Mechanisms and signals for the nuclear import of proteins

Current Genomics

Volumn 10, Issue 8, 2009, Pages 550-557

  Freitas, Natália ^a   Cunha, Celso ^a  

^a INSTITUTO DE HIGIENE E MEDICINA TROPICAL   (Portugal)

Author keywords

Importin; Nuclear localization signal; Nuclear pore complex; Nuclear transport

Indexed keywords

GUANOSINE DIPHOSPHATE; HISTONE; KARYOPHERIN ALPHA; KARYOPHERIN BETA; RAN PROTEIN; REX PROTEIN; RIBOSOME PROTEIN; STAT1 PROTEIN; SURVIVAL MOTOR NEURON PROTEIN;

CELL COMPARTMENTALIZATION; COMPLEX FORMATION; GENE EXPRESSION REGULATION; HUMAN T CELL LEUKEMIA VIRUS 1; MOLECULAR MECHANICS; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR PORE; NUCLEAR PORE COMPLEX; NUCLEOCYTOPLASMIC TRANSPORT; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

EUKARYOTA;

EID: 73349140487     PISSN: 13892029     EISSN: None     Source Type: Journal    
DOI: 10.2174/138920209789503941     Document Type: Review

References (87)

1. 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.
2. Adam, S.A. The nuclear pore complex. Genome Biol., 2001, 2, 7.1-7.6
3. Suntharalingam, M.; Wente, S.R. Peering the pore: nuclear pore complex structure, assembly, and function. Develop. Cell, 2003, 4, 775-789.
4. Fahrenkrog, B.; Aebi, U. The nuclear pore complex: nucleocytoplasmic transport and beyond. Mol. Cell Biol., 2003, 4, 757-766.
5. Cronshaw, J.M.; Krutchinsky, A.N.; Zhang, W.; Chait, B.T.; Matutis, M.J. Proteomic analysis of the mammalian nuclear pore complex. J. Cell Biol., 2002, 158, 915-927.
6. 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.
7. Reichelt, R.; Holzenburg, A.; Buhle, Jr. 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.
8. Yang, Q.; Rout, M.P.; Akey, C.W. Three-dimensional architecture of the isolated yeast nuclear pore complex: functional and evolutionary implications. Mol. Cell, 1998, 1, 223-234.
9. Mosammaparast, N.; Pemberton, L.F. Karyopherins: from the nuclear-transport mediators to nuclear-function regulators. Trends Cell Biol., 2004, 14, 547-556.
10. Kohler, A.; Hurt, E. Exporting RNA from the nucleus to the cytoplasm. Mol. Cell Biol., 2007, 8, 761-773.
11. Chook, Y.M.; Blobel, G. Karyopherins and nuclear import. Cur. Opi. Stru. Biol., 2001, 11, 703-715.
12. Kalab, P.; Heald, R. The RanGTP gradient-a GPS for the mitotic spindle. J. Cell. Sci., 2008, 121, 1577-1586.
13. Gorlich, D.; Kutay, U. Transport between the cell nucleus and the cytoplasm. Ann. Rev. Cell Dev. Biol., 1999, 15, 607-660.
14. Madrid, A.S.; Weis, K. Nuclear transport is becoming crystal clear. Chromosoma, 2006, 115, 98-10.
15. Ribbeck, K.; Lipowsky, G.; Kent, H.M.; Stewart, M.; Gorlich, D. NTF2 mediates nuclear import of Ran. EMBO J., 1998, 17, 6587-6598.
16. Quimby, B.B.; Lamitina, T.; L'Hernault, S.W.; Corbett, A.H. The mechanism of Ran import into the nucleus by nuclear transport factor 2. J. Biol. Chem., 2000, 275, 28575-28582.
17. Weis, K. Regulating access to the genome: nucleocytoplasmic transport throughout the cell cycle. Cell, 2003, 112, 441-451.
18. Bednenko, J.; Cingolani, G.; Gerace, L. Nucleocytoplasmic transport: navigating the channel. Traffic, 2003, 4, 127-135.
19. Bednenko, J.; Cingolani, G.; Gerace, L. Importin contains a COOH-terminal nucleoporin binding region important for nuclear import. J. Cell Biol., 2003, 162, 391-401.
20. 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.
21. 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.
22. Ribbeck, K.; Gorlich, D. Kinetic analysis of translocation through nuclear pore complexes. Embo J., 2001, 20, 1320-1330.
