Continuous changes in structure mapped by manifold embedding of single-particle data in cryo-EM

Methods

Volumn 100, Issue , 2016, Pages 61-67

  Frank, Joachim ^a   Ourmazd, Abbas ^b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

Classification; Heterogeneity; Machine learning; Molecular machines; Protein synthesis; Ribosome

Indexed keywords

CHAPERONE; PROTEASOME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; RNA POLYMERASE; FUNGAL PROTEIN;

ARTICLE; CELL ELONGATION; CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; EMBEDDING; IN VITRO STUDY; MACROMOLECULE; MATHEMATICAL COMPUTING; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; RIBOSOME; RNA TRANSPORT; SEPARATION TECHNIQUE; X RAY CRYSTALLOGRAPHY; YEAST; MOLECULAR MODEL; PROCEDURES; THREE DIMENSIONAL IMAGING; ULTRASTRUCTURE;

CRYOELECTRON MICROSCOPY; FUNGAL PROTEINS; IMAGING, THREE-DIMENSIONAL; MODELS, MOLECULAR; RIBOSOMES; YEASTS;

EID: 84959133785     PISSN: 10462023     EISSN: 10959130     Source Type: Journal    
DOI: 10.1016/j.ymeth.2016.02.007     Document Type: Article

References (51)

1. Nogales E., Scheres S.H.W. Cryo-EM: a unique tool for the visualization of macromolecular complexity. Mol. Cell 2015, 58:677-689.
2. Fischer N., Neumann P., Konevega A.L., Bock L.V., Ficner R., Rodnina M.V., Stark H. Structure of the E. coli ribosome-EF-Tu complex at <3 Å resolution by Cs-corrected cryo-EM. Nature 2015, 520:567-570.
3. Z. Liu, J. Wei, C. Gutierrez-Vargas, M. Sun, N. Espina, S. Madison-Antenucci, L. Tong, J. Frank, Cryo-EM structure of the Trypanosoma cruzi ribosome at 2.5 Å (2016), Submitted.
4. Frank J. Story in a sample-the potential (and limitations) of cryo-electron microscopy applied to molecular machines. Biopolymers 2013, 99:832-836.
5. Scheres S.H.W., Gao H., Valle M., Herman G.T., Eggermont P.P.B., Frank J., Carazo J.-M. Disentangling conformational states of macromolecules in 3D-EM through likelihood optimization. Nat. Methods 2007, 4:27-29.
6. Sigworth F.J. From cryo-EM, multiple protein structures in one shot. Nat. Methods 2007, 4:20-21.
7. Valle M., Sengupta J., Swami N.K., Grassucci R.A., Burkhardt N., Nierhaus K.H., Agrawal R.K., Frank J. Cryo-EM reveals an active role for aminoacyl-tRNA in the accommodation process. EMBO J. 2002, 21:3557-3567.
8. Leschziner A.E., Nogales E. Visualizing flexibility at molecular resolution: analysis of heterogeneity in single-particle electron microscopy reconstructions. Annu. Rev. Biophys. Biomol. Struct. 2007, 36:43-62.
9. Elad N., Clare D.K., Saibil H.R., Orlova E.V. Detection and separation of heterogeneity in molecular complexes by statistical analysis of their two-dimensional projections. J. Struct. Biol. 2008, 162:108-120.
10. Herman G.T., Kalinowski M. Classification of heterogeneous electron microscopic projections into homogeneous subsets. Ultramicroscopy 2008, 108:327-338.
11. Zhang W., Kimmel M., Spahn C.M.T., Penczek P.A. Heterogeneity of large macromolecular complexes revealed by 3-D cryo-EM variance analysis. Structure 2008, 16:1770-1776.
12. Elmlund D., Davis R., Elmlund H. Ab initio structure determination from electron microscopic images of single molecules coexisting in different functional states. Structure 2010, 18:777-786.
