The importin β binding domain as a master regulator of nucleocytoplasmic transport

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1813, Issue 9, 2011, Pages 1578-1592

  Lott, Kaylen ^a,b   Cingolani, Gino ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

IBB; Importin ; Importin ; Karyopherins; NLS; NPC; Nuclear import; Ran

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ISOPROTEIN; KARYOPHERIN ALPHA; KARYOPHERIN BETA; NUCLEOCYTOPLASMIC TRANSPORT PROTEIN; NUCLEOPORIN; STAT1 PROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CYTOPLASM; ENTHALPY; HELA CELL; HUMAN; INHIBITION KINETICS; MOLECULAR DOCKING; MOLECULAR EVOLUTION; NONHUMAN; NUCLEAR PORE COMPLEX; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REVIEW; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; ANIMALS; BETA KARYOPHERINS; BINDING SITES; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR LOCALIZATION SIGNALS; PHYLOGENY; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RNA CAP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 79960915158     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2010.10.012     Document Type: Review

References (119)

1. Kalderon D., Richardson W.D., Markham A.F., Smith A.E. Sequence requirements for nuclear location of simian virus 40 large-T antigen. Nature 1984, 311:33-38.
2. Kalderon D., Roberts B.L., Richardson W.D., Smith A.E. A short amino acid sequence able to specify nuclear location. Cell 1984, 39:499-509.
3. Robbins J., Dilworth S.M., Laskey R.A., Dingwall C. Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 1991, 64:615-623.
4. Jans D.A., Xiao C.Y., Lam M.H. Nuclear targeting signal recognition: a key control point in nuclear transport?. Bioessays 2000, 22:532-544.
5. Sessler R.J., Noy N. A ligand-activated nuclear localization signal in cellular retinoic acid binding protein-II. Mol. Cell 2005, 18:343-353.
6. Weis K., Ryder U., Lamond A.I. The conserved amino-terminal domain of hSRP1 alpha is essential for nuclear protein import. EMBO J. 1996, 15:1818-1825.
7. Huber J., Cronshagen U., Kadokura M., Marshallsay C., Wada T., Sekine M., Luhrmann R. Snurportin1, an m3G-cap-specific nuclear import receptor with a novel domain structure. EMBO J. 1998, 17:4114-4126.
8. Jullien D., Gorlich D., Laemmli U.K., Adachi Y. Nuclear import of RPA in Xenopus egg extracts requires a novel protein XRIPalpha but not importin alpha. EMBO J. 1999, 18:4348-4358.
9. Cingolani G., Petosa C., Weis K., Muller C.W. Structure of importin-beta bound to the IBB domain of importin-alpha. Nature 1999, 399:221-229.
10. Mitrousis G., Olia A.S., Walker-Kopp N., Cingolani G. Molecular basis for the recognition of snurportin 1 by importin beta. J. Biol. Chem. 2008, 283:7877-7884.
11. Siomi H., Dreyfuss G. A nuclear localization domain in the hnRNP A1 protein. J. Cell Biol. 1995, 129:551-560.
12. Lee B.J., Cansizoglu A.E., Suel K.E., Louis T.H., Zhang Z., Chook Y.M. Rules for nuclear localization sequence recognition by karyopherin beta 2. Cell 2006, 126:543-558.
13. Cingolani G., Bednenko J., Gillespie M.T., Gerace L. Molecular basis for the recognition of a nonclassical nuclear localization signal by importin beta. Mol. Cell 2002, 10:1345-1353.
14. Gorlich D., Kutay U. Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell Dev. Biol. 1999, 15:607-660.
15. 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.
16. Rout M.P., Aitchison J.D., Magnasco M.O., Chait B.T. Virtual gating and nuclear transport: the hole picture. Trends Cell Biol. 2003, 13:622-628.
17. Fried H., Kutay U. Nucleocytoplasmic transport: taking an inventory. Cell. Mol. Life Sci. 2003, 60:1659-1688.
18. Peters R. Translocation through the nuclear pore complex: selectivity and speed by reduction-of-dimensionality. Traffic 2005, 6:421-427.
19. Tran E.J., Wente S.R. Dynamic nuclear pore complexes: life on the edge. Cell 2006, 125:1041-1053.
20. Weis K. The nuclear pore complex: oily spaghetti or gummy bear?. Cell 2007, 130:405-407.
21. 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.
