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Licensed Unlicensed Requires Authentication Published by De Gruyter July 7, 2021

Biophysical applications in structural and molecular biology

  • Solomon Tsegaye , Gobena Dedefo and Mohammed Mehdi ORCID logo EMAIL logo
From the journal Biological Chemistry

Abstract

The main objective of structural biology is to model proteins and other biological macromolecules and link the structural information to function and dynamics. The biological functions of protein molecules and nucleic acids are inherently dependent on their conformational dynamics. Imaging of individual molecules and their dynamic characteristics is an ample source of knowledge that brings new insights about mechanisms of action. The atomic-resolution structural information on most of the biomolecules has been solved by biophysical techniques; either by X-ray diffraction in single crystals or by nuclear magnetic resonance (NMR) spectroscopy in solution. Cryo-electron microscopy (cryo-EM) is emerging as a new tool for analysis of a larger macromolecule that couldn’t be solved by X-ray crystallography or NMR. Now a day’s low-resolution Cryo-EM is used in combination with either X-ray crystallography or NMR. The present review intends to provide updated information on applications like X-ray crystallography, cryo-EM and NMR which can be used independently and/or together in solving structures of biological macromolecules for our full comprehension of their biological mechanisms.


Corresponding author: Mohammed Mehdi, Department of Biochemistry, College of Health Sciences, Addis Ababa University, Addis Ababa, Ethiopia, E-mail:

Acknowledgements

We would like to express our deepest heartfelt gratitude to the department of biochemistry, Addis Ababa University.

  1. Author contributions: All authors made a significant contribution to the work reported, whether that is in drafting, revising or critically reviewing the article; gave final approval of the version to be published; have agreed on the journal to which the article has been submitted; and agree to be accountable for all aspects of the work.

  2. Research funding: None declared.

  3. Conflict of interest statement: The authors declare that there is no conflict of interest.

References

Alderson, T.R. and Kay, L.E. (2020). Unveiling invisible protein states with NMR spectroscopy. Curr. Opin. Struct. Biol. 60: 39–49, https://doi.org/10.1016/j.sbi.2019.10.008.Search in Google Scholar

Apostol, M.I., Sawaya, M.R., Cascio, D., and Eisenberg, D. (2010). Crystallographic studies of prion protein (PrP) segments suggest how structural changes encoded by polymorphism at residue 129 modulate susceptibility to human prion disease. J. Biol. Chem. 285: 29671–29675, https://doi.org/10.1074/jbc.c110.158303.Search in Google Scholar

Asano, S., Engel, B.D., and Baumeister, W. (2016). In situ cryo-electron tomography: a post-reductionist approach to structural biology. J. Mol. Biol. 428: 332–343, https://doi.org/10.1016/j.jmb.2015.09.030.Search in Google Scholar

Bai, X.-C., Mcmullan, G., and Scheres, S.H. (2015). How cryo-EM is revolutionizing structural biology. Trends Biochem. Sci. 40: 49–57, https://doi.org/10.1016/j.tibs.2014.10.005.Search in Google Scholar

Barnes, C.A., Robertson, A.J., Louis, J.M., Anfinrud, P., and Bax, A. (2019). Observation of β-amyloid peptide oligomerization by pressure-jump NMR spectroscopy. J. Am. Chem. Soc. 141: 13762–13766, https://doi.org/10.1021/jacs.9b06970.Search in Google Scholar

Bax, A. and Clore, G.M. (2019). Protein NMR: boundless opportunities. J. Magn. Reson. 306: 187–191, https://doi.org/10.1016/j.jmr.2019.07.037.Search in Google Scholar

Bermejo, G.A., Clore, G.M., and Schwieters, C.D. (2016). Improving NMR structures of RNA. Structure 24: 806–815, https://doi.org/10.1016/j.str.2016.03.007.Search in Google Scholar

Bertini, I., Mcgreevy, K.S., and Parigi, G. (2012). NMR and its place in mechanistic systems biology. NMR Biomol. 3.10.1002/9783527644506.ch1Search in Google Scholar