23. Frey, S.; Richter, R.P.; Gorlich, D. FG-rich repeats of nuclear pore proteins form a three-dimensional meshwork with hydrogel-like properties. Science, 2006, 314, 815-817.
24. Ben-Efraim, I.; Gerace, L. Gradient of increasing affinity of importin β for nucleoporins along the pathway of nuclear import. J. Cell Biol., 2001, 152, 411-417.
25. Zeitler, B.; Weis, K. The FG-repeat asymmetry of the nuclear pore complex is dispensable for bulk nucleocytoplasmic transport in vivo. J. Cell Biol., 2004, 167, 583-590.
26. 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.
27. Dingwall, C.; Sharnick, S.V.; Laskey, R.A. A polypeptide domain that specifies migration of nucleoplasmin into the nucleus. Cell, 1982, 30, 449-458.
28. 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.
29. Dingwall, C.; Robbins, J.; Dilworth, S.M.; Roberts, B.; Richardson, W.D. The nucleoplasmin nuclear location sequence is larger and more complex than that of SV-40 large T antigen. J. Cell Biol., 1988, 107, 841-849.
30. 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.
31. 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-α. J. Biol. Chem., 2007, 282, 5101-5105.
32. Dang, C.V.; Lee, W.M. Identification of the human c-myc protein nuclear translocation signal. Mol. Cell. Biol., 1988, 8, 4048-4054.
33. Siomi, H.; Dreyfuss, G. A nuclear localization domain in the hnRNP A1 protein. J. Cell Biol., 1995, 129, 551-560.
34. Jakel, S.; Gorlich, D. Importinβ, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J., 1988, 17, 4491-4502.
35. Melén, K.; Kinnunen, L.; Julkunen, I. Arginine/lysine-rich structural element is involved in interferon-induced nuclear import of STATs. J. Biol. Chem., 2001, 276, 16447-1455.
36. Fagerlund, R.; Melén, K.; Kinnunen, L.; Julkunen, I. Arginine/ lysine-rich nuclear localization signals mediate interactions between dimeric STATs and importin α5. J. Biol. Chem., 2002, 277, 30072-30078.
37. Meyer, T.; Vinkemeier, U. Nucleocytoplasmic shuttling of STAT transcription factors. Eur. J. Biochem., 2004, 271, 4606-4612.
38. Vinkemeier, U. Getting the message across, STAT! Design principles of a molecular signaling circuit. J. Cell Biol., 2004, 167, 197-201.
39. Leslie, D.M.; Zhang, W.; Timney, B.L.; Chait, B.T.; Rout, M.P.; Wozniak, R.W.; Aitchison, J.D. Characterization of karyopherin cargoes reveals unique mechanisms of kap121-p mediated nuclear import. Mol. Cell. Biol., 2004, 24, 8487-8503.
40. Jans, D.A.; Briggs, L.J.; Gustin, S.E.; Jans, P.; Ford, S.; Young, I.G. The cytokine interleukin-5 (IL-5) effects cotransport of its receptor subunits to the nucleus in vitro. FEBS lett., 1997, 410, 368-372.
41. Shiota, C.; Coffey, J.; Grimsby, J.; Grippo, J.F.; Magnuson, M.A. Nuclear import of hepatic glucokinase depends upon glucokinase regulatory protein, whereas export is due to a nuclear export signal sequence in glucokinase. J. Biol. Chem., 1999, 274, 37125-37130.
42. Xia, Y.-P.; Yeh, C.-T.; Ou, J.-H.; Lai, M.M.C. Characterization of nuclear targeting signal of hepatitis delta antigen: nuclear transport as a protein complex. J. Virol., 1992, 66, 914-921.
43. Goldfarb, D.S.; Corbett, A. H.; Mason, D.A.; Harreman, M.T.; Adam, S.A. Importin α: a multipurpose nuclear-transport receptor. Trends Cell Biol., 2004, 14, 505-514.
44. 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.
45. Fontes, M.R.; The, 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.
46. Leung, S.W.; Harreman, M.T.; Hodel, M.R.; Hodel, A.E.; Corbett, A.H. Dissection of the karyopherin nuclear localization signal (NLS)-binding groove. Functional requirements for NLS binding. J. Biol. Chem., 2003, 278, 41947-41953.
