Stimulated nuclear import by β-like importins

F1000Prime Reports

Volumn 5, Issue , 2013, Pages

  Flores, Karen ^a   Seger, Rony ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LIKE IMPORTIN; EXPORTIN 4; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMPORTIN 11; IMPORTIN 13; IMPORTIN 2; IMPORTIN 3; IMPORTIN 4; IMPORTIN 5; IMPORTIN 6; IMPORTIN 7; IMPORTIN 8; IMPORTIN 9; KARYOPHERIN; KARYOPHERIN ALPHA; KARYOPHERIN BETA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 7; NUCLEAR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL STIMULATION; CELLULAR DISTRIBUTION; CONFORMATIONAL TRANSITION; DROSOPHILA; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; INTRACELLULAR SIGNALING; NONHUMAN; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; PROTEIN LOCALIZATION;

EID: 84885579408     PISSN: None     EISSN: 20517599     Source Type: Journal    
DOI: 10.12703/P5-41     Document Type: Article

References (99)

1. Marfori M, Mynott A, Ellis JJ, Mehdi AM, Saunders NFW, Curmi PM, Forwood JK, Bodén M, Kobe B: Molecular basis for specificity of nuclear import and prediction of nuclear localization. Biochim Biophys Acta 2011, 1813:1562-77.
2. Frankel MB, Knoll LJ: The ins and outs of nuclear trafficking: unusual aspects in apicomplexan parasites. DNA Cell Biol 2009, 28:277-84.
3. Riddick G, Macara IG: A systems analysis of importin-{alpha}-{beta} mediated nuclear protein import. J Cell Biol 2005, 168:1027-38.
4. Chook YM, Süel KE: Nuclear import by karyopherin-bs: recognition and inhibition. Biochim Biophys Acta 2011, 1813: 1593-606.
5. Moroianu J, Blobel G, Radu A: Nuclear protein import: Ran-GTP dissociates the karyopherin alphabeta heterodimer by displacing alpha from an overlapping binding site on beta. Proc Natl Acad Sci U S A 1996, 93:7059-62.
6. Stewart M: Molecular mechanism of the nuclear protein import cycle. Nat Rev Mol Cell Biol 2007, 8:195-208.
7. Magnani M, Crinelli R, Bianchi M, Antonelli A: The ubiquitindependent proteolytic system and other potential targets for the modulation of nuclear factor-kB (NF-kB). Curr Drug Targets 2000, 1:387-99.
8. Kondoh K, Terasawa K, Morimoto H, Nishida E: Regulation of nuclear translocation of extracellular signal-regulated kinase 5 by active nuclear import and export mechanisms. Mol Cell Biol 2006, 26:1679-90.
9. Plotnikov A, Zehorai E, Procaccia S, Seger R: The MAPK cascades: signaling components, nuclear roles and mechanisms of nuclear translocation. Biochim Biophys Acta 2011, 1813:1619-33.
10. Nardozzi JD, Lott K, Cingolani G: Phosphorylation meets nuclear import: a review. Cell Commun Signal 2010, 8:32.
11. Xu D, Farmer A, Chook YM: Recognition of nuclear targeting signals by Karyopherin-b proteins. Curr Opin Struct Biol 2010, 20:782-90.
12. Ström AC, Weis K: Importin-beta-like nuclear transport receptors. Genome Biol 2001, 2:REVIEWS3008.
13. Yoon S, Seger R: The extracellular signal-regulated kinase: multiple substrates regulate diverse cellular functions. Growth Factors 2006, 24:21-44. (Pubitemid 43108774)
14. Carlson SM, Chouinard CR, Labadorf A, Lam CJ, Schmelzle K, Fraenkel E, White FM: Large-scale discovery of ERK2 substrates identifies ERK-mediated transcriptional regulation by ETV3. Sci Signal 2011, 4:rs11.
15. Kosako H, Yamaguchi N, Aranami C, Ushiyama M, Kose S, Imamoto N, Taniguchi H, Nishida E, Hattori S: Phosphoproteomics reveals new ERK MAP kinase targets and links ERK to nucleoporin-mediated nuclear transport. Nat Struct Mol Biol 2009, 16:1026-35.
