A physical model describing the interaction of nuclear transport receptors with FG nucleoporin domain assemblies

eLife

Volumn 5, Issue APRIL2016, 2016, Pages

  Zahn, Raphael ^a   Osmanović, Dino ^b,c   Ehret, Severin ^a   Callis, Carolina Araya ^a   Frey, Steffen ^d,i   Stewart, Murray ^e   You, Changjiang ^f   Görlich, Dirk ^d   Hoogenboom, Bart W ^b   Richter, Ralf P ^a,g,h  

^a CIC BIOMAGUNE   (Spain)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c BAR ILAN UNIVERSITY   (Israel)

^d MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^e MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^f UNIVERSITY OF OSNABRÜCK   (Germany)

^g UNIV GRENOBLE ALPES   (France)

^h MAX PLANCK INSTITUTE FOR INTELLIGENT SYSTEMS   (Germany)

ⁱ NanoTag Biotechnologies GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOPORIN; NUCLEOCYTOPLASMIC TRANSPORT PROTEIN; PROTEIN BINDING;

ARTICLE; ELLIPSOMETRY; FILM; MATHEMATICAL PARAMETERS; MONTE CARLO METHOD; NUCLEOCYTOPLASMIC TRANSPORT; PERMEABILITY BARRIER; PHYSICAL MODEL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; QUARTZ CRYSTAL MICROBALANCE; BIOLOGICAL MODEL; METABOLISM;

ACTIVE TRANSPORT, CELL NUCLEUS; MODELS, BIOLOGICAL; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; PROTEIN BINDING;

EID: 84971577933     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.14119     Document Type: Article

References (88)

1. Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, Devos D, Suprapto A, Karni-Schmidt O, Williams R, Chait BT, Sali A, Rout MP. 2007. The molecular architecture of the nuclear pore complex. Nature 450:695–701. doi: 10.1038/nature06405
2. Ando D, Colvin M, Rexach M, Gopinathan A. 2013. Physical motif clustering within intrinsically disordered nucleoporin sequences reveals universal functional features. PLoS ONE 8:e73831: doi: 10.1371/journal.pone.0073831
3. Ando D, Zandi R, Kim YW, Colvin M, Rexach M, Gopinathan A. 2014. Nuclear pore complex protein sequences determine overall copolymer brush structure and function. Biophysical Journal 106:1997–2007. doi: 10.1016/j.bpj.2014.03.021
4. Bayliss R, Ribbeck K, Akin D, Kent HM, Feldherr CM, Görlich D, Stewart M. 1999. Interaction between NTF2 and xfxfg-containing nucleoporins is required to mediate nuclear import of rangdp. Journal of Molecular Biology 293:579–593. doi: 10.1006/jmbi.1999.3166
5. Bayliss R, Littlewood T, Stewart M. 2000. Structural basis for the interaction between fxfg nucleoporin repeats and importin-beta in nuclear trafficking. Cell 102:99–108. doi: 10.1016/s0092-8674(00)00014-3
6. Bayliss R, Leung SW, Baker RP, Quimby BB, Corbett AH, Stewart M. 2002. Structural basis for the interaction between NTF2 and nucleoporin fxfg repeats. The EMBO Journal 21:2843–2853. doi: 10.1093/emboj/cdf305
7. Bestembayeva A, Kramer A, Labokha AA, Osmanović D, Liashkovich I, Orlova EV, Ford IJ, Charras G, Fassati A, Hoogenboom BW. 2015. Nanoscale stiffness topography reveals structure and mechanics of the transport barrier in intact nuclear pore complexes. Nature Nanotechnology 10:60–64. doi: 10.1038/nnano.2014.262
8. Beutel O, Nikolaus J, Birkholz O, You C, Schmidt T, Herrmann A, Piehler J. 2014. High-fidelity protein targeting into membrane lipid microdomains in living cells. Angewandte Chemie (International Ed. in English) 53:1311–1315. doi: 10.1002/anie.201306328
9. Bui KH, von Appen A, DiGuilio AL, Ori A, Sparks L, Mackmull MT, Bock T, Hagen W, Andrés-Pons A, Glavy JS, Beck M. 2013. Integrated structural analysis of the human nuclear pore complex scaffold. Cell 155:1233–1243. doi: 10.1016/j.cell.2013.10.055
10. Carton I, Brisson AR, Richter RP. 2010. Label-free detection of clustering of membrane-bound proteins. Analytical Chemistry 82:9275–9281. doi: 10.1021/ac102495q
11. Clarkson WD, Corbett AH, Paschal BM, Kent HM, McCoy AJ, Gerace L, Silver PA, Stewart M. 1997. Nuclear protein import is decreased by engineered mutants of nuclear transport factor 2 (NTF2) that do not bind gdp-ran. Journal of Molecular Biology 272:716–730. doi: 10.1006/jmbi.1997.1255
12. De Feijter JA, Benjamins J, Veer FA. 1978. Ellipsometry as a tool to study the adsorption behavior of synthetic and biopolymers at the air-water interface. Biopolymers 17:1759–1772. doi: 10.1002/bip.1978.360170711
13. Denning DP, Uversky V, Patel SS, Fink AL, Rexach M. 2002. The saccharomyces cerevisiae nucleoporin nup2p is a natively unfolded protein. The Journal of Biological Chemistry 277:33447–33455. doi: 10.1074/jbc.M203499200
14. Denning DP, Patel SS, Uversky V, Fink AL, Rexach M. 2003. Disorder in the nuclear pore complex: The FG repeat regions of nucleoporins are natively unfolded. Proceedings of the National Academy of Sciences of the United States of America 100:2450–2455. doi: 10.1073/pnas.0437902100
15. Denning DP, Rexach MF. 2007. Rapid evolution exposes the boundaries of domain structure and function in natively unfolded FG nucleoporins. Molecular & Cellular Proteomics 6:272–282. doi: 10.1074/mcp.M600309-MCP200
16. Domack A, Prucker O, Rühe J, Johannsmann D. 1997. Swelling of a polymer brush probed with a quartz crystal resonator. Physical Review E 56:680–689. doi: 10.1103/PhysRevE.56.680
