Single molecule studies of nucleocytoplasmic transport

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1813, Issue 9, 2011, Pages 1607-1618

  Tu, Li Chun ^a   Musser, Siegfried M ^a  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

Nuclear pore complex; Nuclear transport; Single molecule fluorescence

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; EXPORTIN 1; GLYCINE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; KARYOPHERIN; KARYOPHERIN BETA; NUCLEOPLASMIN; NUCLEOPORIN; PHENYLALANINE;

CYTOPLASM; EPIFLUORESCENCE MICROSCOPY; FLUORESCENCE ANALYSIS; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; MEMBRANE PERMEABILITY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR PORE COMPLEX; NUCLEOCYTOPLASMIC TRANSPORT; PARTITION COEFFICIENT; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; SUMOYLATION; TETRATRICOPEPTIDE REPEAT; THERMODYNAMICS;

ACTIVE TRANSPORT, CELL NUCLEUS; HUMANS; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; PERMEABILITY; SIGNAL TRANSDUCTION;

EUKARYOTA;

EID: 79960927256     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2010.12.011     Document Type: Review

References (111)

1. Ribbeck K., Görlich D. Kinetic analysis of translocation through nuclear pore complexes. EMBO J. 2001, 20:1320-1330.
2. Rout M.P., Blobel G. Isolation of the yeast nuclear pore complex. J. Cell Biol. 1993, 123:771-783.
3. Reichelt R., Holzenburg A., Buhle J.E.L., Jarnik M., Engel A., Aebi U. Correlation between structure and mass distribution of the nuclear pore complex and of distinct pore complex components. J. Cell Biol. 1990, 110:883-894.
4. Stoffler D., Feja B., Fahrenkrog B., Walz J., Typke D., Aebi U. Cryo-electron tomography provides novel insights into nuclear pore architecture: implications for nucleocytoplasmic transport. J. Mol. Biol. 2003, 328:119-130.
5. Pante N., Kann M. Nuclear pore complex is able to transport macromolecules with diameters of about 39nm. Mol. Biol. Cell 2002, 13:425-434.
6. Naim B., Zbaida D., Dagan S., Kapon R., Reich Z. Cargo surface hydrophobicity is sufficient to overcome the nuclear pore complex selectivity barrier. EMBO J. 2009, 28:2697-2705.
7. Colwell L.J., Brenner M.P., Ribbeck K. Charge as a selection criterion for translocation through the nuclear pore complex. PLoS Comput. Biol. 2010, 6:e1000747.
8. Terry L.J., Wente S.R. Flexible gates: dynamic typologies and functions for FG nucleoporins in nucleocytoplasmic transport. Euk. Cell 2009, 8:1814-1827.
9. Brohawn S.G., Partridge J.R., Whittle J.R.R., Schwartz T.U. The nuclear pore complex has entered the atomic age. Structure 2009, 17:1156-1168.
10. Lim R.Y.H., Aebi U., Fahrenkrog B. Towards reconciling structure and function in the nuclear pore complex. Histochem. Cell Biol. 2008, 129:105-116.
11. Stewart M. Molecular mechanism of the nuclear protein import cycle. Nat. Rev. Mol. Cell Biol. 2007, 8:195-208.
12. Cronshaw J.M., Krutchinsky A.N., Zhang W., Chait B.T., Matunis M.J. Proteomic analysis of the mammalian nuclear pore complex. J. Cell Biol. 2002, 158:915-927.
13. Rout M.P., Aitchison J.D., Suprapto A., Hjertaas K., Zhao Y., Chait B.T. The yeast nuclear pore complex: composition, architecture, and transport mechanism. J. Cell Biol. 2000, 148:635-651.
14. Patel S.S., Belmont B.J., Sante J.M., Rexach M.F. Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex. Cell 2007, 129:83-96.
15. Denning D.P., Rexach M.F. Rapid evolution exposes the boundaries of domain structure and function in natively unfolded FG nucleoporins. Mol. Cell. Proteomics 2007, 6:272-282.
16. Krishnan V.V., Lau E.Y., Yamada J., Denning D.P., Patel S.S., Colvin M.E., Rexach M.F. Intramolecular cohesion of coils mediated by phenylalanine-glycine motifs in the natively unfolded domain of a nucleoporin. PLoS Comput. Biol. 2008, 4:e1000145.