22. Fahrenkrog B., Aebi U. The nuclear pore complex: nucleocytoplasmic transport and beyond. Nat. Rev. Mol. Cell Biol. 2003, 4:757-766.
23. Drummond S., Allen T. Structure, function and assembly of the nuclear pore complex. Symp. Soc. Exp. Biol. 2004, 89-114.
24. D'Angelo M.A., Hetzer M.W. Structure, dynamics and function of nuclear pore complexes. Trends Cell Biol. 2008, 18:456-466.
25. Fernandez-Martinez J., Rout M.P. Nuclear pore complex biogenesis. Curr. Opin. Cell Biol. 2009, 21:603-612.
26. Brohawn S.G., Partridge J.R., Whittle J.R., Schwartz T.U. The nuclear pore complex has entered the atomic age. Structure 2009, 17:1156-1168.
27. 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.
28. 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.
29. Bischoff F.R., Gorlich D. RanBP1 is crucial for the release of RanGTP from importin beta-related nuclear transport factors. FEBS Lett. 1997, 419:249-254.
30. Fornerod M., van Deursen J., van Baal S., Reynolds A., Davis D., Murti K.G., Fransen J., Grosveld G. The human homologue of yeast CRM1 is in a dynamic subcomplex with CAN/Nup214 and a novel nuclear pore component Nup88. EMBO J. 1997, 16:807-816.
31. Mosammaparast N., Pemberton L.F. Karyopherins: from nuclear-transport mediators to nuclear-function regulators. Trends Cell Biol. 2004, 14:547-556.
32. Lange A., Mills R.E., Lange C.J., Stewart M., Devine S.E., Corbett A.H. Classical nuclear localization signals: definition, function, and interaction with importin alpha. J. Biol. Chem. 2007, 282:5101-5105.
33. 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.
34. 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.
35. Matunis M.J., Wu J., Blobel G. SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex. J. Cell Biol. 1998, 140:499-509.
36. Ohtsubo M., Okazaki H., Nishimoto T. The RCC1 protein, a regulator for the onset of chromosome condensation locates in the nucleus and binds to DNA. J. Cell Biol. 1989, 109:1389-1397.
37. Richards S.A., Carey K.L., Macara I.G. Requirement of guanosine triphosphate-bound ran for signal-mediated nuclear protein export. Science 1997, 276:1842-1844.
38. Moroianu J., Blobel G. Protein export from the nucleus requires the GTPase Ran and GTP hydrolysis. Proc. Natl Acad. Sci. USA 1995, 92:4318-4322.
39. 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.
40. Goldfarb D.S., Corbett A.H., Mason D.A., Harreman M.T., Adam S.A. Importin alpha: a multipurpose nuclear-transport receptor. Trends Cell Biol. 2004, 14:505-514.
41. Kohler M., Speck C., Christiansen M., Bischoff F.R., Prehn S., Haller H., Gorlich D., Hartmann E. Evidence for distinct substrate specificities of importin alpha family members in nuclear protein import. Mol. Cell. Biol. 1999, 19:7782-7791.
42. O'Neill R.E., Palese P. NPI-1, the human homolog of SRP-1, interacts with influenza virus nucleoprotein. Virology 1995, 206:116-125.
43. Meyer T., Vinkemeier U. Nucleocytoplasmic shuttling of STAT transcription factors. Eur. J. Biochem. 2004, 271:4606-4612.
44. Tarendeau F., Boudet J., Guilligay D., Mas P.J., Bougault C.M., Boulo S., Baudin F., Ruigrok R.W., Daigle N., Ellenberg J., Cusack S., Simorre J.P., Hart D.J. Structure and nuclear import function of the C-terminal domain of influenza virus polymerase PB2 subunit. Nat. Struct. Mol. Biol. 2007, 14:229-233.
45. Fagerlund R., Kinnunen L., Kohler M., Julkunen I., Melen K. NF-{kappa}B is transported into the nucleus by importin {alpha}3 and importin {alpha}4. J. Biol. Chem. 2005, 280:15942-15951.
46. 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.
47. Malik H.S., Eickbush T.H., Goldfarb D.S. Evolutionary specialization of the nuclear targeting apparatus. Proc. Natl Acad. Sci. USA 1997, 94:13738-13742.
48. Andrade M.A., Petosa C., O'Donoghue S.I., Muller C.W., Bork P. Comparison of ARM and HEAT protein repeats. J. Mol. Biol. 2001, 309:1-18.
49. Conti E., Muller C.W., Stewart M. Karyopherin flexibility in nucleocytoplasmic transport. Curr. Opin. Struct. Biol. 2006, 16:237-244.