16. Shaul YD, Seger R: The MEK/ERK cascade: from signaling specificity to diverse functions. Biochim Biophys Acta 2007, 1773:1213-26. (Pubitemid 47125968)
17. Raman M, Chen W, Cobb MH: Differential regulation and properties of MAPKs. Oncogene 2007, 26:3100-12. (Pubitemid 46763006)
18. Pimienta G, Pascual J: Canonical and alternative MAPK signaling. Cell Cycle 2007, 6:2628-32. (Pubitemid 350224045)
19. Zehorai E, Yao Z, Plotnikov A, Seger R: The subcellular localization of MEK and ERK-a novel nuclear translocation signal (NTS) paves a way to the nucleus. Mol Cell Endocrinol 2010, 314:213-20.
20. Wortzel I, Seger R: The ERK Cascade: Distinct Functions within Various Subcellular Organelles. Genes Cancer 2011, 2:195-209.
21. Harding A, Tian T, Westbury E, Frische E, Hancock JF: Subcellular localization determines MAP kinase signal output. Curr Biol 2005, 15:869-73. (Pubitemid 40689407)
22. Formstecher E, Ramos JW, Fauquet M, Calderwood DA, Hsieh JC, Canton B, Nguyen XT, Barnier JV, Camonis J, Ginsberg MH, Chneiweiss H: PEA-15 mediates cytoplasmic sequestration of ERK MAP kinase. Dev Cell 2001, 1:239-50. (Pubitemid 33653059)
23. Yao Z, Flash I, Raviv Z, Yung Y, Asscher Y, Pleban S, Seger R: Nonregulated and stimulated mechanisms cooperate in the nuclear accumulation of MEK1. Oncogene 2001, 20:7588-96. (Pubitemid 33111859)
24. Casar B, Pinto A, Crespo P: ERK dimers and scaffold proteins: unexpected partners for a forgotten (cytoplasmic) task. Cell Cycle 2009, 8:1007-13.
25. Reszka AA, Seger R, Diltz CD, Krebs EG, Fischer EH: Association of mitogen-activated protein kinase with the microtubule cytoskeleton. Proc Natl Acad Sci U S A 1995, 92:8881-5.
26. Rubinfeld H, Hanoch T, Seger R: Identification of a cytoplasmicretention sequence in ERK2. J Biol Chem 1999, 274:30349-52.
27. Zúñiga A, Torres J, Ubeda J, Pulido R: Interaction of mitogenactivated protein kinases with the kinase interaction motif of the tyrosine phosphatase PTP-SL provides substrate specificity and retains ERK2 in the cytoplasm. J Biol Chem 1999, 274:21900-7.
28. Chuderland D, Seger R: Protein-protein interactions in the regulation of the extracellular signal-regulated kinase. Mol Biotechnol 2005, 29:57-74. (Pubitemid 41411094)
29. Chuderland D, Konson A, Seger R: Identification and characterization of a general nuclear translocation signal in signaling proteins. Mol Cell 2008, 31:850-61.
30. Plotnikov A, Chuderland D, Karamansha Y, Livnah O, Seger R: Nuclear extracellular signal-regulated kinase 1 and 2 translocation is mediated by casein kinase 2 and accelerated by autophosphorylation. Mol Cell Biol 2011, 31:3515-30.
31. Xu L, Massagué J: Nucleocytoplasmic shuttling of signal transducers. Nat Rev Mol Cell Biol 2004, 5:209-19. (Pubitemid 38325802)
32. Chuderland D, Marmor G, Shainskaya A, Seger R: Calciummediated interactions regulate the subcellular localization of extracellular signal-regulated kinases. J Biol Chem 2008, 283:11176-88.
33. Chuderland D, Seger R: Calcium regulates ERK signaling by modulating its protein-protein interactions. Commun Integr Biol 2008, 1:4-5.
