Super-resolution 3D tomography of interactions and competition in the nuclear pore complex (original) (raw)

References

1. Rout, M.P. et al. The yeast nuclear pore complex: composition, architecture, and transport mechanism. J. Cell Biol. 148, 635–651 (2000).
   Article CAS PubMed PubMed Central Google Scholar
2. Suntharalingam, M. & Wente, S.R. Peering through the pore: nuclear pore complex structure, assembly, and function. Dev. Cell 4, 775–789 (2003).
   Article CAS PubMed Google Scholar
3. Fried, H. & Kutay, U. Nucleocytoplasmic transport: taking an inventory. Cell. Mol. Life Sci. 60, 1659–1688 (2003).
   Article CAS PubMed Google Scholar
4. Fahrenkrog, B. & Aebi, U. The nuclear pore complex: nucleocytoplasmic transport and beyond. Nat. Rev. Mol. Cell Biol. 4, 757–766 (2003).
   Article CAS PubMed Google Scholar
5. Denning, D.-P., Patel, S.S., Uversky, V., Fink, A.L. & Rexach, M. Disorder in the nuclear pore complex: the FG repeat regions of nucleoporins are natively unfolded. Proc. Natl. Acad. Sci. USA 100, 2450–2455 (2003).
   Article CAS PubMed PubMed Central Google Scholar
6. Stewart, M. Molecular mechanism of the nuclear protein import cycle. Nat. Rev. Mol. Cell Biol. 8, 195–208 (2007).
   Article CAS PubMed Google Scholar
7. Palmeri, D. & Malim, M.H. Importin beta can mediate the nuclear import of an arginine-rich nuclear localization signal in the absence of importin alpha. Mol. Cell. Biol. 19, 1218–1225 (1999).
   Article CAS PubMed PubMed Central Google Scholar
8. Hoelz, A., Debler, E.W. & Blobel, G. The structure of the nuclear pore complex. Annu. Rev. Biochem. 80, 613–643 (2011).
   Article CAS PubMed Google Scholar
9. Rout, M.P. & Blobel, G. Isolation of the yeast nuclear pore complex. J. Cell Biol. 123, 771–783 (1993).
   Article CAS PubMed Google Scholar
10. Terry, L.J. & Wente, S.R. Flexible gates: dynamic topologies and functions for FG nucleoporins in nucleocytoplasmic transport. Eukaryot. Cell 8, 1814–1827 (2009).
    Article CAS PubMed PubMed Central Google Scholar
11. Macara, I.G. Transport into and out of the nucleus. Microbiol. Mol. Biol. Rev. 65, 570–594 (2001).
    Article CAS PubMed PubMed Central Google Scholar
12. Rout, M.P. & Aitchison, J.D. The nuclear pore complex as a transport machine. J. Biol. Chem. 276, 16593–16596 (2001).
    Article CAS PubMed Google Scholar
13. Peters, R. Translocation through the nuclear pore complex: selectivity and speed by reduction-of-dimensionality. Traffic 6, 421–427 (2005).
    Article CAS PubMed Google Scholar
14. Lim, R.Y. et al. Nanomechanical basis of selective gating by the nuclear pore complex. Science 318, 640–643 (2007).
    Article CAS PubMed Google Scholar
15. 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 PubMed Google Scholar
16. Ribbeck, K. & Görlich, D. Kinetic analysis of translocation through nuclear pore complexes. EMBO J. 20, 1320–1330 (2001).
    Article CAS PubMed PubMed Central Google Scholar
17. 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 PubMed Google Scholar
18. Mohr, D., Frey, S., Fischer, T., Güttler, T. & Görlich, D. Characterisation of the passive permeability barrier of nuclear pore complexes. EMBO J. 28, 2541–2553 (2009).
    Article CAS PubMed PubMed Central Google Scholar
19. Frey, S., Richter, R.P. & Görlich, D. FG-rich repeats of nuclear pore proteins form a three-dimensional meshwork with hydrogel-like properties. Science 314, 815–817 (2006).
    Article CAS PubMed Google Scholar
20. la Cour, T. et al. Analysis and prediction of leucine-rich nuclear export signals. Protein Eng. Des. Sel. 17, 527–536 (2004).
    Article CAS PubMed Google Scholar
21. 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 PubMed PubMed Central Google Scholar
22. Ma, J. & Yang, W. Three-dimensional distribution of transient interactions in the nuclear pore complex obtained from single-molecule snapshots. Proc. Natl. Acad. Sci. USA 107, 7305–7310 (2010).
    Article CAS PubMed PubMed Central Google Scholar
23. 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 PubMed PubMed Central Google Scholar
24. Ma, J. et al. High-resolution three-dimensional mapping of mRNA export through the nuclear pore. Nat. Commun. 4, 2414 (2013).
    Article PubMed CAS Google Scholar
25. Kutay, U., Izaurralde, E., Bischoff, F.R., Mattaj, I.W. & Görlich, D. Dominant-negative mutants of importin-beta block multiple pathways of import and export through the nuclear pore complex. EMBO J. 16, 1153–1163 (1997).