13. Shatsky M., Hall R.J., Nogales E., Malik J., Brenner S.E. Automated multi-model reconstruction from single-particle electron microscopy data. J. Struct. Biol. 2010, 170:98-108.
14. Lyumkis D., Brilot A.F., Theobald D.L., Grigorieff N. Likelihood-based classification of cryo-EM images using FREALIGN. J. Struct. Biol. 2013, 183:377-388.
15. Behrmann E., Loerke J., Budkevich T.V., Yamamoto K., Schmidt A., Penczek P.A., Vos M.R., Bürger J., Mielke T., Scheerer P., Spahn C.M. Structural snapshots of actively translating human ribosomes. Cell 2015, 161:845-857.
16. Scheres S.H.W. A Bayesian view on cryo-EM structure determination. J. Mol. Biol. 2012, 415:406-418.
17. Scheres S.H.W. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 2012, 180:519-530.
18. Agirrezabala X., Liao H.Y., Schreiner E., Fu J., Ortiz-Meoz R.F., Schulten K., Green R., Frank J. Structural characterization of mRNA-tRNA translocation intermediates. Proc. Natl. Acad. Sci. USA 2012, 109:6094-6099.
19. Liao M., Cao E., Julius D., Cheng Y. Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 2013, 504:107-112.
20. Hashem Y., des Georges A., Dhote V., Langlois R., Liao H.Y., Grassucci R.A., Hellen C.U.T., Pestova T.V., Frank J. Structure of the mammalian ribosomal 43S preinitiation complex bound to the scanning factor DHX29. Cell 2013, 153:1108-1119.
21. Amunts A., Brown A., Toots J., Scheres S.H.W., Ramakrishnan V. The structure of the human mitochondrial ribosome. Science 2015, 348:95-98.
22. Li W., Liu Z., Koripella R.K., Langlois R., Sanyal S., Frank J. Activation of GTP hydrolysis in mRNA-tRNA translocation by Elongation Factor G. Sci. Adv. 2015, 1.
23. Zalk R., Clarke O.B., des Georges A., Grassucci R.A., Reiken S., Mancia F., Hendrickson W.A., Frank J., Marks A.R. Structure of a mammalian ryanodine receptor. Nature 2015, 517:44-49.
24. Chen B., Shen B., Frank J. Particle migration analysis in iterative classification of cryo-EM single-particle data. J. Struct. Biol. 2014, 188:267-273.
25. Shen B., Chen B., Liao H., Frank J. Quantitative analysis in iterative classification schemes for cryo-EM applications. Computational Methods for Three-dimensional Microscopy Reconstruction 2014, 67-95. Birkhauser, Basel. G.T. Herman, J. Frank (Eds.).
26. Hashem Y., des Georges A., Dhote V., Langlois R., Liao H.Y., Grassucci R.A., Pestova T.V., Hellen C.U.T., Frank J. Hepatitis-C-virus-like internal ribosome entry sites displace eIF3 to gain access to the 40S subunit. Nature 2013, 503:539-543.
27. Zhao J., Benlekbir S., Rubinstein J.L. Electron cryomicroscopy observation of rotational states in a eukaryotic V-ATPase. Nature 2015, 521:241-245.
28. Dashti A., Schwander P., Langlois R., Fung R., Li W., Hosseinizadeh A., Liao H.Y., Pallesen J., Sharma G., Stupina V.A., Simon A.E., Dinman J.D., Frank J., Ourmazd A. Trajectories of the ribosome as a brownian nanomachine. Proc. Natl. Acad. Sci. USA 2014, 111:17492-17497.
29. Chen B., Frank J. Two promising future developments of cryo-EM: capturing short-lived states and mapping a continuum of states of a macromolecule. Microscopy 2015, 2015:1-11. 10.1093/jmicro/dfv344.
30. van Heel M., Frank J. Use of multivariates statistics in analysing the images of biological macromolecules. Ultramicroscopy 1981, 6:187-194.
31. Frank J., van Heel M. Correspondence analysis of aligned images of biological particles. J. Mol. Biol. 1982, 161:134-137.