Bijelic, A. and Rompel, A. (2018). Polyoxometalates: more than a phasing tool in protein crystallography. ChemTexts 4: 10, https://doi.org/10.1007/s40828-018-0064-1.Search in Google Scholar

Boland, A., Chang, L., and Barford, D. (2017). The potential of cryo-electron microscopy for structure-based drug design. Essays Biochem. 61: 543–560, https://doi.org/10.1042/ebc20170032.Search in Google Scholar

Bonomi, M., Heller, G.T., Camilloni, C., and Vendruscolo, M. (2017). Principles of protein structural ensemble determination. Curr. Opin. Struct. Biol. 42: 106–116, https://doi.org/10.1016/j.sbi.2016.12.004.Search in Google Scholar

Bonomi, M. and Vendruscolo, M. (2019). Determination of protein structural ensembles using cryo-electron microscopy. Curr. Opin. Struct. Biol. 56: 37–45, https://doi.org/10.1016/j.sbi.2018.10.006.Search in Google Scholar

Brewster, A.S., Bhowmick, A., Bolotovsky, R., Mendez, D., Zwart, P.H., and Sauter, N.K. (2019). SAD phasing of XFEL data depends critically on the error model. Acta Crystallogr. D Struct. Biol. 75: 959–968, https://doi.org/10.1107/s2059798319012877.Search in Google Scholar

Brilot, A.F., Chen, J.Z., Cheng, A., Pan, J., Harrison, S.C., Potter, C.S., Carragher, B., Henderson, R., and Grigorieff, N. (2012). Beam-induced motion of vitrified specimen on holey carbon film. J. Struct. Biol. 177: 630–637, https://doi.org/10.1016/j.jsb.2012.02.003.Search in Google Scholar

Brito, J.A. and Archer, M. (2020). Structural biology techniques: X-ray crystallography, cryo-electron microscopy, and small-angle X-ray scattering. In: Practical approaches to biological inorganic chemistry. Elsevier, New York City.10.1016/B978-0-444-64225-7.00010-9Search in Google Scholar

Burley, S.K., Berman, H.M., Bhikadiya, C., Bi, C., Chen, L., Di Costanzo, L., Christie, C., Dalenberg, K., Duarte, J.M., and Dutta, S. (2019). RCSB Protein Data Bank: biological macromolecular structures enabling research and education in fundamental biology, biomedicine, biotechnology and energy. Nucleic Acids Res. 47: D464–D474, https://doi.org/10.1093/nar/gky1004.Search in Google Scholar

Carroni, M. and Saibil, H.R. (2016). Cryo electron microscopy to determine the structure of macromolecular complexes. Methods 95: 78–85, https://doi.org/10.1016/j.ymeth.2015.11.023.Search in Google Scholar

Chen, P.-C., Shevchuk, R., Strnad, F.M., Lorenz, C., Karge, L., Gilles, R., Stadler, A.M., Hennig, J., and Hub, J.S. (2019). Combined small-angle X-ray and neutron scattering restraints in molecular dynamics simulations. J. Chem. Theor. Comput. 15: 4687–4698, https://doi.org/10.1021/acs.jctc.9b00292.Search in Google Scholar

Cheng, R.K. (2020). Towards an optimal sample delivery method for serial crystallography at XFEL. Crystals 10: 215, https://doi.org/10.3390/cryst10030215.Search in Google Scholar

Cheng, Y. (2015). Single-particle cryo-EM at crystallographic resolution. Cell 161: 450–457, https://doi.org/10.1016/j.cell.2015.03.049.Search in Google Scholar

Cordeiro, T.N., Herranz-Trillo, F., Urbanek, A., Estaña, A., Cortés, J., Sibille, N., and Bernadó, P. (2017a). Small-angle scattering studies of intrinsically disordered proteins and their complexes. Curr. Opin. Struct. Biol. 42: 15–23, https://doi.org/10.1016/j.sbi.2016.10.011.Search in Google Scholar

