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Physiol. Rev. 76: 651-685, 1996;
0031-9333/96 $15.00
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Physiological Reviews, Vol 76, 651-685, Copyright © 1996 by American Physiological Society

JOURNAL ARTICLE

Regulation of protein transport to the nucleus: central role of phosphorylation

D. A. Jans and S. Hubner
Nuclear Signalling Laboratory, Division for Biochemistry and Molecular Biology, John Curtin School of Medical Research, Australian National University, Canberra, Australia.

Nuclear protein transport is integral to eukaryotic cell processes such as differentiation, transformation, and the control of gene expression. Although the targeting role of nuclear localization signals (NLSs) has been known for some time, more recent results indicate that NLS-dependent nuclear protein import is precisely regulated. Phosphorylation appears to be the main mechanism controlling the nuclear transport of a number of proteins, including transcription factors such as NFkappaB, c-rel, dorsal, and SWI5 from yeast. Cytoplasmic retention factors, intra- and intermolecular NLS masking, and NLS masking by phosphorylation are some of the mechanisms by which phosphorylation specifically regulates nuclear transport. Even nuclear localization of the archetypal NLS-containing simian virus 40 large tumor antigen (T-ag) is regulated, namely by the "CcN motif," which comprises the T-ag NLS ("N") determining ultimate subcellular destination, a casein kinase II site ("C") 13 amino acids NH2-terminal to the NLS modulating the rate of nuclear import, and a cyclin-dependent kinase site ("c") adjacent to the NLS regulating the maximal level of nuclear accumulation. The CcN motif appears to be a special form of phosphorylation-regulated NLS (prNLS), where phosphorylation at site(s) close to the NLS specifically regulates NLS function. The regulation of nuclear transport through phosphorylation and prNLSs appears to be common in eukaryotic cells from yeast and plants to higher mammals.


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Senescence represses the nuclear localization of the serum response factor and differentiation regulates its nuclear localization with lineage specificity
J. Cell Sci., January 3, 2001; 114(5): 1011 - 1018.
[Abstract] [PDF]

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 JCBHome page
D. Lechardeur, L. Drzymala, M. Sharma, D. Zylka, R. Kinach, J. Pacia, C. Hicks, N. Usmani, J. M. Rommens, and G. L. Lukacs
Determinants of the Nuclear Localization of the Heterodimeric DNA Fragmentation Factor (Icad/Cad)
J. Cell Biol., July 24, 2000; 150(2): 321 - 334.
[Abstract] [Full Text] [PDF]

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 J. Virol.Home page
Y. Zhou and L. Ratner
Phosphorylation of Human Immunodeficiency Virus Type 1 Vpr Regulates Cell Cycle Arrest
J. Virol., July 15, 2000; 74(14): 6520 - 6527.
[Abstract] [Full Text]

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 Mol. Biol. CellHome page
T. Sekito, J. Thornton, and R. A. Butow
Mitochondria-to-Nuclear Signaling Is Regulated by the Subcellular Localization of the Transcription Factors Rtg1p and Rtg3p
Mol. Biol. Cell, June 1, 2000; 11(6): 2103 - 2115.
[Abstract] [Full Text]

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N. Zou, B. Y. Lin, F. Duan, K.-Y. Lee, G. Jin, R. Guan, G. Yao, E. J. Lefkowitz, T. R. Broker, and L. T. Chow
The Hinge of the Human Papillomavirus Type 11 E2 Protein Contains Major Determinants for Nuclear Localization and Nuclear Matrix Association
J. Virol., April 15, 2000; 74(8): 3761 - 3770.
[Abstract] [Full Text]

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 J. Virol.Home page
E. Lombardo, J. C. Ramírez, M. Agbandje-McKenna, and J. M. Almendral
A Beta-Stranded Motif Drives Capsid Protein Oligomers of the Parvovirus Minute Virus of Mice into the Nucleus for Viral Assembly
J. Virol., April 15, 2000; 74(8): 3804 - 3814.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
I. V. Smirnova, D. C. Bittel, R. Ravindra, H. Jiang, and G. K. Andrews
Zinc and Cadmium Can Promote Rapid Nuclear Translocation of Metal Response Element-binding Transcription Factor-1
J. Biol. Chem., March 24, 2000; 275(13): 9377 - 9384.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M.-C. Lai, R.-I. Lin, S.-Y. Huang, C.-W. Tsai, and W.-Y. Tarn
A Human Importin-beta Family Protein, Transportin-SR2, Interacts with the Phosphorylated RS Domain of SR Proteins
J. Biol. Chem., March 10, 2000; 275(11): 7950 - 7957.
[Abstract] [Full Text] [PDF]