50. Stewart M. Molecular mechanism of the nuclear protein import cycle. Nat. Rev. Mol. Cell Biol. 2007, 8:195-208.
51. Chook Y.M., Blobel G. Karyopherins and nuclear import. Curr. Opin. Struct. Biol. 2001, 11:703-715.
52. Cook A., Bono F., Jinek M., Conti E. Structural biology of nucleocytoplasmic transport. Annu. Rev. Biochem. 2007, 76:647-671.
53. Mans B.J., Anantharaman V., Aravind L., Koonin E.V. Comparative genomics, evolution and origins of the nuclear envelope and nuclear pore complex. Cell Cycle 2004, 3:1612-1637.
54. Andrade M.A., Bork P. HEAT repeats in the Huntington's disease protein. Nat. Genet. 1995, 11:115-116.
55. Will C.L., Luhrmann R. Spliceosomal UsnRNP biogenesis, structure and function. Curr. Opin. Cell Biol. 2001, 13:290-301.
56. Dong X., Biswas A., Suel K.E., Jackson L.K., Martinez R., Gu H., Chook Y.M. Structural basis for leucine-rich nuclear export signal recognition by CRM1. Nature 2009, 458:1136-1141.
57. Wold M.S. Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem. 1997, 66:61-92.
58. Kobe B. Autoinhibition by an internal nuclear localization signal revealed by the crystal structure of mammalian importin alpha. Nat. Struct. Biol. 1999, 6:388-397.
59. Fanara P., Hodel M.R., Corbett A.H., Hodel A.E. Quantitative analysis of nuclear localization signal (NLS)-importin alpha interaction through fluorescence depolarization. Evidence for auto-inhibitory regulation of NLS binding. J. Biol. Chem. 2000, 275:21218-21223.
60. Conti E., Uy M., Leighton L., Blobel G., Kuriyan J. Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin alpha. Cell 1998, 94:193-204.
61. Conti E., Kuriyan J. Crystallographic analysis of the specific yet versatile recognition of distinct nuclear localization signals by karyopherin alpha. Structure 2000, 8:329-338.
62. Fontes M.R., Teh T., Kobe B. Structural basis of recognition of monopartite and bipartite nuclear localization sequences by mammalian importin-alpha. J. Mol. Biol. 2000, 297:1183-1194.
63. Fontes M.R., Teh T., Jans D., Brinkworth R.I., Kobe B. Structural basis for the specificity of bipartite nuclear localization sequence binding by importin-alpha. J. Biol. Chem. 2003, 278:27981-27987.
64. Chen M.H., Ben-Efraim I., Mitrousis G., Walker-Kopp N., Sims P.J., Cingolani G. Phospholipid scramblase 1 contains a nonclassical nuclear localization signal with unique binding site in importin alpha. J. Biol. Chem. 2005, 280:10599-10606.
65. S.N. Yang, A.A. Takeda, M.R. Fontes, J.M. Harris, D.A. Jans, B. Kobe, Probing the specificity of binding to the major nuclear localization sequence-binding site of importin-alpha using oriented peptide library screening, J Biol Chem.
66. Hodel M.R., Corbett A.H., Hodel A.E. Dissection of a nuclear localization signal. J. Biol. Chem. 2001, 276:1317-1325.
67. Harreman M.T., Cohen P.E., Hodel M.R., Truscott G.J., Corbett A.H., Hodel A.E. Characterization of the auto-inhibitory sequence within the N-terminal domain of importin alpha. J. Biol. Chem. 2003, 278:21361-21369.
68. Harreman M.T., Hodel M.R., Fanara P., Hodel A.E., Corbett A.H. The auto-inhibitory function of importin alpha is essential in vivo. J. Biol. Chem. 2003, 278:5854-5863.
69. Catimel B., Teh T., Fontes M.R., Jennings I.G., Jans D.A., Howlett G.J., Nice E.C., Kobe B. Biophysical characterization of interactions involving importin-alpha during nuclear import. J. Biol. Chem. 2001, 276:34189-34198.
70. Nardozzi J., Wenta N., Noriko Y., Vinkemeier W., Cingolani G. Molecular basis for the recognition of phosphorylated STAT1 by importin a5. J. Mol. Biol. 2010.
71. Strasser A., Dickmanns A., Luhrmann R., Ficner R. Structural basis for m3G-cap-mediated nuclear import of spliceosomal UsnRNPs by snurportin1. EMBO J. 2005, 24:2235-2243.