17. Dyson HJ, Wright PE. 2005. Intrinsically unstructured proteins and their functions. Nature Reviews. Molecular Cell Biology 6:197–208. doi: 10.1038/nrm1589
18. Eibauer M, Pellanda M, Turgay Y, Dubrovsky A, Wild A, Medalia O. 2015. Structure and gating of the nuclear pore complex. Nature Communications 6:7532. doi: 10.1038/ncomms8532
19. Eisele NB, Frey S, Piehler J, Görlich D, Richter RP. 2010. Ultrathin nucleoporin phenylalanine-glycine repeat films and their interaction with nuclear transport receptors. EMBO Reports 11:366–372. doi: 10.1038/embor.2010.34
20. Eisele NB, Andersson FI, Frey S, Richter RP. 2012. Viscoelasticity of thin biomolecular films: A case study on nucleoporin phenylalanine-glycine repeats grafted to a histidine-tag capturing QCM-D sensor. Biomacromolecules 13:2322–2332. doi: 10.1021/bm300577s
21. Eisele NB, Labokha AA, Frey S, Görlich D, Richter RP. 2013. Cohesiveness tunes assembly and morphology of FG nucleoporin domain meshworks - implications for nuclear pore permeability. Biophysical Journal 105:1860–1870. doi: 10.1016/j.bpj.2013.09.006
22. Fahrenkrog B, Aebi U. 2003. The nuclear pore complex: Nucleocytoplasmic transport and beyond. Nature Reviews. Molecular Cell Biology 4:757–766. doi: 10.1038/nrm1230
23. Fernandez-Martinez J, Rout MP. 2012. A jumbo problem: Mapping the structure and functions of the nuclear pore complex. Current Opinion in Cell Biology 24:92–99. doi: 10.1016/j.ceb.2011.12.013
24. Floch AG, Palancade B, Doye V. 2014. Fifty years of nuclear pores and nucleocytoplasmic transport studies: Multiple tools revealing complex rules. Methods in Cell Biology 122:1–40. doi: 10.1016/B978-0-12-417160-2.00001-1
25. Forwood JK, Lange A, Zachariae U, Marfori M, Preast C, Grubmüller H, Stewart M, Corbett AH, Kobe B. 2010. Quantitative structural analysis of importin-b flexibility: Paradigm for solenoid protein structures. Structure 18: 1171–1183. doi: 10.1016/j.str.2010.06.015
26. Frey S, Richter RP, Görlich D. 2006. Fg-rich repeats of nuclear pore proteins form a three-dimensional meshwork with hydrogel-like properties. Science 314:815–817. doi: 10.1126/science.1132516
27. Frey S, Görlich D. 2007. A saturated fg-repeat hydrogel can reproduce the permeability properties of nuclear pore complexes. Cell 130:512–523. doi: 10.1016/j.cell.2007.06.024
28. Frey S, Görlich D. 2009. Fg/FxFG as well as GLFG repeats form a selective permeability barrier with self-healing properties. The EMBO Journal 28:2554–2567. doi: 10.1038/emboj.2009.199
29. Gamini R, Han W, Stone JE, Schulten K. 2014. Assembly of nsp1 nucleoporins provides insight into nuclear pore complex gating. PLoS Computational Biology 10:e1003488. doi: 10.1371/journal.pcbi.1003488
30. Ghavami A, Veenhoff LM, van der Giessen E, Onck PR. 2014. Probing the disordered domain of the nuclear pore complex through coarse-grained molecular dynamics simulations. Biophysical Journal 107:1393–1402. doi: 10.1016/j.bpj.2014.07.060
31. Görlich D, Kutay U. 1999. Transport between the cell nucleus and the cytoplasm. Annual Review of Cell and Developmental Biology 15:607–660. doi: 10.1146/annurev.cellbio.15.1.607
32. Görlich D, Seewald MJ, Ribbeck K. 2003. Characterization of ran-driven cargo transport and the rangtpase system by kinetic measurements and computer simulation. The EMBO Journal 22:1088–1100. doi: 10.1093/emboj/cdg113
33. Grossman E, Medalia O, Zwerger M. 2012. Functional architecture of the nuclear pore complex. Annual Review of Biophysics 41:557–584. doi: 10.1146/annurev-biophys-050511-102328
34. Hahn S, Schlenstedt G. 2011. Importin b-type nuclear transport receptors have distinct binding affinities for ran-gtp. Biochemical and Biophysical Research Communications 406:383–388. doi: 10.1016/j.bbrc.2011.02.051
