Role of molecular charge in nucleocytoplasmic transport

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Goryaynov, Alexander ^a   Yang, Weidong ^a  

^a Temple University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; RIBOSOMAL PROTEIN L17; RIBOSOME PROTEIN;

ARTICLE; BINDING KINETICS; CELL NUCLEUS; CHEMICAL PARAMETERS; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; HELA CELL; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MOLECULAR CHARGE; MOLECULAR SIZE; NUCLEAR PORE COMPLEX; NUCLEOCYTOPLASMIC TRANSPORT; SINGLE MOLECULE FLUORESCENCE MICROSCOPY; SPATIOTEMPORAL ANALYSIS; STATIC ELECTRICITY; SURFACE CHARGE; THREE DIMENSIONAL IMAGING; ACTIVE TRANSPORT; CHEMICAL STRUCTURE; CHEMISTRY; DIFFUSION; HELA CELL LINE; KINETICS; METABOLISM; MOLECULAR WEIGHT; NUCLEAR PORE; PROBABILITY; PROTEIN CONFORMATION;

ACTIVE TRANSPORT, CELL NUCLEUS; DIFFUSION; HELA CELLS; HUMANS; KINETICS; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; MOLECULAR WEIGHT; NUCLEAR PORE; PROBABILITY; PROTEIN CONFORMATION; RIBOSOMAL PROTEINS;

EID: 84895887455     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088792     Document Type: Article

References (53)