Cordeiro, T.N., Herranz-Trillo, F., Urbanek, A., Estaña, A., Cortés, J., Sibille, N., and Bernadó, P. (2017b). Structural characterization of highly flexible proteins by small-angle scattering. In: Biological small angle scattering: techniques, strategies and tips. Springer, Singapore.10.1007/978-981-10-6038-0_7Search in Google Scholar PubMed

Cuniasse, P., Tavares, P., Orlova, E.V., and Zinn-Justin, S. (2017). Structures of biomolecular complexes by combination of NMR and cryoEM methods. Curr. Opin. Struct. Biol. 43: 104–113, https://doi.org/10.1016/j.sbi.2016.12.008.Search in Google Scholar

Dahlström, K.M. (2015). From protein structure to function with bioinformatics. Åbo Akademi University, Finland.Search in Google Scholar

Danev, R., Yanagisawa, H., and Kikkawa, M. (2019). Cryo-electron microscopy methodology: current aspects and future directions. Trends Biochem. Sci 44: 837–848, https://doi.org/10.1016/j.tibs.2019.04.008.Search in Google Scholar

Dasgupta, M., Budday, D., De Oliveira, S.H., Madzelan, P., Marchany-Rivera, D., Seravalli, J., Hayes, B., Sierra, R.G., Boutet, S., and Hunter, M.S. (2019). Mix-and-inject XFEL crystallography reveals gated conformational dynamics during enzyme catalysis. Proc. Natl. Acad. Sci. Unit. States Am. 116: 25634–25640, https://doi.org/10.1073/pnas.1901864116.Search in Google Scholar

Dauter, Z. and Jaskolski, M. (2016). Crystal pathologies in macromolecular crystallography. Postepy Biochem. 62: 401–407.10.18388/pb.2016_45Search in Google Scholar

Dona, A., Elena-Herrmann, B., Weljie, A., Keun, H., Wong, A.C.-W., Bathen, T., Wijeyesekera, A., Engelsen, S.B., Verpoorte, R., and Saric, J. (2018). NMR-based metabolomics. Royal Society of Chemistry, London.Search in Google Scholar

Doost, A.S., Akbari, M., Stevens, C.V., Setiowati, A.D., and Van Der Meeren, P. (2019). A review on nuclear overhauser enhancement (NOE) and rotating-frame overhauser effect (ROE) NMR techniques in food science: basic principles and applications. Trends Food Sci. Technol 86: 16–24, https://doi.org/10.1016/j.tifs.2019.02.001.Search in Google Scholar

Drulyte, I., Johnson, R.M., Hesketh, E.L., Hurdiss, D.L., Scarff, C.A., Porav, S.A., Ranson, N.A., Muench, S.P., and Thompson, R.F. (2018). Approaches to altering particle distributions in cryo-electron microscopy sample preparation. Acta Crystallogr. D Struct. Biol. 74: 560–571, https://doi.org/10.1107/s2059798318006496.Search in Google Scholar

Dubochet, J., Adrian, M., Chang, J.-J., Homo, J.-C., Lepault, J., Mcdowall, A.W., and Schultz, P. (1988). Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21: 129–228, https://doi.org/10.1017/s0033583500004297.Search in Google Scholar

Eisenberg, D. and Jucker, M. (2012). The amyloid state of proteins in human diseases. Cell 148: 1188–1203, https://doi.org/10.1016/j.cell.2012.02.022.Search in Google Scholar

Ennifar, E. (2016). Nucleic acid crystallography. Springer, New York City.10.1007/978-1-4939-2763-0Search in Google Scholar

Fernandez-Leiro, R. and Scheres, S.H. (2016). Unravelling biological macromolecules with cryo-electron microscopy. Nature 537: 339–346, https://doi.org/10.1038/nature19948.Search in Google Scholar

Fitzpatrick, A.W., Debelouchina, G.T., Bayro, M.J., Clare, D.K., Caporini, M.A., Bajaj, V.S., Jaroniec, C.P., Wang, L., Ladizhansky, V., and Müller, S.A. (2013). Atomic structure and hierarchical assembly of a cross-β amyloid fibril. Proc. Natl. Acad. Sci. U.S.A. 110: 5468–5473, https://doi.org/10.1073/pnas.1219476110.Search in Google Scholar

