Intramolecular cohesion of coils mediated by phenylalanine-glycine motifs in the natively unfolded domain of a nucleoporin

PLoS Computational Biology

Volumn 4, Issue 8, 2008, Pages

  Krishnan, V V ^a,b,c   Lau, Edmond Y ^d   Yamada, Justin ^b   Denning, Daniel P ^e   Patel, Samir S ^b   Colvin, Michael E ^f   Rexach, Michael F ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CALIFORNIA STATE UNIVERSITY   (United States)

^d LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION; CELLS; CYTOLOGY; PROTEINS;

BIOPHYSICAL TECHNIQUES; COMPLEX PERMEABILITY; DYNAMIC ENSEMBLE; DYNAMIC STRUCTURE; MOLECULAR MODELING TECHNIQUES; NUCLEAR PORE COMPLEXES; NUCLEOPORINS; PERMEABILITY BARRIERS; SIZE-SELECTIVE; YEAST NUCLEOPORIN;

AMINO ACIDS;

GLYCINE; KARYOPHERIN; NUCLEOPORIN; PHENYLALANINE; POLYPEPTIDE; NUP116 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE PERMEABILITY; CELL NUCLEUS; CYTOPLASM; MACROMOLECULE; MOLECULAR MODEL; NUCLEAR PORE COMPLEX; PERMEABILITY BARRIER; PROTEIN STRUCTURE; ACTIVE TRANSPORT; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR WEIGHT; NUCLEAR PORE; PHYSIOLOGY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN QUATERNARY STRUCTURE; SACCHAROMYCES CEREVISIAE; THERMODYNAMICS; ULTRASTRUCTURE;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID MOTIFS; GLYCINE; MODELS, MOLECULAR; MOLECULAR WEIGHT; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; PHENYLALANINE; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, QUATERNARY; REPETITIVE SEQUENCES, AMINO ACID; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; THERMODYNAMICS;

EID: 50949090481     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000145     Document Type: Article

References (64)