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 J. Virol.Home page
P. R. Kinchington, K. Fite, and S. E. Turse
Nuclear Accumulation of IE62, the Varicella-Zoster Virus (VZV) Major Transcriptional Regulatory Protein, Is Inhibited by Phosphorylation Mediated by the VZV Open Reading Frame 66 Protein Kinase
J. Virol., March 1, 2000; 74(5): 2265 - 2277.
[Abstract] [Full Text]

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 Nucleic Acids ResHome page
T. K. Albert, M. Lemaire, N. L. van Berkum, R. Gentz, M. A. Collart, and H. Th. M. Timmers
Isolation and characterization of human orthologs of yeast CCR4-NOT complex subunits
Nucleic Acids Res., February 1, 2000; 28(3): 809 - 817.
[Abstract] [Full Text] [PDF]

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 JCBHome page
M. P. Czubryt, J. A. Austria, and G. N. Pierce
Hydrogen Peroxide Inhibition of Nuclear Protein Import Is Mediated by the Mitogen-Activated Protein Kinase, Erk2
J. Cell Biol., January 10, 2000; 148(1): 7 - 16.
[Abstract] [Full Text] [PDF]

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 J. Gen. Virol.Home page
R. Bullido, P. Gómez-Puertas, C. Albo, and A. Portela
Several protein regions contribute to determine the nuclear and cytoplasmic localization of the influenza A virus nucleoprotein
J. Gen. Virol., January 1, 2000; 81(1): 135 - 142.
[Abstract] [Full Text]

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 EndocrinologyHome page
T. N. Alliston, I. J. Gonzalez-Robayna, P. Buse, G. L. Firestone, and J. S. Richards
Expression and Localization of Serum/Glucocorticoid-Induced Kinase in the Rat Ovary: Relation to Follicular Growth and Differentiation
Endocrinology, January 1, 2000; 141(1): 385 - 395.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
B. B. Singh, H. H. Patel, R. Roepman, D. Schick, and P. A. Ferreira
The Zinc Finger Cluster Domain of RanBP2 Is a Specific Docking Site for the Nuclear Export Factor, Exportin-1
J. Biol. Chem., December 24, 1999; 274(52): 37370 - 37378.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
K. Welch, J. Franke, M. Kohler, and I. G. Macara
RanBP3 Contains an Unusual Nuclear Localization Signal That Is Imported Preferentially by Importin-alpha 3
Mol. Cell. Biol., December 1, 1999; 19(12): 8400 - 8411.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. L. Kingsley-Kallesen, D. Kelly, and A. Rizzino
Transcriptional Regulation of the Transforming Growth Factor-beta 2 Promoter by cAMP-responsive Element-binding Protein (CREB) and Activating Transcription Factor-1 (ATF-1) Is Modulated by Protein Kinases and the Coactivators p300 and CREB-binding Protein
J. Biol. Chem., November 26, 1999; 274(48): 34020 - 34028.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
T. G. Canty Jr, E. M. Boyle Jr, A. Farr, E. N. Morgan, E. D. Verrier, and T. H. Pohlman
Oxidative Stress Induces NF-{kappa}B Nuclear Translocation Without Degradation of I{kappa}B{alpha}
Circulation, November 9, 1999; 100 (2009): II-361 - II-364.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. M. Healy, M. Peters-Golden, J. P. Yao, and T. G. Brock
Identification of a Bipartite Nuclear Localization Sequence Necessary for Nuclear Import of 5-Lipoxygenase
J. Biol. Chem., October 15, 1999; 274(42): 29812 - 29818.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
F. Wellmer, S. Kircher, A. Rugner, H. Frohnmeyer, E. Schafer, and K. Harter
Phosphorylation of the Parsley bZIP Transcription Factor CPRF2 Is Regulated by Light
J. Biol. Chem., October 8, 1999; 274(41): 29476 - 29482.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. Hubner, H. M. S. Smith, W. Hu, C. K. Chan, H.-P. Rihs, B. M. Paschal, N. V. Raikhel, and D. A. Jans
Plant Importin alpha Binds Nuclear Localization Sequences with High Affinity and Can Mediate Nuclear Import Independent of Importin beta
J. Biol. Chem., August 6, 1999; 274(32): 22610 - 22617.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
I. J. Gonzalez-Robayna, T. N. Alliston, P. Buse, G. L. Firestone, and J. S. Richards
Functional and Subcellular Changes in the A-Kinase-Signaling Pathway: Relation to Aromatase and Sgk Expression during the Transition of Granulosa Cells to Luteal Cells
Mol. Endocrinol., August 1, 1999; 13(8): 1318 - 1337.
[Abstract] [Full Text]