Fowler, N.J., Sljoka, A., and Williamson, M.P. (2020). A method for validating the accuracy of NMR protein structures. bioRxiv, https://doi.org/10.1101/2020.04.20.048777.Search in Google Scholar

Gabel, F. (2015). Small-angle neutron scattering for structural biology of protein–RNA complexes. Methods Enzymol 558: 391–415, https://doi.org/10.1016/bs.mie.2015.02.003.Search in Google Scholar

Geraets, J.A., Pothula, K.R., and Schröder, G.F. (2020). Integrating cryo-EM and NMR data. Curr. Opin. Struct. Biol. 61: 173–181, https://doi.org/10.1016/j.sbi.2020.01.008.Search in Google Scholar

Giassa, I.C., Rynes, J., Fessl, T., Foldynova‐Trantirkova, S., and Trantirek, L. (2018). Advances in the cellular structural biology of nucleic acids. FEBS (Fed. Eur. Biochem. Soc.) Lett. 592: 1997–2011, https://doi.org/10.1002/1873-3468.13054.Search in Google Scholar

Harris, J.R. (2015). Transmission electron microscopy in molecular structural biology: a historical survey. Arch. Biochem. Biophys. 581: 3–18, https://doi.org/10.1016/j.abb.2014.11.011.Search in Google Scholar

Gibbs, E.B., Cook, E.C., and Showalter, S.A. (2017). Application of NMR to studies of intrinsically disordered proteins. Arch. Biochem. Biophys. 628: 57–70, https://doi.org/10.1016/j.abb.2017.05.008.Search in Google Scholar

Harris, K.D. (2011). Powder diffraction crystallography of molecular solids. In: Advanced X-ray crystallography. Springer, Berlin, Heidelberg.10.1007/128_2011_251Search in Google Scholar PubMed

Henderson, R., Sali, A., Baker, M.L., Carragher, B., Devkota, B., Downing, K.H., Egelman, E.H., Feng, Z., Frank, J., and Grigorieff, N. (2012). Outcome of the first electron microscopy validation task force meeting. Structure 20: 205–214, https://doi.org/10.1016/j.str.2011.12.014.Search in Google Scholar

Hutchison, C.D. and van Thor, J.J. (2017). Populations and coherence in femtosecond time resolved X-ray crystallography of the photoactive yellow protein. Int. Rev. Phys. Chem. 36: 117–143, https://doi.org/10.1080/0144235x.2017.1276726.Search in Google Scholar

Ikeya, T., Güntert, P., and Ito, Y. (2019). Protein structure determination in living cells from NOE-derived distance restraints. In: In-cell NMR spectroscopy. International Journal of Molecular Science, Australia.10.1039/9781788013079-00063Search in Google Scholar

Ilari, A. and Savino, C. (2008). Protein structure determination by X-ray crystallography. Bioinformatics. Springer. https://doi.org/10.1007/978-1-60327-159-2_3.Search in Google Scholar

Irobalieva, R.N., Martins, B., and Medalia, O. (2016). Cellular structural biology as revealed by cryo-electron tomography. J. Cell Sci. 129: 469–476, https://doi.org/10.1242/jcs.171967.Search in Google Scholar

Jiang, W. and Ludtke, S.J. (2005). Electron cryomicroscopy of single particles at subnanometer resolution. Curr. Opin. Struct. Biol. 15: 571–577, https://doi.org/10.1016/j.sbi.2005.08.004.Search in Google Scholar

Kaplan, M., Pinto, C., Houben, K., and Baldus, M. (2016). Nuclear magnetic resonance (NMR) applied to membrane–protein complexes. Q. Rev. Biophys. 49, https://doi.org/10.1017/S003358351600010X.Search in Google Scholar

Katragadda, M., Alderfer, J.L., and Yeagle, P.L. (2001). Assembly of a polytopic membrane protein structure from the solution structures of overlapping peptide fragments of bacteriorhodopsin. Biophys. J. 81: 1029–1036, https://doi.org/10.1016/s0006-3495(01)75760-8.Search in Google Scholar