72. Fukuhara N., Fernandez E., Ebert J., Conti E., Svergun D. Conformational variability of nucleo-cytoplasmic transport factors. J. Biol. Chem. 2004, 279:2176-2181.
73. Zachariae U., Grubmuller H. Importin-beta: structural and dynamic determinants of a molecular spring. Structure 2008, 16:906-915.
74. Cingolani G., Lashuel H.A., Gerace L., Muller C.W. Nuclear import factors importin alpha and importin beta undergo mutually induced conformational changes upon association. FEBS Lett. 2000, 484:291-298.
75. Bhardwaj A., Cingolani G. Conformational Selection in the Recognition of Snurportin IBB-domain by Importin beta. Biochemistry 2010.
76. Jakel S., Mingot J.M., Schwarzmaier P., Hartmann E., Gorlich D. Importins fulfil a dual function as nuclear import receptors and cytoplasmic chaperones for exposed basic domains. EMBO J. 2002, 21:377-386.
77. Wohlwend D., Strasser A., Dickmanns A., Ficner R. Structural basis for RanGTP independent entry of spliceosomal U snRNPs into the nucleus. J. Mol. Biol. 2007, 374:1129-1138.
78. Matsuura Y., Stewart M. Structural basis for the assembly of a nuclear export complex. Nature 2004, 432:872-877.
79. Boehr D.D., Nussinov R., Wright P.E. The role of dynamic conformational ensembles in biomolecular recognition. Nat. Chem. Biol. 2009, 5:789-796.
80. Nevo R., Stroh C., Kienberger F., Kaftan D., Brumfeld V., Elbaum M., Reich Z., Hinterdorfer P. A molecular switch between alternative conformational states in the complex of Ran and importin beta1. Nat. Struct. Biol. 2003, 10:553-557.
81. Zachariae U., Grubmuller H. A highly strained nuclear conformation of the exportin Cse1p revealed by molecular dynamics simulations. Structure 2006, 14:1469-1478.
82. Boehr D.D., McElheny D., Dyson H.J., Wright P.E. The dynamic energy landscape of dihydrofolate reductase catalysis. Science 2006, 313:1638-1642.
83. Yang W., Musser S.M. Nuclear import time and transport efficiency depend on importin beta concentration. J. Cell Biol. 2006, 174:951-961.
84. Lyman S.K., Guan T., Bednenko J., Wodrich H., Gerace L. Influence of cargo size on Ran and energy requirements for nuclear protein import. J. Cell Biol. 2002, 159:55-67.
85. K. Lott, A. Bhardwaj, G. Mitrousis, N. Pante, G. Cingolani, The importin beta binding domain modulates the avidity of importin beta for the nuclear pore complex. J Biol Chem 285; 13769-13780.
86. Moore M.S., Blobel G. The GTP-binding protein Ran/TC4 is required for protein import into the nucleus. Nature 1993, 365:661-663.
87. Weis K., Dingwall C., Lamond A.I. Characterization of the nuclear protein import mechanism using Ran mutants with altered nucleotide binding specificities. EMBO J. 1996, 15:7120-7128.
88. Melchior F., Paschal B., 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.
89. Cassany A., Gerace L. Reconstitution of nuclear import in permeabilized cells. Meth. Mol. Biol. 2009, 464:181-205.
90. Huber J., Dickmanns A., Luhrmann R. The importin-beta binding domain of snurportin1 is responsible for the Ran- and energy-independent nuclear import of spliceosomal U snRNPs in vitro. J. Cell Biol. 2002, 156:467-479.
91. Rollenhagen C., Muhlhausser P., Kutay U., Pante N. Importin beta-depending nuclear import pathways: role of the adapter proteins in the docking and releasing steps. Mol. Biol. Cell 2003, 14:2104-2115.
92. Rexach M., Blobel G. Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell 1995, 83:683-692.
93. Lee S.J., Matsuura Y., Liu S.M., Stewart M. Structural basis for nuclear import complex dissociation by RanGTP. Nature 2005, 435:693-696.
94. Gorlich 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.
95. Matsuura Y., Stewart M. Nup50/Npap60 function in nuclear protein import complex disassembly and importin recycling. EMBO J. 2005, 24:3681-3689.
96. Guan T., Kehlenbach R.H., Schirmer E.C., Kehlenbach A., Fan F., Clurman B.E., Arnheim N., Gerace L. Nup50, a nucleoplasmically oriented nucleoporin with a role in nuclear protein export. Mol. Cell. Biol. 2000, 20:5619-5630.