34. Marenda DR, Vrailas AD, Rodrigues AB, Cook S, Powers MA, Lorenzen JA, Perkins LA, Moses K: MAP kinase subcellular localization controls both pattern and proliferation in the developing Drosophila wing. Development 2006, 133:43-51. (Pubitemid 43169319)
35. Lorenzen JA, Baker SE, Denhez F, Melnick MB, Brower DL, Perkins LA: Nuclear import of activated D-ERK by DIM-7, an importin family member encoded by the gene moleskin. Development 2001, 128:1403-14. (Pubitemid 32409660)
36. Vrailas AD, Marenda DR, Cook SE, Powers MA, Lorenzen JA, Perkins LA, Moses K: smoothened and thickveins regulate Moleskin/Importin 7-mediated MAP kinase signaling in the developing Drosophila eye. Development 2006, 133:1485-94. (Pubitemid 43732962)
37. Kumar JP, Hsiung F, Powers MA, Moses K: Nuclear translocation of activated MAP kinase is developmentally regulated in the developing Drosophila eye. Development 2003, 130:3703-14. (Pubitemid 37039076)
38. Kumar JP, Tio M, Hsiung F, Akopyan S, Gabay L, Seger R, Shilo BZ, Moses K: Dissecting the roles of the Drosophila EGF receptor in eye development and MAP kinase activation. Development 1998, 125:3875-85. (Pubitemid 28488362)
39. Aitchison JD, Blobel G, Rout MP: Kap104p: a karyopherin involved in the nuclear transport of messenger RNA binding proteins. Science 1996, 274:624-7. (Pubitemid 26360444)
40. Fornerod M, van Deursen J, van Baal S, Reynolds A, Davis D, Murti KG, 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, 16:807-16. (Pubitemid 27089527)
41. Yaseen NR, Blobel G: Cloning and characterization of human karyopherin beta3. Proc Natl Acad Sci U S A 1997, 94:4451-6. (Pubitemid 27194262)
42. Fridell RA, Truant R, Thorne L, Benson RE, Cullen BR: Nuclear import of hnRNP A1 ismediated by a novel cellular cofactor related to karyopherin-beta. J Cell Sci 1997, 110(Pt 11):1325-31. (Pubitemid 27273703)
43. Rout MP, Blobel G, Aitchison JD: A distinct nuclear import pathway used by ribosomal proteins. Cell 1997, 89:715-25. (Pubitemid 27516174)
44. Görlich D, Dabrowski M, Bischoff FR, Kutay U, Bork P, Hartmann E, Prehn S, Izaurralde E: A novel class of RanGTP binding proteins. J Cell Biol 1997, 138:65-80. (Pubitemid 27337453)
45. Kutay U, Hartmann E, Treichel N, Calado A, Carmo-Fonseca M, Prehn S, Kraft R, Gorlich D, Bischoff FR: Identification of two novel RanGTP-binding proteins belonging to the importin beta superfamily. J Biol Chem 2000, 275:40163-8. (Pubitemid 32064644)
46. Chook YM, Blobel G: Karyopherins and nuclear import. Curr Opin Struct Biol 2001, 11:703-15. (Pubitemid 34076632)
47. Görlich D, Kutay U: Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol 1999, 15:607-60. (Pubitemid 32250388)
48. Jäkel S, Albig W, Kutay U, Bischoff FR, Schwamborn K, Doenecke D, Görlich D: The importin beta/importin 7 heterodimer is a functional nuclear import receptor for histone H1. EMBO J 1999, 18:2411-23. (Pubitemid 29213275)
49. Gontan C, Güttler T, Engelen E, Demmers J, Fornerod M, Grosveld FG, Tibboel D, Görlich D, Poot RA, Rottier RJ: Exportin 4 mediates a novel nuclear import pathway for Sox family transcription factors. J Cell Biol 2009, 185:27-34.
50. Waldmann I, Wälde S, Kehlenbach RH: Nuclear import of c-Jun is mediated by multiple transport receptors. J Biol Chem 2007, 282:27685-92. (Pubitemid 47529531)
51. Chachami G, Paraskeva E, Mingot J, Braliou GG, Görlich D, Simos G: Transport of hypoxia-inducible factor HIF-1alpha into the nucleus involves importins 4 and 7. Biochem Biophys Res Commun 2009, 390:235-40.