47. Gorlich, D.; Henklein, P.; Laskey, R.A.; Hartmann, E. A 41 amino acid motif in importin-alpha confers binding to importin-beta and hence transit into the nucleus. EMBO J., 1996, 15, 1810-1817.
48. Weis, K.; Ryder, U.; Lamond, A.I. The conserved amino-terminal domain of hSRP1 is essential for nuclear protein import. EMBO J., 1996, 15, 1818-1825.
49. Moroianu, J.; Blobel, G.; Radu, A. The binding site of karyopherin α for karyopherin β overlaps with a nuclear localization sequence. Proc. Natl. Acad. Sci. USA, 1996, 93, 6572-6576.
50. Stewart M. Molecular mechanism of the nuclear protein import cycle. Mol. Cell. Biol., 2007, 8, 195-208.
51. Lee, S.J.; Matsuura, Y.; Liu, S.M.; Stewart, M. Structural basis for nuclear import complex dissociation by RanGTP. Nature, 2005, 435, 693-696.
52. Gilchrist, D.; Mykytka, B.; Rexach, M. Accelerating the rate of disassembly of karyopherin-cargo complexes. J. Biol. Chem., 2002, 277, 18161-18172.
53. Kutay, U.; Bischoff, F.R.; Kostka, S.; Kraft, R.; Gorlich, D. Export of importin α from the nucleus is mediated by a specific nuclear transport factor. Cell, 1997, 90, 1061-1071.
54. Matsuura, Y.; Stewart, M. Nup50/Npap60 function in nuclear protein import complex disassembly and importin recycling. EMBO J., 2005, 24, 3681-3689.
55. Matsuura, Y.; Lange, A.; Harreman, M.T.; Corbett, A.H.; Stewart, M. Structural basis for Nup2p function in cargo release and karyopherin recycling in nuclear import. EMBO J., 2003, 22, 5358-5369.
56. Quensel, C.; Friedrich, B.; Sommer, T.; Hartmann, E.; Kohler, M. In vivo analysis of importin α proteins reveals cellular proliferation inhibition and substrate specificity. Mol. Cell. Biol., 2004, 24, 10246-10255.
57. Kohler, M.; Ansieau, S.; Prehn, S.; Leutz, A.; Haller, H.; Hartmann, E. Cloning of two novel human importin-α subunits and analysis of the expression pattern of the importin-α protein family. FEBS lett., 1997, 417, 104-108.
58. Kohler, M.; Speck, C.; Christiansen, M.; Bischoff, F.R.; Prehn, S.; Haller, H.; Gorlich, D.; Hartmann, E. Evidence for distinct substrate specificities of importin α family members in nuclear protein import. Mol. Cell. Biol., 1999, 19, 7782-7791.
59. Kamei, Y.; Yuba, S.; Nakayama, T.; Yoneda, Y. Three distinct classes of the α-subunit of the nuclear pore-targeting complex (importin-α ) are differentially expressed in adult mouse tissues. J. Histochem. Cytochem., 1999, 47, 363-372.
60. Miyamoto, Y.; Imamoto, N.; Sekimoto, T.; Tachibana, T.; Seki, T.; Tada, S.; Enomoto, T.; Yoneda, Y. Differential modes of nuclear localization signal (NLS) recognition by three distinct classes of NLS receptors. J. Biol. Chem., 1997, 272, 26375-26381.
61. Talcott, B.; Moore, M.S. The nuclear import of RCC1 requires a specific nuclear localization sequence receptor, karyopherin α3/Qip. J. Biol. Chem., 2000, 275, 10099-10104.
62. Friedrich, B.; Quensel, C.; Sommer, T.; Hartmann, E.; Kohler, M. Nuclear localization signal and protein context both mediate importin α specificity of nuclear import substrates. Mol. Cell. Biol., 2006, 26, 8697-8709.
63. Palacios, I.; Hetzer, M.; Adam, S.A.; Mattaj, I.W. Nuclear import of U snRNPs requires importin β. EMBO J., 1997, 16, 6783-6792.
64. Jullien, D.; Gorlich, D.; Laemmli, U.K.; Adachi, Y. Nuclear import of RPA in Xenopus egg extracts requires a novel protein XRIPα but not importin α. EMBO J., 1999, 18, 4348-4358.
65. 3G cap. EMBO J., 1993, 12, 573-583.
66. 3G-cap-specific nuclear import receptor with a novel domain structure. EMBO J., 1998, 17, 4114-4126.
67. Huber, J.; Dickmanns, A.; Luhrmann, R. The importin-β binding domain of snurportin1 is responsible for the Ran- and energy-independent nuclear import of spliceosomal U snRNP in vitro. J. Cell Biol., 2002, 156, 467-479.