17. Frey S., Görlich D. A saturated FG-repeat hydrogel can reproduce the permeability properties of nuclear pore complexes. Cell 2007, 130:512-523.
18. Lim R.Y., Huang N.P., Koser J., Deng J., Lau K.H., Schwarz-Herion K., Fahrenkrog B., Aebi U. Flexible phenylalanine-glycine nucleoporins as entropic barriers to nucleocytoplasmic transport. Proc. Natl Acad. Sci. USA 2006, 103:9512-9517.
19. Macara I.G. Transport into and out of the nucleus. Microbiol. Mol. Biol. Rev. 2001, 65:570-594.
20. Yang W., Gelles J., Musser S.M. Imaging of single-molecule translocation through nuclear pore complexes. Proc. Natl Acad. Sci. USA 2004, 101:12887-12892.
21. Yang W., Musser S.M. Nuclear import time and transport efficiency depend on importin beta concentration. J. Cell Biol. 2006, 174:951-961.
22. Fried H., Kutay U. Nucleocytoplasmic transport: taking an inventory. Cell. Mol. Life Sci. 2003, 60:1659-1688.
23. Görlich D., Kutay U. Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell Dev. Biol. 1999, 15:607-660.
24. Lim R.Y., Ullman K.S., Fahrenkrog B. Biology and biophysics of the nuclear pore complex and its components. Int. Rev. Cell Mol. Biol. 2008, 267:299-342.
25. Peters R. Functionalization of a nanopore: the nuclear pore complex paradigm. Biochim. Biophys. Acta 2009, 1793:1533-1539.
26. Tran E.J., Wente S.R. Dynamic nuclear pore complexes: life on the edge. Cell 2006, 125:1041-1053.
27. Frey S., Görlich D. FG/FxFG as well as GLFG repeats form a selective permeability barrier with self-healing properties. EMBO J. 2009, 28:2554-2567.
28. Naim B., Brumfeld V., Kapon R., Kiss V., Nevo R., Reich Z. Passive and facilitated transport in nuclear pore complexes is largely uncoupled. J. Biol. Chem. 2007, 282:3881-3888.
29. McLane L.M., Corbett A.H. Nuclear localization signals and human disease. IUBMB Life 2009, 61:697-706.
30. Mason D.A., Stage D.E., Goldfarb D.S. Evolution of the metazoan-specific importin alpha gene family. J. Mol. Evol. 2009, 68:351-365.
31. Tejomurtula J., Lee K.B., Tripurani S.K., Smith G.W., Yao J. Role of importin alpha8, a new member of the importin alpha family of nuclear transport proteins, in early embryonic development in cattle. Biol. Reprod. 2009, 81:333-342.
32. Askjaer P., Jensen T.H., Nilsson J., Englmeier L., Kjems J. The specificity of the CRM1-Rev nuclear export signal interaction is mediated by RanGTP. J. Biol. Chem. 1998, 273:33414-33422.
33. Paraskeva E., Izaurralde E., Bischoff F.R., Huber J., Kutay U., Hartmann E., Luhrmann R., Görlich D. CRM1-mediated recycling of snurportin 1 to the cytoplasm. J. Cell Biol. 1999, 145:255-264.
34. Yaseen N.R., Blobel G. GTP hydrolysis links initiation and termination of nuclear import on the nucleoporin Nup358. J. Biol. Chem. 1999, 274:26493-26502.
35. Floer M., Blobel G. Putative reaction intermediates in Crm1-mediated nuclear protein export. J. Biol. Chem. 1999, 274:16279-16286.
36. Floer M., Blobel G., Rexach M. Disassembly of RanGTP-karyopherin β complex, an intermediate in nuclear protein import. J. Biol. Chem. 1997, 272:19538-19546.
37. Bischoff F.R., Görlich D. RanBP1 is crucial for the release of RanGTP from importin β-related nuclear transport factors. FEBS Lett. 1997, 419:249-254.
38. Ribbeck K., Lipowsky G., Kent H.M., Stewart M., Görlich D. NTF2 mediates nuclear import of Ran. EMBO J. 1998, 17:6587-6598.
39. Matsuura Y., Stewart M. Nup50/Npap60 function in nuclear protein import complex disassembly and importin recycling. EMBO J. 2005, 24:3681-3689.
40. 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 2008, 105:8613-8618.