    Article CAS PubMed PubMed Central Google Scholar
26. Bayliss, R., Littlewood, T., Strawn, L.A., Wente, S.R. & Stewart, M. GLFG and FxFG nucleoporins bind to overlapping sites on importin-beta. J. Biol. Chem. 277, 50597–50606 (2002).
    Article CAS PubMed Google Scholar
27. Patel, S.S., Belmont, B.J., Sante, J.M. & Rexach, M.F. Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex. Cell 129, 83–96 (2007).
    Article CAS PubMed Google Scholar
28. Peters, R. Translocation through the nuclear pore: Kaps pave the way. BioEssays 31, 466–477 (2009).
    Article CAS PubMed Google Scholar
29. Ben-Efraim, I. & Gerace, L. Gradient of increasing affinity of importin beta for nucleoporins along the pathway of nuclear import. J. Cell Biol. 152, 411–417 (2001).
    Article CAS PubMed PubMed Central Google Scholar
30. Isgro, T.A. & Schulten, K. Association of nuclear pore FG-repeat domains to NTF2 import and export complexes. J. Mol. Biol. 366, 330–345 (2007).
    Article CAS PubMed Google Scholar
31. Iwamoto, M., Asakawa, H., Hiraoka, Y. & Haraguchi, T. Nucleoporin Nup98: a gatekeeper in the eukaryotic kingdoms. Genes Cells 15, 661–669 (2010).
    Article CAS PubMed Google Scholar
32. Katahira, J., Straesser, K., Saiwaki, T., Yoneda, Y. & Hurt, E. Complex formation between Tap and p15 affects binding to FG-repeat nucleoporins and nucleocytoplasmic shuttling. J. Biol. Chem. 277, 9242–9246 (2002).
    Article CAS PubMed Google Scholar
33. 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 PubMed PubMed Central Google Scholar
34. 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 PubMed PubMed Central Google Scholar
35. Wagner, R.S., Kapinos, L.E., Marshall, N.J., Stewart, M. & Lim, R.Y. Promiscuous binding of Karyopherinβ1 modulates FG nucleoporin barrier function and expedites NTF2 transport kinetics. Biophys. J. 108, 918–927 (2015).
    Article CAS PubMed PubMed Central Google Scholar
36. Tetenbaum-Novatt, J., Hough, L.E., Mironska, R., McKenney, A.S. & Rout, M.P. Nucleocytoplasmic transport: a role for nonspecific competition in karyopherin-nucleoporin interactions. Mol. Cell. Proteomics 11, 31–46 (2012).
    Article CAS PubMed PubMed Central Google Scholar
37. Kerr, A.R. & Schirmer, E.C. FG repeats facilitate integral protein trafficking to the inner nuclear membrane. Commun. Integr. Biol. 4, 557–559 (2011).
    Article CAS PubMed PubMed Central Google Scholar
38. Yang, W., Gelles, J. & Musser, S.M. Imaging of single-molecule translocation through nuclear pore complexes. Proc. Natl. Acad. Sci. USA 101, 12887–12892 (2004).
    Article CAS PubMed PubMed Central Google Scholar
39. Yang, W. & Musser, S.M. Nuclear import time and transport efficiency depend on importin beta concentration. J. Cell Biol. 174, 951–961 (2006).
    Article CAS PubMed PubMed Central Google Scholar
40. Yang, W. & Musser, S.M. Visualizing single molecules interacting with nuclear pore complexes by narrow-field epifluorescence microscopy. Methods 39, 316–328 (2006).
    Article CAS PubMed PubMed Central Google Scholar
41. Sun, C., Yang, W., Tu, L.C. & Musser, S.M. Single-molecule measurements of importin alpha/cargo complex dissociation at the nuclear pore. Proc. Natl. Acad. Sci. USA 105, 8613–8618 (2008).
    Article CAS PubMed PubMed Central Google Scholar
42. Mortensen, K.I., Churchman, L.S., Spudich, J.A. & Flyvbjerg, H. Optimized localization analysis for single-molecule tracking and super-resolution microscopy. Nat. Methods 7, 377–381 (2010).
    Article CAS PubMed PubMed Central Google Scholar
43. Quan, T., Zeng, S. & Huang, Z.L. Localization capability and limitation of electron-multiplying charge-coupled, scientific complementary metal-oxide semiconductor, and charge-coupled devices for superresolution imaging. J. Biomed. Opt. 15, 066005 (2010).
    Article PubMed Google Scholar
44. Robbins, M.S. & Hadwen, B.J. The noise performance of electron multiplying charge-coupled devices. IEEE Trans. Electron. Dev. 50, 1227–1232 (2003).
    Article Google Scholar
45. Deschout, H., Neyts, K. & Braeckmans, K. The influence of movement on the localization precision of sub-resolution particles in fluorescence microscopy. J. Biophotonics 5, 97–109 (2012).
    Article CAS PubMed Google Scholar

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