Kazemi, S., Würz, J.M., Schmidt, E., Bagaria, A., Güntert, P. (2017). Automated structure determination from NMR spectra. J. Mod. Magn. Reson.: 1–8.10.1007/978-3-319-28275-6_32-1Search in Google Scholar

Kendrew, J.C. (1961). The three-dimensional structure of a protein molecule. Sci. Am. 205: 96–111, https://doi.org/10.1038/scientificamerican1261-96.Search in Google Scholar

Kendrew, J.C., Dickerson, R.E., Strandberg, B.E., Hart, R.G., Davies, D.R., Phillips, D.C., and Shore, V. (1960). Structure of myoglobin: a three-dimensional Fourier synthesis at 2 Å resolution. Nature 185: 422–427, https://doi.org/10.1038/185422a0.Search in Google Scholar

Krueger, S. (2017). Designing and performing biological solution small-angle neutron scattering contrast variation experiments on multi-component assemblies. In: Biological small angle scattering: techniques, strategies and tips. Springer, New York City.10.1007/978-981-10-6038-0_5Search in Google Scholar

Kufareva, I. and Abagyan, R. (2011). Methods of protein structure comparison. In: Homology modeling. Springer, New York City.10.1007/978-1-61779-588-6_10Search in Google Scholar PubMed PubMed Central

Lander, G.C., Saibil, H.R., and Nogales, E. (2012). Go hybrid: EM, crystallography, and beyond. Curr. Opin. Struct. Biol. 22: 627–635, https://doi.org/10.1016/j.sbi.2012.07.006.Search in Google Scholar

Landreh, M., Sawaya, M.R., Hipp, M.S., Eisenberg, D.S., Wüthrich, K., and Hartl, F.U. (2016). The formation, function and regulation of amyloids: insights from structural biology. J. Intern. Med. 280: 164–176, https://doi.org/10.1111/joim.12500.Search in Google Scholar

Lian, L.-Y. and Roberts, G. (2011). Protein NMR spectroscopy: practical techniques and applications. John Wiley & Sons, Hoboken, New Jersey.10.1002/9781119972006Search in Google Scholar

Liu, Y., Saurí, J., Mevers, E., Peczuh, M.W., Hiemstra, H., Clardy, J., Martin, G.E., and Williamson, R.T. (2017). Unequivocal determination of complex molecular structures using anisotropic NMR measurements. Science 356: eaam5349, https://doi.org/10.1126/science.aam5349.Search in Google Scholar

Liu, H. and Spence, J.C. (2016). XFEL data analysis for structural biology. Quant. Biol. 4: 159–176, https://doi.org/10.1007/s40484-016-0076-z.Search in Google Scholar

Lipfert, J., Chu, V.B., Bai, Y., Herschlag, D., and Doniach, S. (2007). Low-resolution models for nucleic acids from small-angle X-ray scattering with applications to electrostatic modeling. Appl. Crystallogr. 40: s229–s234, https://doi.org/10.1107/s0021889807001707.Search in Google Scholar

Liu, W., Wacker, D., Wang, C., Abola, E., and Cherezov, V. (2014). Femtosecond crystallography of membrane proteins in the lipidic cubic phase. Phil. Trans. Biol. Sci. 369: 20130314, https://doi.org/10.1098/rstb.2013.0314.Search in Google Scholar

Lu, J.-X., Qiang, W., Yau, W.-M., Schwieters, C.D., Meredith, S.C., and Tycko, R. (2013). Molecular structure of β-amyloid fibrils in Alzheimer’s disease brain tissue. Cell 154: 1257–1268, https://doi.org/10.1016/j.cell.2013.08.035.Search in Google Scholar

Luchinat, E. and Banci, L. (2017). In-cell NMR: a topical review. IUCrJ 4: 108–118, https://doi.org/10.1107/s2052252516020625.Search in Google Scholar