41. Gilchrist D., Mykytka B., Rexach M. Accelerating the rate of disassembly of karyopherin cargo complexes. J. Biol. Chem. 2002, 277:18161-18172.
42. Gilchrist D., Rexach M. Molecular basis for the rapid dissociation of nuclear localization signals from karyopherin α in the nucleoplasm. J. Biol. Chem. 2003, 278:51937-51949.
43. Hutten S., Flotho A., Melchior F., Kehlenbach R.H. The Nup358-RanGAP complex is required for efficient importin alpha/beta-dependent nuclear import. Mol. Biol. Cell 2008, 19:2300-2310.
44. Hutten S., Walde S., Spillner C., Hauber J., Kehlenbach R.H. The nuclear pore component Nup358 promotes transportin-dependent nuclear import. J. Cell Sci. 2009, 122:1100-1110.
45. Görlich D., Seewald M.J., Ribbeck K. Characterization of Ran-driven cargo transport and the RanGTPase system by kinetic measurements and computer simulation. EMBO J. 2003, 22:1088-1100.
46. Nachury M.V., Weis K. The direction of transport through the nuclear pore can be inverted. Proc. Natl Acad. Sci. USA 1999, 96:9622-9627.
47. Grünwald D., Hoekstra A., Dange T., Buschmann V., Kubitscheck U. Direct observation of single protein molecules in aqueous solution. Chemphyschem 2006, 7:812-815.
48. 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. 2008, 183:77-86.
49. Kubitscheck U., Grünwald D., Hoekstra A., Rohleder D., Kues T., Siebrasse J.P., Peters R. Nuclear transport of single molecules: dwell times at the nuclear pore complex. J. Cell Biol. 2005, 168:233-243.
50. Yang W., Musser S.M. Visualizing single molecules interacting with nuclear pore complexes by narrow-field epifluorescence microscopy. Methods 2006, 39:316-328.
51. Daigle N., Beaudouin J., Hartnell L., Imreh G., Hallberg E., Lippincott-Schwartz J., Ellenberg J. Nuclear pore complexes form immobile networks and have a very low turnover in live mammalian cells. J. Cell Biol. 2001, 154:71-84.
52. Lang E., Baier J., Kohler J. Epifluorescence, confocal and total internal reflection microscopy for single-molecule experiments: a quantitative comparison. J. Microsc. 2006, 222:118-123.
53. Schmidt T., Schutz G.J., Baumgartner W., Gruber H.J., Schindler H. Imaging of single molecule diffusion. Proc. Natl Acad. Sci. USA 1996, 93:2926-2929.
54. Peter J., Kubitscheck U. Single molecule tracking for studying nucleocytoplasmic transport and intranuclear dynamics. The Nucleus 2008, vol. 2:343-361. Humana, Totowa, N.J.
55. Tokunaga M., Imamoto N., Sakata-Sogawa K. Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat. Meth. 2008, 5:159-161.
56. 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 2010, 107:7305-7310.
57. Day R.N., Davidson M.W. The fluorescent protein palette: tools for cellular imaging. Chem. Soc. Rev. 2009, 38:2887-2921.
58. Leslie D.M., Timney B., Rout M.P., Aitchison J.D. Studying nuclear protein import in yeast. Methods 2006, 39:291-308.
59. Bucci M., Wente S.R. In vivo dynamics of nuclear pore complexes in yeast. J. Cell Biol. 1997, 136:1185-1199.
60. Adam S.A., Marr R.S., Gerace L. Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J. Cell Biol. 1990, 111:807-816.
61. Görlich D., Prehn S., Laskey R.A., Hartmann E. Isolation of a protein that is essential for the first step of nuclear protein import. Cell 1994, 79:767-778.
62. Adam E.J.H., Adam S.A. Identification of cytosolic factors required for nuclear location sequence-mediated binding to the nuclear envelope. J. Cell Biol. 1994, 125:547-555.
63. Melchior F., Paschal B.M., Evans J., Gerace L. Inhibition of nuclear protein import by nonhydrolyzable analogues of GTP and identification of the small GTPase Ran/TC4 as an essential transport factor. J. Cell Biol. 1993, 123:1649-1659.
64. Moore M.S., Blobel G. The GTP-binding protein Tan/TC4 is required for protein import into the nucleus. Nature 1993, 365:661-663.