52. Yao X, Chen X, Cottonham C, Xu L: Preferential utilization of Imp7/8 in nuclear import of Smads. J Biol Chem 2008, 283: 22867-74.
53. Chen X, Xu L: Mechanism and regulation of nucleocytoplasmic trafficking of smad. Cell Biosci 2011, 1:40.
54. Freedman ND, Yamamoto KR: Importin 7 and importin alpha/importin beta are nuclear import receptors for the glucocorticoid receptor. Mol Biol Cell 2004, 15:2276-86. (Pubitemid 38580645)
55. Fassati A, Görlich D, Harrison I, Zaytseva L, Mingot J: Nuclear import of HIV-1 intracellular reverse transcription complexes is mediated by importin 7. EMBO J 2003, 22:3675-85. (Pubitemid 36898344)
56. Chen J, Liu MY, Parish CR, Chong BH, Khachigian L: Nuclear import of early growth response-1 involves importin-7 and the novel nuclear localization signal serine-proline-serine. Int J Biochem Cell Biol 2011, 43:905-12.
57. WuF, Wang P, Young LC, Lai R, Li L: Proteome-wide identification of novel binding partners to the oncogenic fusion gene protein, NPM-ALK, using tandem affinity purification and mass spectrometry. Am J Pathol 2009, 174:361-70.
58. Weinmann L, Höck J, Ivacevic T, Ohrt T, Mütze J, Schwille P, Kremmer E, Benes V, Urlaub H, Meister G: Importin 8 is a gene silencing factor that targets argonaute proteins to distinct mRNAs. Cell 2009, 136:496-507.
59. Arnold M, Nath A, Wohlwend D, Kehlenbach RH: Transportin is a major nuclear import receptor for c-Fos: a novel mode of cargo interaction. J Biol Chem 2006, 281:5492-9. (Pubitemid 43847644)
60. Higashi N, Kunimoto H, Kaneko S, Sasaki T, Ishii M, Kojima H, Nakajima K: Cytoplasmic c-Fos induced by the YXXQ-derived STAT3 signal requires the co-operative MEK/ERK signal for its nuclear translocation. Genes Cells 2004, 9:233-42. (Pubitemid 38380230)
61. Miyauchi Y, Michigami T, Sakaguchi N, Sekimoto T, Yoneda Y, Pike JW, Yamagata M, Ozono K: Importin 4 is responsible for ligand-independent nuclear translocation of vitamin D receptor. J Biol Chem 2005, 280:40901-8. (Pubitemid 41780583)
62. Lipowsky G, Bischoff FR, Schwarzmaier P, Kraft R, Kostka S, Hartmann E, Kutay U, Görlich D: Exportin 4: a mediator of a novel nuclear export pathway in higher eukaryotes. EMBO J 2000, 19:4362-71. (Pubitemid 30623747)
63. Harootunian AT, Adams SR, Wen W, Meinkoth JL, Taylor SS, Tsien RY: Movement of the free catalytic subunit of cAMPdependent protein kinase into and out of the nucleus can be explained by diffusion. Mol Biol Cell 1993, 4:993-1002. (Pubitemid 23331539)
64. Adachi M, Fukuda M, Nishida E: Two co-existing mechanisms for nuclear import of MAP kinase: passive diffusion of a monomer and active transport of a dimer. EMBO J 1999, 18: 5347-58. (Pubitemid 29465584)
65. Melen K, Kinnunen L, Julkunen I: Arginine/lysine-rich structural element is involved in interferon-induced nuclear import of STATs. J Biol Chem 2001, 276:16447-55.
66. Khokhlatchev AV, Canagarajah B, Wilsbacher J, Robinson M, Atkinson M, Goldsmith E, Cobb MH: Phosphorylation of the MAP kinase ERK2 promotes its homodimerization and nuclear translocation. Cell 1998, 93:605-15. (Pubitemid 28240721)
67. Fagotto F, Glück U, Gumbiner BM: Nuclear localization signalindependent and importin/karyopherin-independent nuclear import of beta-catenin. Curr Biol 1998, 8:181-90. (Pubitemid 28126609)
68. Xu L, Alarcón C, Cöl S, Massagué J: Distinct domain utilization by Smad3 and Smad4 for nucleoporin interaction and nuclear import. J Biol Chem 2003, 278:42569-77. (Pubitemid 37310530)
69. Matsubayashi Y, Fukuda M, Nishida E: Evidence for existence of a nuclear pore complex-mediated, cytosol-independent pathway of nuclear translocation of ERK MAP kinase in permeabilized cells. J Biol Chem 2001, 276:41755-60.