68. Mitrousis, G.; Olia, A.S.; Walker-Kopp, N.; Cingolani, G. Molecular basis for the recognition of snurportin 1 by importin-β. J. Biol. Chem., 2008, 283, 7877-7884.
69. Walther, T.C.; Fornerod, M.; Pickersgill, H.; Goldberg, M.; Allen, T.D.; Mattaj, I.W. The nucleoporin Nup153 is required for nuclear pore basket formation, nuclear pore complex anchoring and import of a subset of nuclear proteins. EMBO J., 2001, 20, 5703-5714.
70. Narayanan, U.; Ospina, J.K.; Frey, M.R.; Hebert, M.D.; Matera, A.G. SMN, the spinal muscular atrophy protein, forms a pre-import snRNP complex with snurportin1 and importin β. Hum. Mol. Genet., 2002, 11, 1785-1795.
71. Massenet, S.; Pellizzoni, L.; Paushkin, S.; Mattaj, I.W.; Dreyfuss, G. The SMN complex is associated with snRNPs throughout their cytoplasmic assembly pathway. Mol. Cell. Biol., 2002, 22, 6533-6541.
72. Narayanan, U.; Achsel, T.; Luhrmann, R.; Matera, A.G. Coupled in vitro import of U snRNPs and SMN, the spinal muscular atrophy protein. Mol. Cell, 2004, 16, 223-234.
73. Palmeri, D.; Malim, M.H. Importin β can mediate the nuclear import of an arginine-rich nuclear localization signal in the absence of importin α. Mol. Cell. Biol., 1999, 19, 1218-1225.
74. Muhlhausser, P.; Muller, E.-C.; Otto, A.; Kutay, U. Multiple pathways contribute to nuclear import of core histones. EMBO Reports, 2001, 2, 690-696.
75. 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 β2. Cell, 2006, 126, 543-558.
76. Alves, C.; Freitas, N.; Cunha, C. Characterization of the nuclear localization signal of the hepatitis delta virus antigen. Virology, 2008, 370, 12-21.
77. Richardson, W.D.; Roberts, B.L.; Smith, A.E. Nuclear location signals in polyoma virus large-T. Cell, 1986, 44, 77-85.
78. Shaulsky, G.; Goldfinger, N.; Ben-Ze'ev, A.; Rotter, V. Nuclear accumulation of p53 protein is mediated by several nuclear localization signals and plays a role in tumorigenesis. Mol. Cell Biol., 1990, 10, 6565-6577.
79. Henkel, T.; Zabel, U.; Zee, K.V.; Müller, J.M.; Fanning, E.; Baeuerle, P.A. Intramolecular masking of the nuclear location signal and dimerization domain in the precursor for the p50 NF-κB subunit. Cell, 1992, 68, 1121-1133.
80. Zabel, U.; Henkel, T; Silva, M.S.; Baeuerle, P.A. Nuclear uptake control of NF-kappa B by MAD-3, and I kappa B protein present in the nucleus. EMBO J., 1993, 12, 201-211.
81. Picard, D.; Yamamoto, K.R. Two signals mediate hormonedependent nuclear localization of the glucocorticoid receptor. EMBO J., 1987, 6, 3333-3340.
82. Nemergut, M.E.; Macara, I.G. Nuclear import of the Ran exchange factor, Rcc1, is mediated by at least two distinct mechanisms. J. Cell Biol., 2000, 149, 835-850.
83. Ou, J.-H.; Yeh, C.-T.; Yen, T.B. Transport of hepatitis B virus precore protein into the nucleus after cleavage of its signal peptide. J. Virol., 1989, 63, 5238-5243.
84. Truant, R.; Cullen, B.R. The arginine-rich domains present in human immunodeficiency vírus type 1 Tat and Rev function as direct importin β-dependent nuclear localization signals. Mol. Cell. Biol., 1999, 19, 1210-1217.
85. Hall, M. L.; Hereford, L.; Herskowitz, I. Targeting of E. coli β-galactosidase to the nucleus in yeast. Cell, 1984, 36, 1057-1065.
86. Nagoshi, E.; Yoneda, Y. Dimerization of sterol regulatory elementbinding protein 2 via the helix-loop-helix-leucine zipper domain is a prerequisite for its nuclear localization mediated by importin β. Mol. Cell. Biol., 2001, 21, 2779-2789.
87. Siomi, H.; Dreyfuss, G. A nuclear localization domain in the hnRNP A1 protein. J. Cell Biol., 1995, 129, 551-560.