65. Kehlenbach R.H. In vitro analysis of nuclear mRNA export using molecular beacons for target detection. Nucleic Acids Res. 2003, 31:e64.
66. Grünwald D., Singer R.H. In vivo imaging of labelled endogeneous β-actin mRNA during nucleocytoplasmic transport. Nature 2010, 467:604-607.
67. Huang B., Bates M., Zhuang X. Super-resolution fluorescence microscopy. Annu. Rev. Biochem. 2009, 78:993-1016.
68. Yildiz A., Forkey J.N., McKinney S.A., Ha T., Goldman Y.E., Selvin P.R. Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization. Science 2003, 300:2061-2065.
69. Kahms M., Lehrich P., Huve J., Sanetra N., Peters R. Binding site distribution of nuclear transport receptors and transport complexes in single nuclear pore complexes. Traffic 2009, 10:1228-1242.
70. Lowe A.R., Siegel J.J., Kalab P., Siu M., Weis K., Liphardt J.T. Selectivity mechanism of the nuclear pore complex characterized by single cargo tracking. Nature 2010, 467:600-603.
71. Joo C., Balci H., Ishitsuka Y., Buranachai C., Ha T. Advances in single-molecule fluorescence methods for molecular biology. Annu. Rev. Biochem. 2008, 77:51-76.
72. Carmody S.R., Wente S.R. mRNA nuclear export at a glance. J. Cell Sci. 2009, 122:1933-1937.
73. Zilman A., Pearson J., Bel G. Effects of jamming on nonequilibrium transport times in nanochannels. Phys. Rev. Lett. 2009, 103:128103.
74. Görlich D., Pante N., Kutay U., Aebi U., Bischoff F.R. Identification of different roles for RanGDP and RanGTP in nuclear protein import. EMBO J. 1996, 15:5584-5594.
75. Zilman A. Effects of multiple occupancy and interparticle interactions on selective transport through narrow channels: theory versus experiment. Biophys. J. 2009, 96:1235-1248.
76. Zilman A., Di Talia S., Chait B.T., Rout M.P., Magnasco M.O. Efficiency, selectivity, and robustness of nucleocytoplasmic transport. PLoS Comput. Biol. 2007, 3:e125.
77. Zilman A., Di Talia S., Jovanovic-Talisman T., Chait B.T., Rout M.P., Magnasco M.O. Enhancement of transport selectivity through nano-channels by non-specific competition. PLoS Comp. Biol. 2010, 6:e1000804.
78. Rexach M., Blobel G. Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell 1995, 83:683-692.
79. Kutay U., Bischoff F.R., Kostka S., Kraft R., Görlich D. Export of importin α from the nucleus is mediated by a specific nuclear transport factor. Cell 1997, 90:1061-1071.
80. Jovanovic-Talisman T., Tetenbaum-Novatt J., McKenney A.S., Zilman A., Peters R., Rout M.P., Chait B.T. Artificial nanopores that mimic the transport selectivity of the nuclear pore complex. Nature 2009, 457:1023-1027.
81. Mohr D., Frey S., Fischer T., Guttler T., Görlich D. Characterisation of the passive permeability barrier of nuclear pore complexes. EMBO J. 2009, 28:2541-2553.
82. Zemp I., Kutay U. Nuclear export and cytoplasmic maturation of ribosomal subunits. FEBS Lett. 2007, 581:2783-2793.
83. Smith A.E., Helenius A. How viruses enter animal cells. Science 2004, 304:237-242.
84. Kapon R., Topchik A., Mukamel D., Reich Z. A possible mechanism for self-coordination of bidirectional traffic across nuclear pores. Phys. Biol. 2008, 5:036001.
85. Yamada J., Phillips J.L., Patel S., Goldfien G., Calestagne-Morelli A., Huang H., Rexza R., Acheson J., Krishnan V.V., Newsam S., Gopinathan A., Lau E.Y., Colvin M.E., Uversky V.N., Rexach M.F. A bimodal distribution of two distinct categories of intrinsically-disordered structures with separate functions in FG nucleoporins. Mol. Cell. Proteomics 2010, 9:2205-2224.
86. 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 2003, 100:2450-2455.
87. de Gennes P.-G. Scaling Concepts in Polymer Physics 1979, Cornell University Press, Ithaca, N.Y.
