Spatiotemporal dynamics of the nuclear pore complex transport barrier resolved by high-speed atomic force microscopy (original) (raw)

References

  1. Grünwald, D., Singer, R. H. & Rout, M. Nuclear export dynamics of RNA-protein complexes. Nature 475, 333–341 (2011).
    Article Google Scholar
  2. Popken, P., Ghavami, A., Onck, P. R., Poolman, B. & Veenhoff, L. M. Size-dependent leak of soluble and membrane proteins through the yeast nuclear pore complex. Mol. Biol. Cell 26, 1386–1394 (2015).
    Article CAS Google Scholar
  3. Yamada, J. et al. A bimodal distribution of two distinct categories of intrinsically disordered structures with separate functions in FG nucleoporins. Mol. Cell. Proteomics 9, 2205–2224 (2010).
    Article CAS Google Scholar
  4. Stoffler, D. et al. Cryo-electron tomography provides novel insights into nuclear pore architecture Implications for nucleocytoplasmic transport. J. Mol. Biol. 328, 119–130 (2003).
    Article CAS Google Scholar
  5. Beck, M. et al. Nuclear pore complex structure and dynamics revealed by cryoelectron tomography. Science 306, 1387–1390 (2004).
    Article CAS Google Scholar
  6. Eibauer, M. et al. Structure and gating of the nuclear pore complex. Nature Commun. 6, 7532 (2015).
    Article CAS Google Scholar
  7. Rout, M. P. et al. The yeast nuclear pore complex: composition, architecture, and transport mechanism. J. Cell Biol. 148, 635–651 (2000).
    Article CAS Google Scholar
  8. Rout, M. P., Aitchison, J. D., Magnasco, M. O. & Chait, B. T. Virtual gating and nuclear transport: the hole picture. Trends Cell Biol. 13, 622–628 (2003).
    Article CAS Google Scholar
  9. Lim, R. Y. H. et al. Flexible phenylalanine-glycine nucleoporins as entropic barriers to nucleocytoplasmic transport. Proc. Natl Acad. Sci. USA 103, 9512–9517 (2006).
    Article CAS Google Scholar
  10. Lim, R. Y. H. et al. Nanomechanical basis of selective gating by the nuclear pore complex. Science 318, 640–643 (2007).
    Article CAS Google Scholar
  11. Frey, S. & Görlich, D. A saturated FG-repeat hydrogel can reproduce the permeability properties of nuclear pore complexes. Cell 130, 512–523 (2007).
    Article CAS Google Scholar
  12. Hülsmann, B. B., Labokha, A. A. & Görlich, D. The permeability of reconstituted nuclear pores provides direct evidence for the selective phase model. Cell 150, 738–751 (2012).
    Article Google Scholar
  13. Akey, C. W. Visualization of transport-related configurations of the nuclear-pore transporter. Biophys. J. 58, 341–355 (1990).
    Article CAS Google Scholar
  14. Dange, T., Grünwald, D., Grünwald, A., Peters, R. & Kubitscheck, U. Autonomy and robustness of translocation through the nuclear pore complex A single-molecule study. J. Cell Biol. 183, 77–86 (2008).
    Article CAS Google Scholar
  15. Fahrenkrog, B. et al. Domain-specific antibodies reveal multiple-site topology of Nup153 within the nuclear pore complex. J. Struct. Biol. 140, 254–267 (2002).
    Article CAS Google Scholar
  16. Stoffler, D., Goldie, K. N., Feja, B. & Aebi, U. Calcium-mediated structural changes of native nuclear pore complexes monitored by time-lapse atomic force microscopy. J. Mol. Biol. 287, 741–752 (1999).
    Article CAS Google Scholar
  17. Bestembayeva, A. et al. Nanoscale stiffness topography reveals structure and mechanics of the transport barrier in intact nuclear pore complexes. Nature Nanotech. 10, 60–64 (2015).
    Article CAS Google Scholar
  18. Kramer, A., Liashkovich, I., Ludwig, Y. & Shahin, V. Atomic force microscopy visualises a hydrophobic meshwork in the central channel of the nuclear pore. Pflugers Arch. 456, 155–162 (2008).
    Article CAS Google Scholar
  19. Cardarelli, F., Lanzano, L. & Gratton, E. Capturing directed molecular motion in the nuclear pore complex of live cells. Proc. Natl Acad. Sci. USA 109, 9863–9868 (2012).
    Article CAS Google Scholar
  20. Ma, J., Goryaynov, A., Sarma, A. & Yang, W. Self-regulated viscous channel in the nuclear pore complex. Proc. Natl Acad. Sci. USA 109, 7326–7331 (2012).
    Article CAS Google Scholar
  21. Ma, J., Goryaynov, A. & Yang, W. Super-resolution 3D tomography of interactions and competition in the nuclear pore complex. Nature Struct. Mol. Biol. 23, 239–247 (2016).
    Article CAS Google Scholar
  22. 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).
    Article CAS Google Scholar
  23. Uchihashi, T., Kodera, N. & Ando, T. Guide to video recording of structure dynamics and dynamic processes of proteins by high-speed atomic force microscopy. Nature Protoc. 7, 1193–1206 (2012).
    Article CAS Google Scholar
  24. Kodera, N., Yamamoto, D., Ishikawa, R. & Ando, T. Video imaging of walking myosin V by high-speed atomic force microscopy. Nature 468, 72–76 (2010).