35. Hough LE, Dutta K, Sparks S, Temel DB, Kamal A, Tetenbaum-Novatt J, Rout MP, Cowburn D. 2015. The molecular mechanism of nuclear transport revealed by atomic-scale measurements. eLife 4. doi: 10.7554/eLife.10027
36. Hülsmann BB, Labokha AA, Görlich D. 2012. The permeability of reconstituted nuclear pores provides direct evidence for the selective phase model. Cell 150:738–751. doi: 10.1016/j.cell.2012.07.019
37. Hyman AA, Simons K. 2012. Cell biology. beyond oil and water–phase transitions in cells. Science 337:1047–1049. doi: 10.1126/science.1223728
38. Isgro TA, Schulten K. 2005. Binding dynamics of isolated nucleoporin repeat regions to importin-beta. Structure 13:1869–1879. doi: 10.1016/j.str.2005.09.007
39. Israelachvili JN. 1991. Intermolecular and Surface Forces. Academic Press.
40. Johannsmann D. Software QTM. http://www2.pc.tu-clausthal.de/dj/software_en.shtml.
41. Johannsmann D. 1999. Viscoelastic analysis of organic thin films on quartz resonators. Macromolecular Chemistry and Physics 200:501–516. doi: 10.1002/(SICI)1521-3935(19990301)200:3<501::AID-MACP501>3.0.CO;2-W
42. Johannsmann D. 2008. Viscoelastic, mechanical, and dielectric measurements on complex samples with the quartz crystal microbalance. Physical Chemistry Chemical Physics 10:4516–4534. doi: 10.1039/b803960g
43. Kapinos LE, Schoch RL, Wagner RS, Schleicher KD, Lim RY. 2014. Karyopherin-centric control of nuclear pores based on molecular occupancy and kinetic analysis of multivalent binding with FG nucleoporins. Biophysical Journal 106:1751–1762. doi: 10.1016/j.bpj.2014.02.021
44. Keminer O, Peters R. 1999. Permeability of single nuclear pores. Biophysical Journal 77:217–228. doi: 10.1016/S0006-3495(99)76883-9
45. Kırlı K, Karaca S, Dehne HJ, Samwer M, Pan KT, Lenz C, Urlaub H, Görlich D. 2015. A deep proteomics perspective on crm1-mediated nuclear export and nucleocytoplasmic partitioning. eLife 4. doi: 10.7554/eLife.11466
46. Labokha AA, Gradmann S, Frey S, Hülsmann BB, Urlaub H, Baldus M, Görlich D. 2013. Systematic analysis of barrier-forming FG hydrogels from xenopus nuclear pore complexes. The EMBO Journal 32:204–218. doi: 10.1038/emboj.2012.302
47. Lata S, Gavutis M, Piehler J. 2006. Monitoring the dynamics of ligand-receptor complexes on model membranes. Journal of the American Chemical Society 128:6–7. doi: 10.1021/ja054700l
48. Lim RY, Fahrenkrog B, Köser J, Schwarz-Herion K, Deng J, Aebi U. 2007. Nanomechanical basis of selective gating by the nuclear pore complex. Science 318:640–643. doi: 10.1126/science.1145980
49. Lowe AR, Tang JH, Yassif J, Graf M, Huang WY, Groves JT, Weis K, Liphardt JT. 2015. Importin-b modulates the permeability of the nuclear pore complex in a ran-dependent manner. eLife 4:e04052. doi: 10.7554/eLife.04052
50. Macara IG. 2001. Transport into and out of the nucleus. Microbiology and Molecular Biology Reviews 65:570–594. doi: 10.1128/MMBR.65.4.570-594.2001
51. Miao L, Schulten K. 2009. Transport-related structures and processes of the nuclear pore complex studied through molecular dynamics. Structure 17:449–459. doi: 10.1016/j.str.2008.12.021
52. Milles S, Mercadante D, Aramburu IV, Jensen MR, Banterle N, Koehler C, Tyagi S, Clarke J, Shammas SL, Blackledge M, Gräter F, Lemke EA. 2015. Plasticity of an ultrafast interaction between nucleoporins and nuclear transport receptors. Cell 163:734–745. doi: 10.1016/j.cell.2015.09.047
53. Mincer JS, Simon SM. 2011. Simulations of nuclear pore transport yield mechanistic insights and quantitative predictions. Proceedings of the National Academy of Sciences of the United States of America 108:E351–358. doi: 10.1073/pnas.1104521108
54. Mohr D, Frey S, Fischer T, Güttler T, Görlich D. 2009. Characterisation of the passive permeability barrier of nuclear pore complexes. The EMBO Journal 28:2541–2553. doi: 10.1038/emboj.2009.200
