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Structural and dynamics analysis of intrinsically disordered proteins by high-speed atomic force microscopy

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  • 1.

    Romero, P. et al. Thousands of proteins likely to have long disordered regions. Pac. Symp. Biocomp. 3, 437–448 (1998).

    Google Scholar 

  • 2.

    Uversky, V. N., Gillespie, J. R. & Fink, A. L. Why are ‘natively unfolded’ proteins unstructured under physiologic conditions? Proteins 41, 415–427 (2000).

    CAS  Article  Google Scholar 

  • 3.

    Wright, P. E. & Dyson, H. J. Intrinsically disordered proteins in cellular signaling and regulation. Nat. Rev. Mol. Cell Biol. 16, 18–29 (2015).

    CAS  Article  Google Scholar 

  • 4.

    Dyson, H. J. & Wright, P. E. Unfolded proteins and protein folding studied by NMR. Chem. Rev. 104, 3607–3622 (2004).

    CAS  Article  Google Scholar 

  • 5.

    Jensen, M. R., Zweckstetter, M., Huang, J. & Blackledge, M. Exploring free-energy landscapes of intrinsically disordered proteins at atomic resolution using NMR spectroscopy. Chem. Rev. 114, 6632–6660 (2014).

    CAS  Article  Google Scholar 

  • 6.

    Kikhney, A. G. & Svergun, D. I. A practical guide to small angle X-ray scattering (SAXS) of flexible and intrinsically disordered proteins. FEBS Lett. 589, 2570–2577 (2015).

    CAS  Article  Google Scholar 

  • 7.

    Dedmon, M., Lindorff-Larsen, K., Christodoulou, J., Vendruscolo, M. & Dobson, C. M. Mapping long-range interactions in alphasynuclein using spin-label NMR and ensemble molecular dynamics simulations. J. Am. Chem. Soc. 127, 476–477 (2005).

    CAS  Article  Google Scholar 

  • 8.

    Henriques, J., Cragnell, C. & Skepö, M. Molecular dynamics simulations of intrinsically disordered proteins: force field evaluation and comparison with experiment. J. Chem. Theory. Comput. 11, 3420–3431 (2015).

    CAS  Article  Google Scholar 

  • 9.

    Bernadó, P. et al. A structural model for unfolded proteins from residual dipolar couplings and small-angle X-ray scattering. Proc. Natl Acad. Sci. USA 102, 17002–17007 (2005).

    Article  CAS  Google Scholar 

  • 10.

    Ozenne, V. et al. Flexible-meccano: a tool for the generation of explicit ensemble descriptions of intrinsically disordered proteins and their associated experimental observables. Bioinformatics 28, 1463–1470 (2012).

    CAS  Article  Google Scholar 

  • 11.

    Schuler, B., Soranno, A., Hofmann, H. & Nettels, D. Single-molecule FRET spectroscopy and the polymer physics of unfolded and intrinsically disordered proteins. Annu. Rev. Biophys. 45, 207–231 (2016).

    CAS  Article  Google Scholar 

  • 12.

    Borgia, A. et al. Consistent view of polypeptide chain expansion in chemical denaturants from multiple experimental methods. J. Am. Chem. Soc. 138, 11714–11726 (2016).

    CAS  Article  Google Scholar 

  • 13.

    Fuertes, G. et al. Decoupling of size and shape fluctuations in heteropolymeric sequences reconciles discrepancies in SAXS vs. FRET measurements. Proc. Natl Acad. Sci. USA 114, E6342–E6351 (2017).

    CAS  Article  Google Scholar 

  • 14.

    Ando, T. et al. A high-speed atomic force microscope for studying biological macromolecules. Proc. Natl Acad. Sci. USA 98, 12468–12472 (2001).

    CAS  Article  Google Scholar 

  • 15.

    Ando, T., Uchihashi, T. & Fukuma, T. High-speed atomic force microscopy for nano-visualization of dynamic biomolecular processes. Prog. Surf. Sci. 83, 337–437 (2008).

    CAS  Article  Google Scholar 

  • 16.

    Miyagi, A. et al. Visualization of intrinsically disordered regions of proteins by high-speed atomic force microscopy. Chem. Phys. Chem. 9, 1859–1866 (2008).

    CAS  Article  Google Scholar 

  • 17.

    Hashimoto, M. et al. Phosphorylation-coupled intramolecular dynamics of unstructured regions in chromatin remodeler FACT. Biophys. J. 104, 2222–2234 (2013).

    CAS  Article  Google Scholar 

  • 18.

    Uchihashi, T., Iino, R., Ando, T. & Noji, H. High-speed atomic force microscopy reveals rotary catalysis of rotorless F1-ATPase. Science 333, 755–758 (2011).

    CAS  Article  Google Scholar 

  • 19.