88. de Gennes P.-G. Polymers at an interface; a simplified view. Adv. Colloid Int. Sci. 1987, 27:189-209.
89. Frey S., Richter R.P., Görlich D. FG-rich repeats of nuclear pore proteins form a three-dimensional meshwork with hydrogel-like properties. Science 2006, 314:815-817.
90. Ader C., Frey S., Maas W., Schmidt H.B., Görlich D., Baldus M. Amyloid-like interactions within nucleoporin FG hydrogels. Proc. Natl Acad. Sci. USA 2010, 107:6281-6285.
91. Strawn L.A., Shen T., Shulga N., Goldfarb D.S., Wente S.R. Minimal nuclear pore complexes define FG repeat domains essential for transport. Nat. Cell Biol. 2004, 6:197-206.
92. Abu-Arish A., Kalab P., Ng-Kamstra J., Weis K., Fradin C. Spatial distribution and mobility of the Ran GTPase in live interphase cells. Biophys. J. 2009, 97:2164-2178.
93. Rhee M., Burns M.A. Nanopore sequencing technology: nanopore preparations. Trends Biotechnol. 2007, 25:174-181.
94. Lim R.Y., Fahrenkrog B., Koser J., Schwarz-Herion K., Deng J., Aebi U. Nanomechanical basis of selective gating by the nuclear pore complex. Science 2007, 318:640-643.
95. Bayliss R., Littlewood T., Stewart M. Structural basis for the interaction between FxFG nucleoporin repeats and importin-beta in nuclear trafficking. Cell 2000, 102:99-108.
96. 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. 2002, 277:50597-50606.
97. Bednenko J., Cingolani G., Gerace L. Importin beta contains a COOH-terminal nucleoporin binding region important for nuclear transport. J. Cell Biol. 2003, 162:391-401.
98. Isgro T.A., Schulten K. Binding dynamics of isolated nucleoporin repeat regions to importin-beta. Structure 2005, 13:1869-1879.
99. Liu S.M., Stewart M. Structural basis for the high-affinity binding of nucleoporin Nup1p to the Saccharomyces cerevisiae importin-beta homologue, Kap95p. J. Mol. Biol. 2005, 349:515-525.
100. Luby-Phelps K. Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area. Int. Rev. Cytol. 2000, 192:189-221.
101. Fiserova J., Richards S.A., Wente S.R., Goldberg M.W. Facilited transport and diffusion take distinct spatial routes through the nuclear pore complex. J. Cell Sci. 2010, 123:2773-2780.
102. Holtzer L., Meckel T., Schmidt T. Nanometric three-dimensional tracking of individual quantum dots in cells. Appl. Phys. Lett. 2007, 90:053902.
103. Prabhat P., Ram S., Ward E.S., Ober R.J. Simultaneous imaging of different focal planes in fluorescence microscopy for the study of cellular dynamics in three dimensions. IEEE Trans. Nanobioscience 2004, 3:237-242.
104. Toprak E., Balci H., Blehm B.H., Selvin P.R. Three-dimensional particle tracking via bifocal imaging. Nano Lett. 2007, 7:2043-2045.
105. Wells N.P., Lessard G.A., Werner J.H. Confocal, three-dimensional tracking of individual quantum dots in high-background environments. Anal. Chem. 2008, 80:9830-9834.
106. Pertsinidis A., Zhang Y., Chu S. Subnanometre single-molecule localization, registration and distance measurements. Nature 2010, 466:647-651.
107. Chaillan-Huntington C., Butler P.J.G., Huntington J.A., Akin D., Feldherr C., Stewart M. NTF2 monomer-dimer equilibrium. J. Mol. Biol. 2001, 314:465-477.
108. Akey C.W., Radermacher M. Architecture of the Xenopus nuclear pore complex revealed by three-dimensional cryo-electron microscopy. J. Cell Biol. 1993, 122:1-19.
109. Jarnik M., Aebi U. Toward a more complete 3-D structure of the nuclear pore complex. J. Struct. Biol. 1991, 107:291-308.
110. Hinshaw J.E., Carragher B.O., Milligan R.A. Architecture and design of the nuclear pore complex. Cell 1992, 69:1133-1141.
111. Frenkiel-Krispin D., Maco B., Aebi U., Medalia O. Structural analysis of a metazoan nuclear pore complex reveals a fused concentric ring architecture. J. Mol. Biol. 2010, 395:578-586.