1. Hetzer M (2010) The nuclear envelope. Cold Spring Harb Perspect Biol 2: a000539.
2. Hetzer M, Wente S (2009) Border control at the nucleus: biogenesis and organization of the nuclear membrane and pore complexes. Dev Cell 17: 606-616.
3. Powers M, Forbes D (2012) Nuclear transport: beginning to gel? Curr Biol 22: R1006-1009.
4. Görlich D, Kutay U (1999) Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol 15: 607-660. (Pubitemid 32250388)
5. Carmody S, Wente S (2009) mRNA nuclear export at a glance. J Cell Sci 122: 1933-1937.
6. Fahrenkrog B, Aebi U (2003) The nuclear pore complex: nucleocytoplasmic transport and beyond. Nat Rev Mol Cell Biol 4: 757-766. (Pubitemid 37229372)
7. Cronshaw JM, Krutchinsky AN, Zhang W, Chait BT, Matunis MJ (2002) Proteomic analysis of the mammalian nuclear pore complex. J Cell Biol 158: 915-927. (Pubitemid 35001082)
8. 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. Proc Natl Acad Sci USA 100: 2450-2455. (Pubitemid 36297519)
9. Cronshaw J, Krutchinsky A, Zhang W, Chait B, Matunis M (2002) Proteomic analysis of the mammalian nuclear pore complex. J Cell Biol 158: 915-27. (Pubitemid 35001082)
10. Rout M, Aitchison J (2001) The nuclear pore complex as a transport machine. J Biol Chem 276: 16593-16596.
11. Rout M, Aitchison J, Magnasco M, Chait B (2003) Virtual gating and nuclear transport: the hole picture. Trends Cell Biol 13: 622-628. (Pubitemid 37415027)
12. Rout M, Aitchison J, Suprapto A, Hjertaas K, Zhao Y, et al (2000) The yeast nuclear pore complex: composition, architecture, and transport mechanism. J Cell Biol 148: 635-641.
13. Suntharalingam M, Wente S (2003) Peering through the pore: nuclear pore complex structure, assembly, and function. Dev Cell 4: 775-789. (Pubitemid 36676031)
14. 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.
15. Bayliss R, Littlewood T, Strawn L, Wente S, Stewart M (2002) GLFG and FxFG nucleoporins bind to overlapping sites on importin-beta. J Biol Chem 277: 50597-50606. (Pubitemid 36042219)
16. Otsuka S, Iwasaka S, Yoneda Y, Takeyasu K, Yoshimura SH (2008) Individual binding pockets of importin-beta for FG-nucleoporins have different binding properties and different sensitivities to RanGTP. Proc Natl Acad Sci USA 105: 16101-16106.
17. Colwell LJ, Brenner MP, Ribbeck K (2010) Charge as a selection criterion for translocation through the nuclear pore complex. PLoS Comput Biol 6: e1000747.
18. Ribbeck K, Gorlich D (2001) Kinetic analysis of translocation through nuclear pore complexes. EMBO J 20: 1320-30. (Pubitemid 32233972)
19. Frey S, Gorlich D (2007) A saturated FG-repeat hydrogel can reproduce the permeability properties of nuclear pore complexes. Cell 130: 512-23. (Pubitemid 47208521)
20. Macara I (2001) Transport into and out of the nucleus. Microbiol Mol Biol Rev 65: 570-594.
21. Peters R (2005) Translocation through the nuclear pore complex: selectivity and speed by reduction-of-dimensionality. Traffic 6: 421-427.
22. Akey CW, Radermacher M (1993) Architecture of the Xenopus nuclear-pore complex revealed by 3-dimensional cryoelectron microscopy. J Cell Biol 122: 1-19. (Pubitemid 23188795)
23. Hinshaw JE, Carragher BO, Milligan RA (1992) Architecture and design of the nuclear pore complex. Cell 69: 1133-1141.
24. Yang Q, Rout M, Akey C (1998) Three-dimensional architecture of the isolated yeast nuclear pore complex: functional and evolutionary implications. Mol Cell 1: 223-234. (Pubitemid 128378663)
25. Kramer A, Liashkovich I, Ludwig Y, Shahin V (2008) Atomic force microscopy visualises a hydrophobic meshwork in the central channel of the nuclear pore. Pflugers Arch 456: 155-162.
26. Naim B, Brumfeld V, Kapon R, Kiss V, Nevo R, et al (2007) Passive and facilitated transport in nuclear pore complexes is largely uncoupled. J Biol Chem 282: 3881-3888. (Pubitemid 47084467)
27. Ma J, Goryaynov A, Sarma A, Yang W (2012) Self-regulated viscous channel in the nuclear pore complex, Proc Natl Acad Sci USA 109: 7326-7331.
28. Goryaynov A, Ma J, Yang W (2012) Single-molecule studies of nuclear transport: from one dimension to three dimensions, Integ Biol 4: 10-21.
29. Yang W (2011) "Natively Unfolded" Nucleoporins in Nucleocytoplasmic Transport: Clustered or Evenly Distributed? Nucleus 2: 10-16.
30. Ma J, Yang W (2010) Three-Dimensional Distribution of Transient Interactions in the Nuclear Pore Obtained by Single-Molecule Snapshots, Proc Natl Acad Sci USA 107: 7305-7310.
31. Yang W (2013) Distinct, but not completely separate spatial transport routes in the nuclear pore complex. Nucleus 4: 166-175.
32. 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. Proc Natl Acad Sci USA 110: 3363-3368.
33. Cronican JJ, Thompson DB, Beier KT, McNaughton BR, Cepko CL, et al (2010) Potent delivery of functional proteins into Mammalian cells in vitro and in vivo using a supercharged protein. ACS Chem Biol 5: 747-752.
34. McNaughton BR, Cronican JJ, Thompson DB, Liu DR (2009) Mammalian cell penetration, siRNA transfection, and DNA transfection by supercharged proteins. Proc Natl Acad Sci USA 106: 6111-6116.
35. Mohr D, Frey S, Fischer T, Güttler T, Görlich D (2009) Characterization of the passive permeability barrier of nuclear pore complexes. EMBO J 28: 2541-2553.
36. Golich D, Laskey R (1995) Distinct functions for the two importin subunits in nuclear protein import. Nature 377: 246248.
37. Yang W, Gelles J, Musser SM (2004) Imaging of single-molecule translocation through nuclear pore complexes. Proc Natl Acad Sci USA 101: 12887-12892. (Pubitemid 39167553)
38. Yang W, Musser S-M (2006) Nuclear import time and transport efficiency depend on importin beta concentration. J Cell Biol 174: 951-961. (Pubitemid 44455184)
39. Dange T, Grünwald D, Grünwald A, Peters R, Kubitscheck U (2008) Autonomy and robustness of translocation through the nuclear pore complex: a single-molecule study. J Cell Biol 183: 77-86.
40. Rexach M, Blobel G (1995) Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell 83: 683-692.
41. Wool IG, Chan YL, Glück A (1996). Structure and evolution of mammalian ribosomal proteins. Biochem Cell Biol 73: 933-947.
42. Shi Y, Zhai H, Wang X, Han Z, Liu C, et al (2004). Ribosomal proteins S13 and L23 promote multidrug resistance in gastric cancer cells by suppressing drug-induced apoptosis. Exp Cell Res 296: 337-346. (Pubitemid 38624654)
43. Jin A, Itahana K, O'Keefe K, Zhang Y (2004). Inhibition of HDM2 and Activation of p53 by Ribosomal Protein L23. Mol Cell Biol 24: 7669-7680. (Pubitemid 39121492)
44. Dai MS, Zeng SX, Jin Y, Sun XX, Lu H (2004). Ribosomal Protein L23 Activates p53 by Inhibiting MDM2 Function in Response to Ribosomal Perturbation but Not to Translation Inhibition. Mol Cell Biol 24: 7654-7668. (Pubitemid 39121491)
45. Naim B, Zbaida D, Dagan S, Kapon R, Reich Z (2009) Cargo surface hydrophobicity is sufficient to overcome the nuclear pore complex selectivity barrier. EMBO J 28: 2697-2705.
46. Kumeta M, Yamaguchi H, Yoshimura SH, Takeyasu K (2012) Karyopherin-independent spontaneous transport of amphiphilic proteins through the nuclear pore J Cell Sci 125: 497 9-4984.
47. Kapon R, Naim B, Zbaida D, Nevo R, Tsabari O, et al (2010) Permeating the nuclear pore complex. Nucleus. 1: 475-480.
48. Schoch R, Kapinos L, Lim R (2012) Nuclear transport receptor binding avidity triggers a self-healing collapse transition in FG-nucleoporin molecular brushes. Proc Natl Acad Sci USA. 109: 16911-16916.
49. Tokunaga M, Imamoto N, Sakata-Sogawa K (2008) Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat Methods 5: 159-161. (Pubitemid 351181742)
50. Adam SA, Marr RS, Gerace L (1990) Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J Cell Biol. 111: 807-816.
51. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA 98: 10037-10041. (Pubitemid 32802969)
52. Dolinsky TJ, Czodrowski P, Li H, Nielsen JE, Jensen JH, et al (2007) Expanding and upgrading automated preparation of biomolecular structures for molecular simulations. Nucleic Acids Res 35: W522-525.
53. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al (2004) A visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.