1. Tran E, Wente S (2006) Dynamic nuclear pore complexes: life on the edge. Cell 125: 1041-1053.
2. Pante N, Kann M (2002) Nuclear pore complex is able to transport macromolecules with diameters of about 39 nm. Mol Biol Cell 13: 425-434.
3. 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.
4. Rout MP, Aitchison JD, Suprapto A, Hjertaas K, Zhao Y, et al. (2000) The yeast nuclear pore complex: composition, architecture, and transport mechanism. J Cell Biol 148: 635-651.
5. Strawn LA, Shen T, Shulga N, Goldfarb DS, Wente SR (2004) Minimal nuclear pore comlexes define FG repeat domains essential for transport. Nat Cell Biol 6: 197-206.
6. Allen NP, Huang L, Burlingame A, Rexach M (2001) Proteomic analysis of nucleoporin interacting proteins. J Biol Chem 276: 29268-29274.
7. Patel SS, Belmont B, Sante J, Rexach M (2007) Natively-unfolded nucleoporins gate protein diffusion across the nuclear pore complex. Cell 129: 83-96.
8. Frey S, Gorlich D (2007) A saturated FG-repeat hydrogel can reproduce the permeability properties of nuclear pore complexes. Cell 130: 512-523.
9. 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 U S A 100: 2450-2455.
10. Yang Q, Rout MP, Akey CW (1998) Three-dimensional architecture of the isolated yeast nuclear pore complex: functional and evolutionary implications. Mol Cell 2: 223-234.
11. Rout MP, Aitchison JD, Magnasco MO, Chait BT (2003) Virtual gating and nuclear transport: the hole picture. Trends Cell Biol 13: 622-628.
12. Lim RY, Huang NP, Koser J, Deng J, Lau KH, et al. (2006) Flexible phenylalanine-glycine nucleoporins as entropic barriers to nucleocytoplasmic transport. Proc Natl Acad Sci U S A 103: 9512-9517.
13. Ribbeck K, Gorlich D (2002) The permeability barrier of nuclear pore complexes appears to operate via hydrophobic exclusion. EMBO J 21: 2664-2671.
14. Frey S, Richter R, Gorlich D (2006) FG-rich repeats of nuclear pore complex proteins form a three-dimensional meshwork with hydrogel-like properties. Science 314: 815-817.
15. Baldwin R, Zimm B (2000) Are denatured proteins ever random coil? Proc Natl Acad Sci U S A 97: 12391-12392.
16. Vucetic S, Brown CJ, Dunker AK, Obradovic Z (2003) Flavors of protein disorder. Proteins 52: 573-584.
17. Bradley P, Misura KM, Baker D (2005) Toward high-resolution de novo structure prediction for small proteins. Science 309: 1868-1871.
18. Kuhlman B, Dantas G, Ireton GC, Varani G, Stoddard BL, et al. (2003) Design of a novel globular protein fold with atomic-level accuracy. Science 302: 1364-1368.
19. Lockless SW, Ranganathan R (1999) Evolutionarily conserved pathways of energetic connectivity in protein families. Science 286: 295-299.
20. Schueler-Furman O, Wang C, Bradley P, Misura K, Baker D (2005) Progress in modeling of protein structures and interactions. Science 310: 638-642.
21. Uversky VN (2002) Natively unfolded proteins: a point where biology waits for physics. Protein Sci 11: 739-756.
22. Dyson HJ, Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6: 197-208.
23. Tompa P (2002) Intrinsically unstructured proteins. Trends Biochem Sci 27: 527-533.
24. Tompa P (2005) The interplay between structure and function in intrinsically unstructured proteins. FEBS Lett 579: 3346-3354.
25. Gilchrist D, Mykytka B, Rexach M (2002) Accelerating the rate of disassembly of karyopherin.cargo complexes. J Biol Chem 277: 18161-18172.
26. Jha AK, Colubri A, Freed KF, Sosnick TR (2005) Statistical coil model of the unfolded state: resolving the reconciliation problem. Proc Natl Acad Sci U S A 102: 13099-13104.
27. Jha AK, Colubri A, Zaman MH, Koide S, Sosnick TR, et al. (2005) Helix, sheet, and polyproline II frequencies and strong nearest neighbor effects in a restricted coil library. Biochemistry 44: 9691-9702.
28. Bernado P, Bertoncini CW, Griesinger C, Zweckstetter M, Blackledge M (2005) Defining long-range order and local disorder in native α-synuclein using residual dipolar couplings. J Am Chem Soc 127: 17968-17969.
29. Bernado P, Blanchard L, Timmins P, Marion D, Ruigrok R, et al. (2005) A structural model for unfolded proteins from residual dipolar couplings and small-angle X-ray scattering. Proc Natl Acad Sci U S A 102: 17002-17007.
30. Tjandra N, Bax A (1997) Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278: 1111-1114.
31. Ollerenshaw JE, Kaya H, Chan HS, Kay LE (2004) Sparsely populated folding intermediates of the Fyn SH3 domain: matching native-centric essential dynamics and experiment. Proc Natl Acad Sci U S A 101: 14748-14753.
32. Wang X, Vitalis A, Wyczalkowski MA, Pappu RV (2006) Characterizing the conformational ensemble of monomeric polyglutamine. Proteins 63: 297-311.
33. Daura X, Gademann K, Schafer H, Jaun B, Seebach D, et al. (2001) The β-hairpin in solution: conformational study of a β-hexapeptide in methanol by NMR spectroscopy and MD simulation. J Am Chem Soc 123: 2393-2404.