32. Fu J., Gao H., Frank J. Unsupervised classification of single particles by cluster tracking in multi-dimensional space. J. Struct. Biol. 2007, 157:226-239.
33. Fung R., Shneerson, Saldin D.K., Ourmazd A. Structure from fleeting illumination of faint spinning objects in flight. Nat. Phys. 2009, 5:64-67.
34. Moths B., Ourmazd A. Bayesian algorithms for recovering structure from single-particle diffraction snapshots of unknown orientation: a comparison. Acta Crystallogr. A 2011, 76:481-486.
35. Schwander P., Fung R., Ourmazd A. Conformations of macromolecules and their complexes from heterogeneous datasets. Philos. Trans. R. Soc. B 2014, 369:20130567.
36. Riemann B. Uber die Hypothesen, welche der Geometrie zu Grunde liegen. Abhandlungen der Königlichen Gesellschaft der Wissenschaften zu Göttingen 1867, vol. 13.
37. Giannakis D., Majda A. Nonlinear Laplacian spectral analysis. Proc. Natl. Acad. Sci. USA 2012, 109:2222-2227.
38. Frank J., Agrawal R.K. A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 2000, 406:318-322.
39. Valle M., Zavialov A., Sengupta J., Rawat U., Ehrenberg M., Frank J. Locking and unlocking of ribosomal motions. Cell 2003, 114:123-134.
40. Cornish P.V., Ermolenko D.N., Noller H.F., Ha T. Spontaneous intersubunit rotation in single ribosomes. Mol. Cell 2008, 30:578-588.
41. Agirrezabala X., Lei J., Brunelle J.L., Ortiz-Meoz R.F., Green R., Frank J. Visualization of the hybrid state of tRNA binding promoted by spontaneous ratcheting of the ribosome. Mol. Cell 2008, 32:190-197.
42. Julian P., Konevega A.L., Scheres S.H., Lazaro M., Gil D., Wintermeyer W., Rodnina M.V., Valle M. Structure of ratcheted ribosomes with tRNAs in hybrid states. Proc. Natl. Acad. Sci. USA 2008, 105:16924-16927.
43. Fischer N., Konevega A.L., Wintermeyer W., Rodnina M.V., Stark H. Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy. Nature 2010, 466:329-333.
44. Noel J.K., Chahine J., Leite V.B.P., Whitford P.C. Capturing transition paths and transition states for conformational rearrangements in the ribosome. Biophys. J. 2014, 107:2872-2881.
45. Korostelev A., Ermolenko D.N., Noller H.F. Structural dynamics of the ribosome. Curr. Opin. Chem. Biol. 2008, 12:674-683.
46. Dunkle J.A., Cate J.H.D. Ribosome structure and dynamics during translocation and termination. Annu. Rev. Biophys. 2010, 39:227-244.
47. Frank J., Gonzalez R.L. Structure and dynamics of a processive Brownian motor: the translating ribosome. Annu. Rev. Biochem. 2010, 79:381-412.
48. Ramakrishnan V. Ribosome structure and the mechanism of translation. Cell 2002, 108:557-572.
49. Fei J., Kosuri P., MacDougall D.D., Gonzalez R.L. Coupling of ribosomal L1 stalk and tRNA dynamics during translation elongation. Mol. Cell 2008, 30:348-359.
50. Ratje A.H., Loerke J., Mikolajka A., Brünner M., Hildebrand P.W., Starosta A.L., Dönhöfer A., Connell S.R., Fucini P., Mielke T., Whitford P.C., Onuchic J.N., Yu Yanan Y., Sanbonmatsu Y.K., Hartmann R.K., Penczek P.A., Wilson D.N., Spahn C.M.T. Head swivel on the ribosome facilitates translocation via intra-subunit tRNA hybrid sites. Nature 2010, 468:713-716.
51. Frank J. The dynamics of the ribosome as inferred by cryo-EM: induced and self-organized motions. Conformational Proteomics of Macromolecular Architecture 2004, 291-306. World Scientific, Singapore. R.H. Cheng, L. Hammar (Eds.).