55. Moussavi-Baygi R, Jamali Y, Karimi R, Mofrad MRK. 2011a. Biophysical coarse-grained modeling provides insights into transport through the nuclear pore complex. Biophysical Journal 100:1410–1419. doi: 10.1016/j.bpj.2011.01.061
56. Moussavi-Baygi R, Jamali Y, Karimi R, Mofrad MRK. 2011b. Brownian dynamics simulation of nucleocytoplasmic transport: A coarse-grained model for the functional state of the nuclear pore complex. PLoS Computational Biology 7:e1002049. doi: 10.1371/journal.pcbi.1002049
57. Opferman MG, Coalson RD, Jasnow D, Zilman A. 2012. Morphological control of grafted polymer films via attraction to small nanoparticle inclusions. Physical Review E 86:031806. doi: 10.1103/PhysRevE.86.031806
58. Opferman MG, Coalson RD, Jasnow D, Zilman A. 2013. Morphology of polymer brushes infiltrated by attractive nanoinclusions of various sizes. Langmuir: The ACS Journal of Surfaces and Colloids 29:8584–8591. doi: 10.1021/la4013922
59. Osmanovic D, Bailey J, Harker AH, Fassati A, Hoogenboom BW, Ford IJ. 2012. Bistable collective behavior of polymers tethered in a nanopore. Physical Review E 85:061917. doi: 10.1103/PhysRevE.85.061917
60. Osmanović D, Fassati A, Ford IJ, Hoogenboom BW. 2013a. Physical modelling of the nuclear pore complex. Soft Matter 9:10442–10451. doi: 10.1039/c3sm50722j
61. Osmanović D, Ford IJ, Hoogenboom BW. 2013b. Model inspired by nuclear pore complex suggests possible roles for nuclear transport receptors in determining its structure. Biophysical Journal 105:2781–2789. doi: 10.1016/j.bpj.2013.11.013
62. Patel SS, Belmont BJ, Sante JM, Rexach MF. 2007. Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex. Cell 129:83–96. doi: 10.1016/j.cell.2007.01.044
63. Peleg O, Tagliazucchi M, Kröger M, Rabin Y, Szleifer I. 2011. Morphology control of hairy nanopores. ACS Nano 5:4737–4747. doi: 10.1021/nn200702u
64. Peters R. 2005. Translocation through the nuclear pore complex: Selectivity and speed by reduction-of-dimensionality. Traffic 6:421–427. doi: 10.1111/j.1600-0854.2005.00287.x
65. Peters R. 2009. Translocation through the nuclear pore: Kaps pave the way. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology 31:466–477. doi: 10.1002/bies.200800159
66. Popken P, Ghavami A, Onck PR, Poolman B, Veenhoff LM. 2015. Size-dependent leak of soluble and membrane proteins through the yeast nuclear pore complex. Molecular biology of the cell 26:1386–1394. doi: 10.1091/mbc.E14-07-1175
67. Port SA, Monecke T, Dickmanns A, Spillner C, Hofele R, Urlaub H, Ficner R, Kehlenbach RH. 2015. Structural and functional characterization of crm1-nup214 interactions reveals multiple fg-binding sites involved in nuclear export. Cell Reports 13:690–702. doi: 10.1016/j.celrep.2015.09.042
68. Radu A, Moore MS, Blobel G. 1995. The peptide repeat domain of nucleoporin nup98 functions as a docking site in transport across the nuclear pore complex. Cell 81:215–222. doi: 10.1016/0092-8674(95)90331-3
69. Ribbeck K, Görlich D. 2001. Kinetic analysis of translocation through nuclear pore complexes. The EMBO Journal 20:1320–1330. doi: 10.1093/emboj/20.6.1320
70. Richter RP, Rodenhausen KB, Eisele NB, Schubert M. 2013. Coupling spectroscopic ellipsometry and quartz crystal microbalance to study organic films at the solid-liquid interface. In: Hinrichs K, Eichhorn K-J (Eds). Ellipsometry of Functional Organic Surfaces and Films. Heidelberg: Springer. doi: 10.1007/978-3-642-40128-2_11
71. Rout MP, Wente SR. 1994. Pores for thought: Nuclear pore complex proteins. Trends in cell biology 4:357–365. doi: 10.1016/0962-8924(94)90085-x
72. Rout MP, Aitchison JD, Suprapto A, Hjertaas K, Zhao Y, Chait BT. 2000. The yeast nuclear pore complex: Composition, architecture, and transport mechanism. The Journal of cell biology 148:635–651. doi: 10.1083/jcb.148.4.635