Luque, D. and Castón, J.R. (2020). Cryo-electron microscopy for the study of virus assembly. Nat. Chem. Biol. 16: 231–239, https://doi.org/10.1038/s41589-020-0477-1.Search in Google Scholar

Lyubimov, A.Y., Uervirojnangkoorn, M., Zeldin, O.B., Zhou, Q., Zhao, M., Brewster, A.S., Michels-Clark, T., Holton, J.M., Sauter, N.K., and Weis, W.I. (2016). Advances in X-ray free electron laser (XFEL) diffraction data processing applied to the crystal structure of the synaptotagmin-1/SNARE complex. Elife 5: e18740, https://doi.org/10.7554/eLife.18740.Search in Google Scholar

Mahieu, E. and Gabel, F. (2018). Biological small-angle neutron scattering: recent results and development. Acta Crystallogr. D: Struct. Biol. 74: 715–726, https://doi.org/10.1107/s2059798318005016.Search in Google Scholar

Markley, J.L., Brüschweiler, R., Edison, A.S., Eghbalnia, H.R., Powers, R., Raftery, D., and Wishart, D.S. (2017). The future of NMR-based metabolomics. Curr. Opin. Biotechnol. 43: 34–40, https://doi.org/10.1016/j.copbio.2016.08.001.Search in Google Scholar

Markwick, P.R., Malliavin, T., and Nilges, M. (2008). Structural biology by NMR: structure, dynamics, and interactions. PLoS Comput. Biol. 4, https://doi.org/10.1371/journal.pcbi.1000168.Search in Google Scholar

Merk, A., Bartesaghi, A., Banerjee, S., Falconieri, V., Rao, P., Davis, M.I., Pragani, R., Boxer, M.B., Earl, L.A., and Milne, J.L. (2016). Breaking cryo-EM resolution barriers to facilitate drug discovery. Cell 165: 1698–1707, https://doi.org/10.1016/j.cell.2016.05.040.Search in Google Scholar

Mooers, B.H. (2009). Crystallographic studies of DNA and RNA. Methods 47: 168–176, https://doi.org/10.1016/j.ymeth.2008.09.006.Search in Google Scholar

Murata, K. and Wolf, M. (2018). Cryo-electron microscopy for structural analysis of dynamic biological macromolecules. Biochim. Biophys. Acta Gen. Subj. 1862: 324–334, https://doi.org/10.1016/j.bbagen.2017.07.020.Search in Google Scholar

Mureddu, L. and Vuister, G.W. (2019). Simple high‐resolution NMR spectroscopy as a tool in molecular biology. FEBS J. 286: 2035–2042, https://doi.org/10.1111/febs.14771.Search in Google Scholar

Murthy, A.C. and Fawzi, N.L. (2020). The (un) structural biology of biomolecular liquid-liquid phase separation using NMR spectroscopy. J. Biol. Chem. 295: 2375–2384, https://doi.org/10.1074/jbc.REV119.009847.Search in Google Scholar

Nogales, E. (2016). The development of cryo-EM into a mainstream structural biology technique. Nat. Methods 13: 24–27, https://doi.org/10.1038/nmeth.3694.Search in Google Scholar

Ooi, L.-L. (2010). Principles of X-ray crystallography. Oxford University Press, Oxford, England.Search in Google Scholar

Petkova, A.T., Yau, W.-M., and Tycko, R. (2006). Experimental constraints on quaternary structure in Alzheimer’s β-amyloid fibrils. Biochemistry 45: 498–512, https://doi.org/10.1021/bi051952q.Search in Google Scholar

Qian, S., Pingali, S.V., Weiss, K.L., Urban, V., O’neill, H.M., and Langan, P. (2016). Neutron scattering for biological research: progress at the bio-SANS beam line. Oak Ridge National Lab.(ORNL), Oak ridge, TN (United States). High flux ….Search in Google Scholar

Rigden, D.J. and Rigden, D.J. (2009). From protein structure to function with bioinformatics. Springer, New York City.10.1007/978-1-4020-9058-5Search in Google Scholar