    Kodera, N., Yamamoto, T., Ishikawa, R. & Ando, T. Video imaging of walking myosin V by high-speed atomic force microscopy. Nature 468, 72–76 (2010).

    CAS  Article  Google Scholar 

  • 20.

    Ando, T., Uchihashi, T. & Scheuring, S. Filming biomolecular processes by high-speed atomic force microscopy. Chem. Rev. 114, 3120–3188 (2014).

    CAS  Article  Google Scholar 

  • 21.

    Ando, T. High-speed atomic force microscopy. Curr. Opin. Chem. Biol. 51, 105–112 (2019).

    CAS  Article  Google Scholar 

  • 22.

    Takahashi, M. et al. Polyglutamine tract binding protein-1 is an intrinsically unstructured protein. Biochim. Biophys. Acta 1794, 936–943 (2009).

    CAS  Article  Google Scholar 

  • 23.

    de Gennes, P. –G. Scaling Concepts in Polymer Physics (Cornell Univ. Press, 1979).

  • 24.

    Frontali, C. Excluded-volume effect on the bidimensional conformation of DNA molecules adsorbed to protein films. Biopolymers 27, 1329–1331 (1988).

    CAS  Article  Google Scholar 

  • 25.

    Pérez, J., Vachette, P., Russo, D., Desmadril, M. & Durand, D. Heat-induced unfolding of neocarzinostatin, a small all-beta protein investigated by small-angle X-ray scattering. J. Mol. Biol. 308, 721–743 (2001).

    Article  CAS  Google Scholar 

  • 26.

    Iwao, T. Polymer Solutions: An Introduction to Physical Properties (John Wiley & Sons, Inc., 2002).

  • 27.

    Kirk, J. & Ilg, P. Chain dynamics in polymer melts at flat surfaces. Macromolecules 50, 3703–3718 (2017).

    CAS  Article  Google Scholar 

  • 28.

    Yamamoto, H. et al. The intrinsically disordered protein Atg13 mediates supramolecular assembly of autophagy initiation complexes. Dev. Cell 38, 86–99 (2016).

    CAS  Article  Google Scholar 

  • 29.

    Mohan, A. et al. Analysis of molecular recognition features (MoRFs). J. Mol. Biol. 362, 1043–1059 (2006).

    CAS  Article  Google Scholar 

  • 30.

    Jensen, M. R. et al. Intrinsic disorder in measles virus nucleocapsids. Proc. Natl Acad. Sci. USA 108, 9839–9844 (2011).

    CAS  Article  Google Scholar 

  • 31.

    Gely, S. et al. Solution structure of the C‐terminal X domain of the measles virus phosphoprotein and interaction with the intrinsically disordered C‐terminal domain of the nucleoprotein. J. Mol. Recognit. 23, 435–447 (2010).

    CAS  Article  Google Scholar 

  • 32.

    Oldfield, C. J. et al. Coupled folding and binding with α-helix-forming molecular recognition elements. Biochemistry 44, 12454–12470 (2005).

    CAS  Article  Google Scholar 

  • 33.

    Morin, B. et al. Assessing induced folding of an intrinsically disordered protein by site-directed spin-labeling electron paramagnetic resonance spectroscopy. J. Phys. Chem. B. 110, 20596–20608 (2006).

    CAS  Article  Google Scholar 

  • 34.

    Belle, V. et al. Mapping α-helical induced folding within the intrinsically disordered C-terminal domain of the measles virus nucleoprotein by site-directed spin-labeling EPR spectroscopy. Proteins 73, 973–988 (2008).

    CAS  Article  Google Scholar 

  • 35.

    Ormö, M. et al. Crystal structure of the Aequorea victoria green fluorescent protein. Science 273, 1392–1395 (1996).

    Article  Google Scholar 

  • 36.

    Milles, S. et al. An ultraweak interaction in the intrinsically disordered replication machinery is essential for measles virus function. Sci. Adv. 4, eaat7778 (2018).

    CAS  Article  Google Scholar 

  • 37.

    Habchi, J., Mamelli, L., Darbon, H. & Longhi, S. Structural disorder within henipavirus nucleoprotein and phosphoprotein: from predictions to experimental assessment. PLoS ONE 5, e11684 (2010).

    Article  CAS  Google Scholar 

  • 38.

    Brocca, S. et al. Compaction properties of an intrinsically disordered protein: Sic1 and its kinase-inhibitor domain. Biophys. J. 100, 2243–2252 (2011).

    CAS  Article  Google Scholar 

  • 39.

    Riback, J. A. et al. Innovative scattering analysis shows that hydrophobic disordered proteins are expanded in water. Science 358, 238–241 (2017).

    CAS  Article  Google Scholar 

  • 40.

    Kohn, J. E. et al. Random-coil behavior and the dimensions of chemically unfolded proteins. Proc. Natl Acad. Sci. USA 101, 12491–12496 (2004).

