Andricioaei, I. _Nucleic Acids Res._ 37, 3670–3679 (2009). Article  CAS  PubMed  PubMed Central

  Google Scholar  * Marsh, J.A., Teichmann, S.A. & Forman-Kay, J.D. _Curr. Opin. Struct. Biol._ 22, 643–650 (2012). Article  CAS  PubMed  Google Scholar  * Chen, Y., Campbell, S.L. &

Dokholyan, N.V. _Biophys. J._ 93, 2300–2306 (2007). Article  CAS  PubMed  PubMed Central  Google Scholar  * Tolman, J.R., Flanagan, J.M., Kennedy, M.A. & Prestegard, J.H. _Proc. Natl.

Acad. Sci. USA_ 92, 9279–9283 (1995). Article  CAS  PubMed  PubMed Central  Google Scholar  * Tjandra, N. & Bax, A. _Science_ 278, 1111–1114 (1997). Article  CAS  PubMed  Google Scholar

  * Bailor, M.H., Mustoe, A.M., Brooks, C.L. III. & Al-Hashimi, H.M. _Nat. Protoc._ 6, 1536–1545 (2011). Article  CAS  PubMed  PubMed Central  Google Scholar  * Salmon, L., Bascom, G.,

Andricioaei, I. & Al-Hashimi, H.M. _J. Am. Chem. Soc._ 135, 5457–5466 (2013). Article  CAS  PubMed  PubMed Central  Google Scholar  * Denning, E.J., Priyakumar, U.D., Nilsson, L. &

Mackerell, A.D. Jr. _J. Comput. Chem._ 32, 1929–1943 (2011). Article  CAS  PubMed  PubMed Central  Google Scholar  * Fisher, C.K., Zhang, Q., Stelzer, A. & Al-Hashimi, H.M. _J. Phys.

Chem. B_ 112, 16815–16822 (2008). Article  CAS  PubMed  PubMed Central  Google Scholar  * Lavery, R. & Sklenar, H. _J. Biomol. Struct. Dyn._ 6, 655–667 (1989). Article  CAS  PubMed 

Google Scholar  Download references ACKNOWLEDGEMENTS We thank members of the Al-Hashimi laboratory for critical comments on the manuscript. This work was supported by the US National

Institutes of Health (R01AI066975 and PO1 GM0066275). AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Department of Chemistry, University of Michigan, Ann Arbor, Michigan, USA Shan Yang *

Biophysics, University of Michigan, Ann Arbor, Michigan, USA Loïc Salmon * Department of Biochemistry and Chemistry, Duke University School of Medicine, Durham, North Carolina, USA Hashim M

Al-Hashimi Authors * Shan Yang View author publications You can also search for this author inPubMed Google Scholar * Loïc Salmon View author publications You can also search for this author

inPubMed Google Scholar * Hashim M Al-Hashimi View author publications You can also search for this author inPubMed Google Scholar CONTRIBUTIONS S.Y., L.S. and H.M.A.-H. conceived the idea;

S.Y. and L.S. carried out the data analysis with help from H.M.A.-H.; S.Y., L.S. and H.M.A.-H. wrote the paper. CORRESPONDING AUTHOR Correspondence to Hashim M Al-Hashimi. ETHICS

DECLARATIONS COMPETING INTERESTS H.M.A.-H. is an advisor to and holds an ownership interest in Nymirum, an RNA-based drug discovery company. SUPPLEMENTARY INFORMATION SUPPLEMENTARY TEXT AND

FIGURES Supplementary Figures 1–7 (PDF 1631 kb) SUPPLEMENTARY SOFTWARE Source code of SAS and ensemble similarity measurement (ZIP 95 kb) SOURCE DATA SOURCE DATA TO FIG. 1 SOURCE DATA TO

FIG. 2 RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Yang, S., Salmon, L. & Al-Hashimi, H. Measuring similarity between dynamic ensembles of

biomolecules. _Nat Methods_ 11, 552–554 (2014). https://doi.org/10.1038/nmeth.2921 Download citation * Received: 04 November 2013 * Accepted: 04 March 2014 * Published: 06 April 2014 * Issue

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