34. Weinstock D, Narayanan C, Felts A, Andrec M, Levy R, et al. (2007) Distinguishing among structural ensembles of the GB1 peptide: REMD simulations and NMR experiments. J Am Chem Soc 129: 4858-4859.
35. Bokor M, Csizmok V, Kovacs D, Banki P, Friedrich P, et al. (2005) NMR relaxation studies on the hydrate layer of intrinsically unstructured proteins. Biophys J 88: 2030-2037.
36. Csizmok V, Bokor M, Banki P, Klement E, Medzihradszky KF, et al. (2005) Primary contact sites in intrinsically unstructured proteins: the case of calpastatin and microtubule-associated protein 2. Biochemistry 44: 3955-3964.
37. Wagner G (1997) An account of NMR in structural biology. Nat Struct Biol 4: 841-844.
38. Wagner G, Wüthrich K (1979) Correlation between the amide proton exchange rates and the denaturation temperatures in globular proteins related to the basic pancreatic trypsin inhibitor. J Mol Biol 130: 31-37.
39. Wilkins DK, Grimshaw SB, Receveur V, Dobson CM, Jones JA, et al. (1999) Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques. Biochemistry 38: 16424-16431.
40. Krishnan V (1997) Determination of oligomeric state of proteins in solution from pulsed-field-gradient self-diffusion coefficient measurements. A comparison of experimental, theoretical, and hard-sphere approximated values. J Magn Reson 124: 468-473.
41. Tcherkasskaya O, Davidson E, Uversky V (2003) Biophysical constraints for protein structure prediction. J Proteome Res 2: 37-42.
42. Denning D, Rexach M (2007) Rapid evolution exposes the boundaries of domain structure and function in natively unfolded FG nucleoporins. Mol Cell Proteomics 6: 272-282.
43. Alber F, Dokudovskaya S, Veenhoff L, Zhang W, Kipper J, et al. (2007) Determining the architectures of macromolecular assemblies. Nature 450: 683-694.
44. Alber F, Dokudovskaya S, Veenhoff L, Zhang W, Kipper J, et al. (2007) The molecular architecture of the nuclear pore complex. Nature 450: 695-701.
45. Lim R, Fahrenkrog B, Köser J, Schwarz-Herion K, Deng J, et al. (2007) Nanomechanical basis for selective gating by the nuclear pore complex. Science 318: 640-643.
46. Lim R, Köser J, Huang S, Schwarz-Herion K, Aebi U (2007) Nanomechanical interactions of phenylalanine-glycine nucleoporins studied by single molecule force-volume microscopy. J Stuct Biol 159: 277-289.
47. Isgro TA, Schulten K (2005) Binding dynamics of isolated nucleoporin repeat regions to importin-̈. Structure 13: 1869-1879.
48. Burley SK, Petsko GA (1985) Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science 229: 23-28.
49. Dhe-Paganon S, Werner ED, Nishi M, Hansen L, Chi YI, et al. (2004) A phenylalanine zipper mediates APS dimerization. Nat Struct Mol Biol 11: 968-974.
50. Callebaut I, Courvalin J, Worman H, Mornon J (1997) Hydrophobic cluster analysis reveals a third chromodomain in the Tetrahymena Pdd1p protein of the chromo superfamily. Biochem Biophys Res Commun 235: 103-107.
51. Gaboriaud C, Bissery V, Benchetrit T, Mornon J (1987) Hydrophobic cluster analysis: an efficient new way to compare and analyse amino acid sequences. FEBS Lett 224: 149-155.
52. Kustanovich T, Rabin Y (2004) Metastable network model of protein transport through nuclear pores. Biophys J 86: 2008-2016.
53. Lim R, Aebi U, Fahrenkrog B (2008) Towards reconciling structure and function in the nuclear pore complex. Histochem Cell Biol 129: 105-116.
54. Macara IG (2001) Transport into and out of the nucleus. Microbiol Mol Biol Rev 65: 570-594.
55. Weis K (2007) The nuclear pore complex: oily spaghetti or gummy bear? Cell 130: 405-407.
56. Wang J, Cieplak P, Kollman PA (2000) How well does a RESP (restrained electrostatic potential) model do in calculating the conformational energies of organic and biological molecules? J Comput Chem 21: 1049-1074.
57. Case DA, Cheatham TE III, Darden T, Gohlke H, Luo R, et al. (2005) The Amber biomolecular simulation programs. J Comput Chem 26: 1668-1688.
58. Wang J, Wolf RM, Caldwell JW, Kollman PA, Case DA (2004) Development and testing of a general amber force field. J Comput Chem 25: 1157-1174.
59. Onufriev A, Case DA, Bashford D (2002) Effective Born radii in the generalized Born approximation: the importance of being perfect. J Comput Chem 23: 1297-1304.
60. Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637.
61. Piotto M, Saudek V, Sklenar V (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J Biomol NMR 2: 661-665.
62. Krishnan VV, Thornton KH, Cosman M (1999) An improved experimental scheme to measure self-diffusion coefficients of biomolecules with an advantageous use of radiation damping. Chem Phys Lett 302: 317-323.
63. Garcia de la Torre JG, Bloomfield VA (1981) Hydrodynamic properties of complex, rigid, biological macromolecules: theory and applications. Q Rev Biophys 14: 81-139.
64. Krishnan VV, Cosman M (1998) An empirical relationship between rotational correlation time and solvent accessible surface area. J Biomol NMR 12: 177-182.