73. Schleicher KD, Dettmer SL, Kapinos LE, Pagliara S, Keyser UF, Jeney S, Lim RY. 2014. Selective transport control on molecular velcro made from intrinsically disordered proteins. Nature Nanotechnology 9:525–530. doi: 10.1038/nnano.2014.103
74. Schmidt HB, Görlich D. 2015. Nup98 FG domains from diverse species spontaneously phase-separate into particles with nuclear pore-like permselectivity. eLife 4. doi: 10.7554/eLife.04251
75. Schoch RL, Kapinos LE, Lim RY. 2012. Nuclear transport receptor binding avidity triggers a self-healing collapse transition in fg-nucleoporin molecular brushes. Proceedings of the National Academy of Sciences of the United States of America 109:16911–16916. doi: 10.1073/pnas.1208440109
76. Shirai A, Matsuyama A, Yashiroda Y, Hashimoto A, Kawamura Y, Arai R, Komatsu Y, Horinouchi S, Yoshida M. 2008. Global analysis of gel mobility of proteins and its use in target identification. The Journal of Biological Chemistry 283:10745–10752. doi: 10.1074/jbc.M709211200
77. Stirnemann G, Giganti D, Fernandez JM, Berne BJ. 2013. Elasticity, structure, and relaxation of extended proteins under force. Proceedings of the National Academy of Sciences of the United States of America 110: 3847–3852. doi: 10.1073/pnas.1300596110
78. Strawn LA, Shen T, Shulga N, Goldfarb DS, Wente SR. 2004. Minimal nuclear pore complexes define FG repeat domains essential for transport. Nature Cell Biology 6:197–206. doi: 10.1038/ncb1097
79. Tagliazucchi M, Peleg O, Kröger M, Rabin Y, Szleifer I. 2013. Effect of charge, hydrophobicity, and sequence of nucleoporins on the translocation of model particles through the nuclear pore complex. Proceedings of the National Academy of Sciences of the United States of America 110:3363–3368. doi: 10.1073/pnas.1212909110
80. Uversky VN, Dunker AK. 2010. Understanding protein non-folding. Biochimica et biophysica acta 1804:1231–1264. doi: 10.1016/j.bbapap.2010.01.017
81. Wagner RS, Kapinos LE, Marshall NJ, Stewart M, Lim RY. 2015. Promiscuous binding of karyopherinb1 modulates FG nucleoporin barrier function and expedites NTF2 transport kinetics. Biophysical Journal 108:918–927. doi: 10.1016/j.bpj.2014.12.041
82. Weiss JN. 1997. The hill equation revisited: Uses and misuses. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 11:835–841.
83. Wolf C, Mofrad MR. 2008. On the octagonal structure of the nuclear pore complex: Insights from coarse-grained models. Biophysical Journal 95:2073–2085. doi: 10.1529/biophysj.108.130336
84. Wühr M, Freeman RM, Presler M, Horb ME, Peshkin L, Gygi SP, Kirschner MW. 2014. Deep proteomics of the xenopus laevis egg using an mrna-derived reference database. Current biology 24:1467–1475. doi: 10.1016/j.cub.2014.05.044
85. Yamada J, Phillips JL, Patel S, Goldfien G, Calestagne-Morelli A, Huang H, Reza R, Acheson J, Krishnan VV, Newsam S, Gopinathan A, Lau EY, Colvin ME, Uversky VN, Rexach MF. 2010. A bimodal distribution of two distinct categories of intrinsically disordered structures with separate functions in FG nucleoporins. Molecular & Cellular Proteomics 9:2205–2224. doi: 10.1074/mcp.M000035-MCP201
86. Yang Q, Rout MP, Akey CW. 1998. Three-dimensional architecture of the isolated yeast nuclear pore complex: Functional and evolutionary implications. Molecular Cell 1:223–234. doi: 10.1016/S1097-2765(00)80023-4
87. Yang W, Musser SM. 2006. Nuclear import time and transport efficiency depend on importin beta concentration. The Journal of Cell Biology 174:951–961. doi: 10.1083/jcb.200605053
88. Zhulina EB, Borisov OV, Priamitsyn VA. 1990. Theory of steric stabilization of colloid dispersions by grafted polymers. Journal of Colloid and Interface Science 137:495–511. doi: 10.1016/0021-9797(90)90423-L