    CAS  Article  Google Scholar 

  • 41.

    Meier, S., Grzesiek, S. & Blackledge, M. Mapping the conformational landscape of urea-denatured ubiquitin using residual dipolar couplings. J. Am. Chem. Soc. 129, 9799–9807 (2007).

    CAS  Article  Google Scholar 

  • 42.

    Le Guillo, J. C. & Zinn-Justin, J. Critical exponents for the n-vector model in three dimensions from field theory. Phys. Rev. Lett. 39, 95–98 (1977).

    Article  Google Scholar 

  • 43.

    Cordeiro, T. N. et al. Structural characterization of highly flexible proteins by small-angle scattering. Adv. Exp. Med. Biol. 1009, 107–129 (2017).

    CAS  Article  Google Scholar 

  • 44.

    Boze, H. et al. Proline-rich salivary proteins have extended conformations. Biophys. J. 99, 656–665 (2010).

    CAS  Article  Google Scholar 

  • 45.

    Kate M. Nairn, K. M. et al. A synthetic resilin is largely unstructured. Biophys. J. 95, 3358–3365 (2008).

    Article  CAS  Google Scholar 

  • 46.

    Salmon, L. et al. NMR characterization of long-range order in intrinsically disordered proteins. J. Am. Chem. Soc. 132, 8407–8418 (2010).

    CAS  Article  Google Scholar 

  • 47.

    Mylonas, E. et al. Domain conformation of tau protein studied by solution small-angle X-ray scattering. Biochemistry 47, 10345–10353 (2008).

    CAS  Article  Google Scholar 

  • 48.

    Lanza, D. C. et al. Human FEZ1 has characteristics of a natively unfolded protein and dimerizes in solution. Proteins 74, 104–121 (2009).

    CAS  Article  Google Scholar 

  • 49.

    Bernadó, P. & Blackledge, M. A. Self-consistent description of the conformational behavior of chemically denatured proteins from NMR and small angle scattering. Biophys. J. 97, 2839–2845 (2009).

    Article  CAS  Google Scholar 

  • 50.

    Müller-Späth, S. et al. Charge interactions can dominate the dimensions of intrinsically disordered proteins. Proc. Natl Acad. Sci. USA 107, 14609–14614 (2010).

    Article  Google Scholar 

  • 51.

    Das, R. K., Huang, Y., Phillips, A. H., Kriwacki, R. W. & Pappu, R. V. Cryptic sequence features within the disordered protein p27Kip1 regulate cell cycle signalling. Proc. Natl Acad. Sci. USA 113, 5616–5621 (2016).

    CAS  Article  Google Scholar 

  • 52.

    Sherrya, K. P., Das, R. K., Pappu, R. V. & Barricka, D. Control of transcriptional activity by design of charge patterning in the intrinsically disordered RAM region of the Notch receptor. Proc. Natl Acad. Sci. USA 114, E9243–E9252 (2017).

    Article  CAS  Google Scholar 

  • 53.

    Sambi, I., Gatti–Lafranconi, P., Longhi, S. & Lotti, M. How disorder influences order and vice versa – mutual effects in fusion proteins containing an intrinsically disordered and a globular protein. FEBS J. 277, 4438–4451 (2010).

    CAS  Article  Google Scholar 

  • 54.

    Gruet, A., Longhi, S. & Bignon, C. One-step generation of error-prone PCR libraries using Gateway® technology. Microb Cell Fact. 11, 15 (2012).

    Article  CAS  Google Scholar 

  • 55.

    Gruet, A. et al. Fuzzy regions in an intrinsically disordered protein impair protein-protein interactions. FEBS J. 283, 576–594 (2016).

    CAS  Article  Google Scholar 

  • 56.

    Petoukhov, M. V. et al. New developments in the ATSAS program package for small-angle scattering data analysis. J. Appl. Cryst. 45, 342–350 (2012).

    CAS  Article  Google Scholar 

  • 57.

    Rambo, R. P., John, A. & Tainer, J. A. Accurate assessment of mass, models and resolution by small-angle scattering. Nature 496, 477–481 (2013).

    CAS  Article  Google Scholar 

  • 58.

    Uchihashi, T., Kodera, N. & Ando, T. Guide to video recording of structure dynamics and dynamic processes of proteins by high-speed atomic force microscopy. Nat. Protoc. 7, 1193–1206 (2012).

    CAS  Article  Google Scholar 

  • 59.

    Ngo, K. X., Kodera, N., Katayama, E., Ando, T. & Uyeda, T. Q. P. Cofilin-induced unidirectional cooperative conformational changes in actin filaments revealed by high-speed AFM. eLife 4, e04806 (2015).

    Article  CAS  Google Scholar 

  • Source: https://www.nature.com/articles/s41565-020-00798-9

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