    Article CAS Google Scholar
  25. Uchihashi, T., Iino, R., Ando, T. & Noji, H. High-speed atomic force microscopy reveals rotary catalysis of rotorless F-1-ATPase. Science 333, 755–758 (2011).
    Article CAS Google Scholar
  26. Miyagi, A. et al. Visualization of intrinsically disordered regions of proteins by high-speed atomic force microscopy. ChemPhysChem 9, 1859–1866 (2008).
    Article CAS Google Scholar
  27. Chatel, G., Desai, S. H., Mattheyses, A. L., Powers, M. A. & Fahrenkrog, B. Domain topology of nucleoporin Nup98 within the nuclear pore complex. J. Struct. Biol. 177, 81–89 (2012).
    Article CAS Google Scholar
  28. Kapinos, L. E., Schoch, R. L., Wagner, R. S., Schleicher, K. D. & Lim, R. Y. H. Karyopherin-centric control of nuclear pores based on molecular occupancy and kinetic analysis of multivalent binding with FG nucleoporins. Biophys. J. 106, 1751–1762 (2014).
    Article CAS Google Scholar
  29. Vesenka, J., Manne, S., Giberson, R., Marsh, T. & Henderson, E. Colloidal gold particles as an incompressible atomic-force microscope imaging standard for assessing the compressibility of biomolecules. Biophys. J. 65, 992–997 (1993).
    Article CAS Google Scholar
  30. Chattopadhyay, K., Elson, E. L. & Frieden, C. The kinetics of conformational fluctuations in an unfolded protein measured by fluorescence methods. Proc. Natl Acad. Sci. USA 102, 2385–2389 (2005).
    Article CAS Google Scholar
  31. Windisch, B., Bray, D. & Duke, T. Balls and chains - A mesoscopic approach to tethered protein domains. Biophys. J. 91, 2383–2392 (2006).
    Article CAS Google Scholar
  32. Kusumi, A., Sako, Y. & Yamamoto, M. Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophys. J. 65, 2021–2040 (1993).
    Article CAS Google Scholar
  33. Schmidt, H. B. & Görlich, D. Nup98 FG domains from diverse species spontaneously phase-separate into particles with nuclear pore-like permselectivity. eLife 4, e04251 (2015).
    Article Google Scholar
  34. Osmanovic, D. et al. Bistable collective behavior of polymers tethered in a nanopore. Phys. Rev. E 85, 061917 (2012).
    Article Google Scholar
  35. Grünwald, D. & Singer, R. H. In vivo imaging of labelled endogenous b-actin mRNA during nucleocytoplasmic transport. Nature 467, 604–609 (2010).
    Article Google Scholar
  36. Tagliazucchi, M., Peleg, O., Kroger, M., Rabin, Y. & Szleifer, I. Effect of charge, hydrophobicity, and sequence of nucleoporins on the translocation of model particles through the nuclear pore complex. Proc. Natl Acad. Sci. USA 110, 3363–3368 (2013).
    Article CAS Google Scholar
  37. Ando, D. et al. Nuclear pore complex protein sequences determine overall copolymer brush structure and function. Biophys. J. 106, 1997–2007 (2014).
    Article CAS Google Scholar
  38. Ghavami, A., Veenhoff, L. M., van der Giessen, E. & Onck, P. R. Probing the disordered domain of the nuclear pore complex through coarse-grained molecular dynamics simulations. Biophys. J. 107, 1393–1402 (2014).
    Article CAS Google Scholar
  39. Mincer, J. S. & Simon, S. M. Simulations of nuclear pore transport yield mechanistic insights and quantitative predictions. Proc. Natl Acad. Sci. USA 108, E351–E358 (2011).
    Article CAS Google Scholar
  40. Gamini, R., Han, W., Stone, J. E. & Schulten, K. Assembly of Nsp1 nucleoporins provides insight into nuclear pore complex gating. PLoS Comp. Biol. 10, e1003488 (2014).
    Article Google Scholar
  41. Peyro, M., Soheilypour, M., Ghavami, A. & Mofrad, M. R. K. Nucleoporin's like charge regions are major regulators of FG coverage and dynamics inside the nuclear pore complex. PLoS ONE 10, e0143745 (2015).
    Article Google Scholar
  42. Ando, T. High-speed atomic force microscopy. Microscopy 62, 81–93 (2013).
    Article CAS Google Scholar
  43. Schmidt, H. B. & Görlich, D. Transport selectivity of nuclear pores, phase separation, and membraneless organelles. Trends Biochem. Sci. 41, 46–61 (2016).
    Article CAS Google Scholar
  44. Hough, L. E. et al. The molecular mechanism of nuclear transport revealed by atomic-scale measurements. eLife 4, e10027 (2015).
    Article Google Scholar
  45. Milles, S. et al. Plasticity of an ultrafast interaction between nucleoporins and nuclear transport receptors. Cell 163, 734–745 (2015).
    Article CAS Google Scholar
  46. Hoh, J. H. Functional protein domains from the thermally driven motion of polypeptide chains A proposal. Proteins 32, 223–228 (1998).
    Article CAS Google Scholar
  47. Fuxreiter, M. et al. Disordered proteinaceous machines. Chem. Rev. 114, 6806–6843 (2014).
    Article CAS Google Scholar

Download references