Roche, J., Royer, C.A., and Roumestand, C. (2017). Monitoring protein folding through high pressure NMR spectroscopy. Prog. Nucl. Magn. Reson. Spectrosc. 102: 15–31, https://doi.org/10.1016/j.pnmrs.2017.05.003.Search in Google Scholar

Schindler, T., González, A., Boopathi, R., Roda, M.M., Romero-Santacreu, L., Wildes, A., Porcar, L., Martel, A., Theodorakopoulos, N., and Cuesta-López, S. (2018). Kinky DNA in solution: small-angle-scattering study of a nucleosome positioning sequence. Phys. Rev. 98: 042417, https://doi.org/10.1103/physreve.98.042417.Search in Google Scholar

Schnieders, R., Keyhani, S., Schwalbe, H., and Fürtig, B. (2020). More than proton detection—new avenues for NMR spectroscopy of RNA. Chemistry 26: 102–113, https://doi.org/10.1002/chem.201903355.Search in Google Scholar

Sheng, J. and Huang, Z. (2008). Selenium derivatization of nucleic acids for phase and structure determination in nucleic acid X-ray crystallography. Int. J. Mol. Sci. 9: 258–271, https://doi.org/10.3390/ijms9030258.Search in Google Scholar

Spence, J. (2017). XFELs for structure and dynamics in biology. IUCrJ 4: 322–339, https://doi.org/10.1107/s2052252517005760.Search in Google Scholar

Stewart, P.L. (2017). Cryo‐electron microscopy and cryo‐electron tomography of nanoparticles. Wiley Interdiscipl. Rev.: Nanomed. Nanobiotechnol. 9: e1417, https://doi.org/10.1002/wnan.1417.Search in Google Scholar

Takayama, Y. and Yonekura, K. (2016). Cryogenic coherent X-ray diffraction imaging of biological samples at SACLA: a correlative approach with cryo-electron and light microscopy. Acta Crystallogr. A Found. Adv. 72: 179–189, https://doi.org/10.1107/s2053273315023980.Search in Google Scholar

Thompson, R.F., Walker, M., Siebert, C.A., Muench, S.P., and Ranson, N.A. (2016). An introduction to sample preparation and imaging by cryo-electron microscopy for structural biology. Methods 100: 3–15, https://doi.org/10.1016/j.ymeth.2016.02.017.Search in Google Scholar

Thonghin, N., Kargas, V., Clews, J., and Ford, R.C. (2018). Cryo-electron microscopy of membrane proteins. Methods 147: 176–186, https://doi.org/10.1016/j.ymeth.2018.04.018.Search in Google Scholar

Tschentscher, T., Bressler, C., Grünert, J., Madsen, A., Mancuso, A.P., Meyer, M., Scherz, A., Sinn, H., and Zastrau, U. (2017). Photon beam transport and scientific instruments at the European XFEL. Appl. Sci. 7: 592, https://doi.org/10.3390/app7060592.Search in Google Scholar

Tuukkanen, A.T., Kleywegt, G.J., and Svergun, D.I. (2016). Resolution of ab initio shapes determined from small-angle scattering. IUCrJ 3: 440–447, https://doi.org/10.1107/s2052252516016018.Search in Google Scholar

Tycko, R. (2015). Amyloid polymorphism: structural basis and neurobiological relevance. Neuron 86: 632–645, https://doi.org/10.1016/j.neuron.2015.03.017.Search in Google Scholar

Tycko, R. and Wickner, R.B. (2013). Molecular structures of amyloid and prion fibrils: consensus versus controversy. Acc. Chem. Res. 46: 1487–1496, https://doi.org/10.1021/ar300282r.Search in Google Scholar

Uervirojnangkoorn, M., Zeldin, O.B., Lyubimov, A.Y., Hattne, J., Brewster, A.S., Sauter, N.K., Brunger, A.T., and Weis, W.I. (2015). Enabling X-ray free electron laser crystallography for challenging biological systems from a limited number of crystals. eLife 4: e05421, https://doi.org/10.7554/eLife.05421.Search in Google Scholar