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 Cancer Res.Home page
W. Ding, M. M. Witte, and R. E. Scott
Transformation Blocks Differentiation-induced Inhibition of Serum Response Factor Interactions with Serum Response Elements
Cancer Res., August 1, 1999; 59(15): 3795 - 3802.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
K. L. Loveland, D. Herszfeld, B. Chu, E. Rames, E. Christy, L. J. Briggs, R. Shakri, D. M. de Kretser, and D. A. Jans
Novel Low Molecular Weight Microtubule-associated Protein-2 Isoforms Contain a Functional Nuclear Localization Sequence
J. Biol. Chem., July 2, 1999; 274(27): 19261 - 19268.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
V. Lang, M. Semichon, F. Michel, C. Brossard, H. Gary-Gouy, and G. Bismuth
Fyn Membrane Localization Is Necessary to Induce the Constitutive Tyrosine Phosphorylation of Sam68 in the Nucleus of T Lymphocytes
J. Immunol., June 15, 1999; 162(12): 7224 - 7232.
[Abstract] [Full Text] [PDF]

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 J. Virol.Home page
J.-L. Liu, Y. Ye, Z. Qian, Y. Qian, D. J. Templeton, L. F. Lee, and H.-J. Kung
Functional Interactions between Herpesvirus Oncoprotein MEQ and Cell Cycle Regulator CDK2
J. Virol., May 1, 1999; 73(5): 4208 - 4219.
[Abstract] [Full Text]

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 Plant Physiol.Home page
S. E. Perry, M. D. Lehti, and D. E. Fernandez
The MADS-Domain Protein AGAMOUS-Like 15 Accumulates in Embryonic Tissues with Diverse Origins
Plant Physiology, May 1, 1999; 120(1): 121 - 130.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
K. Okamoto, H. Tanaka, H. Ogawa, Y. Makino, H. Eguchi, S.-i. Hayashi, N. Yoshikawa, L. Poellinger, K. Umesono, and I. Makino
Redox-dependent Regulation of Nuclear Import of the Glucocorticoid Receptor
J. Biol. Chem., April 9, 1999; 274(15): 10363 - 10371.
[Abstract] [Full Text] [PDF]

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 JCBHome page
M. Kann, B. Sodeik, A. Vlachou, W. H. Gerlich, and A. Helenius
Phosphorylation-dependent Binding of Hepatitis B Virus Core Particles to the Nuclear Pore Complex
J. Cell Biol., April 5, 1999; 145(1): 45 - 55.
[Abstract] [Full Text] [PDF]

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 Genes Dev.Home page
A. Stathopoulos-Gerontides, J. J. Guo, and M. S. Cyert
Yeast calcineurin regulates nuclear localization of the Crz1p transcription factor through dephosphorylation
Genes & Dev., April 1, 1999; 13(7): 798 - 803.
[Abstract] [Full Text]

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 Plant Physiol.Home page
H. M.S. Smith and N. V. Raikhel
Protein Targeting to the Nuclear Pore. What Can We Learn from Plants?
Plant Physiology, April 1, 1999; 119(4): 1157 - 1164.
[Full Text]

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 Plant CellHome page
N. Ohad, R. Yadegari, L. Margossian, M. Hannon, D. Michaeli, J. J. Harada, R. B. Goldberg, and R. L. Fischer
Mutations in FIE, a WD Polycomb Group Gene, Allow Endosperm Development without Fertilization
PLANT CELL, March 1, 1999; 11(3): 407 - 416.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. Herrington, L. Rui, G. Luo, L.-y. Yu-Lee, and C. Carter-Su
A Functional DNA Binding Domain Is Required for Growth Hormone-induced Nuclear Accumulation of Stat5B
J. Biol. Chem., February 19, 1999; 274(8): 5138 - 5145.
[Abstract] [Full Text] [PDF]

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 Cell Growth Differ.Home page
I. Ben-Dor, O. Bern, and T. Tennenbaum
Cell Cycle-dependent Nuclear Accumulation of the p94fer Tyrosine Kinase Is Regulated by Its NH2 Terminus and Is Affected by Kinase Domain Integrity and ATP Binding
Cell Growth Differ., February 1, 1999; 10(2): 113 - 129.
[Abstract] [Full Text]


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