97. Gilchrist D., Mykytka B., Rexach M. Accelerating the rate of disassembly of karyopherin.cargo complexes. J. Biol. Chem. 2002, 277:18161-18172.
98. Lindsay M.E., Plafker K., Smith A.E., Clurman B.E., Macara I.G. Npap60/Nup50 is a tri-stable switch that stimulates importin-alpha:beta-mediated nuclear protein import. Cell 2002, 110:349-360.
99. 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.
100. Kutay U., Bischoff F.R., Kostka S., Kraft R., Gorlich D. Export of importin alpha from the nucleus is mediated by a specific nuclear transport factor. Cell 1997, 90:1061-1071.
101. Hood J.K., Silver P.A. Cse1p is required for export of Srp1p/importin-alpha from the nucleus in Saccharomyces cerevisiae. J. Biol. Chem. 1998, 273:35142-35146.
102. Solsbacher J., Maurer P., Bischoff F.R., Schlenstedt G. Cse1p is involved in export of yeast importin alpha from the nucleus. Mol. Cell. Biol. 1998, 18:6805-6815.
103. Paraskeva E., Izaurralde E., Bischoff F.R., Huber J., Kutay U., Hartmann E., Luhrmann R., Gorlich D. CRM1-mediated recycling of snurportin 1 to the cytoplasm. J. Cell Biol. 1999, 145:255-264.
104. Monecke T., Guttler T., Neumann P., Dickmanns A., Gorlich D., Ficner R. Crystal structure of the nuclear export receptor CRM1 in complex with Snurportin1 and RanGTP. Science 2009, 324:1087-1091.
105. Floer M., Blobel G., Rexach M. Disassembly of RanGTP-karyopherin beta complex, an intermediate in nuclear protein import. J. Biol. Chem. 1997, 272:19538-19546.
106. Matunis M.J., Coutavas E., Blobel G. A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J. Cell Biol. 1996, 135:1457-1470.
107. Mahajan R., Delphin C., Guan T., Gerace L., Melchior F. A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 1997, 88:97-107.
108. Pollard V.W., Malim M.H. The HIV-1 Rev protein. Annu. Rev. Microbiol. 1998, 52:491-532.
109. Truant R., Cullen B.R. The arginine-rich domains present in human immunodeficiency virus type 1 Tat and Rev function as direct importin beta-dependent nuclear localization signals. Mol. Cell. Biol. 1999, 19:1210-1217.
110. Arnold M., Nath A., Hauber J., Kehlenbach R.H. Multiple importins function as nuclear transport receptors for the Rev protein of human immunodeficiency virus type 1. J. Biol. Chem. 2006, 281:20883-20890.
111. Mertz J.A., Lozano M.M., Dudley J.P. Rev and Rex proteins of human complex retroviruses function with the MMTV Rem-responsive element. Retrovirology 2009, 6:10.
112. Henderson B.R., Percipalle P. Interactions between HIV Rev and nuclear import and export factors: the Rev nuclear localisation signal mediates specific binding to human importin-beta. J. Mol. Biol. 1997, 274:693-707.
113. 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. 1999, 19:1218-1225.
114. Dimattia M.A., Watts N.R., Stahl S.J., Rader C., Wingfield P.T., Stuart D.I., Steven A.C., Grimes J.M. Implications of the HIV-1 Rev dimer structure at 3.2 A resolution for multimeric binding to the Rev response element. Proc. Natl Acad. Sci. USA 2010, 107:5810-5814.
115. Timney B.L., Tetenbaum-Novatt J., Agate D.S., Williams R., Zhang W., Chait B.T., Rout M.P. Simple kinetic relationships and nonspecific competition govern nuclear import rates in vivo. J. Cell Biol. 2006, 175:579-593.
116. Moore J.D., Yang J., Truant R., Kornbluth S. Nuclear import of Cdk/cyclin complexes: identification of distinct mechanisms for import of Cdk2/cyclin E and Cdc2/cyclin B1. J. Cell Biol. 1999, 144:213-224.
117. Jakel S., Gorlich D. Importin beta, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J. 1998, 17:4491-4502.
118. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
119. Hu T., Guan T., Gerace L. Molecular and functional characterization of the p62 complex, an assembly of nuclear pore complex glycoproteins. J. Cell Biol. 1996, 134:589-601.