Van Benschoten, A.H., Liu, L., Gonzalez, A., Brewster, A.S., Sauter, N.K., Fraser, J.S., and Wall, M.E. (2016). Measuring and modeling diffuse scattering in protein X-ray crystallography. Proc. Natl. Acad. Sci. U.S.A. 113: 4069–4074, https://doi.org/10.1073/pnas.1524048113.Search in Google Scholar

Van Den Bedem, H. and Fraser, J.S. (2015). Integrative, dynamic structural biology at atomic resolution-it’s about time. Nat. Methods 12: 307, https://doi.org/10.1038/nmeth.3324.Search in Google Scholar

Van Der Wel, P.C. (2018). New applications of solid-state NMR in structural biology. Emerg. Top. Life Sci. 2: 57–67, https://doi.org/10.1042/etls20170088.Search in Google Scholar

Van Melckebeke, H., Wasmer, C., Lange, A., Ab, E., Loquet, A., BöCkmann, A., and Meier, B.H. (2010). Atomic-resolution three-dimensional structure of HET-s (218− 289) amyloid fibrils by solid-state NMR spectroscopy. J. Am. Chem. Soc. 132: 13765–13775, https://doi.org/10.1021/ja104213j.Search in Google Scholar

Vénien-Bryan, C., Li, Z., Vuillard, L., and Boutin, J.A. (2017). Cryo-electron microscopy and X-ray crystallography: complementary approaches to structural biology and drug discovery. Acta Crystallogr. F Struct. Biol. Commun. 73: 174–183, https://doi.org/10.1107/s2053230x17003740.Search in Google Scholar

Wan, W. and Briggs, J. (2016). Cryo-electron tomography and subtomogram averaging. Methods Enzymol 579: 329–367, https://doi.org/10.1016/bs.mie.2016.04.014.Search in Google Scholar

Wang, H.W. and Wang, J.W. (2017). How cryo‐electron microscopy and X‐ray crystallography complement each other. Protein Sci. 26: 32–39, https://doi.org/10.1002/pro.3022.Search in Google Scholar

Wickstrand, C. (2019). Production and structural dynamics of microbial rhodopsins. University of Gothenburg, Gothenburg.Search in Google Scholar

Wickstrand, C., Nogly, P., Nango, E., Iwata, S., Standfuss, J., and Neutze, R. (2019). Bacteriorhodopsin: structural insights revealed using X-ray lasers and synchrotron radiation. Annu. Rev. Biochem. 88: 59–83, https://doi.org/10.1146/annurev-biochem-013118-111327.Search in Google Scholar

Williams, B., Zhao, B., Tandon, A., Ding, F., Weeks, K.M., Zhang, Q., and Dokholyan, N.V. (2017). Structure modeling of RNA using sparse NMR constraints. Nucleic Acids Res. 45: 12638–12647, https://doi.org/10.1093/nar/gkx1058.Search in Google Scholar

Xu, Z., Liu, C., Zhao, S., Chen, S., and Zhao, Y. (2018). Molecular sensors for NMR-based detection. Chem. Rev. 119: 195–230, https://doi.org/10.1021/acs.chemrev.8b00202.Search in Google Scholar

Yao, Y. (2017). Comparing two NMR structure refinement methods. Rutgers University-School of Graduate Studies, New Brunswick/Piscataway, USA.Search in Google Scholar

Zhang, W., Szostak, J.W., and Huang, Z. (2016). Nucleic acid crystallization and X-ray crystallography facilitated by single selenium atom. Front. Chem. Sci. Eng. 10: 196–202, https://doi.org/10.1007/s11705-016-1565-3.Search in Google Scholar

Zheng, S., Palovcak, E., Armache, J.-P., Cheng, Y., and Agard, D. (2017). MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14: 331–332, 061960, https://doi.org/10.1038/nmeth.4193.Search in Google Scholar

Received: 2021-04-15
Accepted: 2021-05-27
Published Online: 2021-07-07
Published in Print: 2021-09-27

© 2021 Walter de Gruyter GmbH, Berlin/Boston

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