70. Whitehurst AW, Wilsbacher JL, You Y, Luby-Phelps K, Moore MS, Cobb MH: ERK2 enters the nucleus by a carrier-independent mechanism. Proc Natl Acad Sci U S A 2002, 99:7496-501. (Pubitemid 34568719)
71. Kawashima T, Bao YC, Nomura Y, Moon Y, Tonozuka Y, Minoshima Y, Hatori T, Tsuchiya A, Kiyono M, Nosaka T, Nakajima H, Williams DA, Kitamura T: Rac1 and a GTPase-activating protein, MgcRac-GAP, are required for nuclear translocation of STAT transcription factors. J Cell Biol 2006, 175:937-46. (Pubitemid 44969199)
72. Williams CC, Allison JG, Vidal GA, Burow ME, Beckman BS, Marrero L, Jones FE: The ERBB4/HER4 receptor tyrosine kinase regulates gene expression by functioning as a STAT5A nuclear chaperone. J Cell Biol 2004, 167:469-78. (Pubitemid 39489055)
73. Wolf I, Rubinfeld H, Yoon S, Marmor G, Hanoch T, Seger R: Involvement of the activation loop of ERK in the detachment from cytosolic anchoring. J Biol Chem 2001, 276:24490-7.
74. Lidke DS, Huang F, Post JN, Rieger B, Wilsbacher J, Thomas JL, Pouysségur J, Jovin TM, Lenormand P: ERK nuclear translocation is dimerization-independent but controlled by the rate of phosphorylation. J Biol Chem 2010, 285:3092-102.
75. Casar B, Pinto A, Crespo P: Essential role of ERK dimers in the activation of cytoplasmic but not nuclear substrates by ERKscaffold complexes. Mol Cell 2008, 31:708-21.
76. Ranganathan A, Yazicioglu MN, Cobb MH: The nuclear localization of ERK2 occurs by mechanisms both independent of and dependent on energy. J Biol Chem 2006, 281:15645-52. (Pubitemid 43848450)
77. Kosugi S, Hasebe M, Entani T, Takayama S, Tomita M, Yanagawa H: Design of peptide inhibitors for the importin alpha/beta nuclear import pathway by activity-based profiling. Chem Biol 2008, 15:940-9.
78. Hintersteiner M, Ambrus G, Bednenko J, Schmied M, Knox AJS, Meisner N, Gstach H, Seifert J, Singer EL, Gerace L, Auer M: Identification of a small molecule inhibitor of importin b mediated nuclear import by confocal on-bead screening of tagged one-bead one-compound libraries. ACS Chem Biol 2010, 5:967-79.
79. Ambrus G, Whitby LR, Singer EL, Trott O, Choi E, Olson AJ, Boger DL, Gerace L: Small molecule peptidomimetic inhibitors of importin a/b mediated nuclear transport. Bioorg Med Chem 2010, 18:7611-20.
80. Soderholm JF, Bird SL, Kalab P, Sampathkumar Y, Hasegawa K, Uehara-Bingen M, Weis K, Heald R: Importazole, a small molecule inhibitor of the transport receptor importin-b. ACS Chem Biol 2011, 6:700-8.
81. Cansizoglu AE, Lee BJ, Zhang ZC, Fontoura BMA, Chook YM: Structure-based design of a pathway-specific nuclear import inhibitor. Nat Struct Mol Biol 2007, 14:452-4. (Pubitemid 46685879)
82. Süel KE, Gu H, Chook YM: Modular organization and combinatorial energetics of proline-tyrosine nuclear localization signals. PLoS Biol 2008, 6:e137.
83. Chook YM, Jung A, Rosen MK, Blobel G: Uncoupling Kapbeta2 substrate dissociation and ran binding. Biochemistry 2002, 41:6955-66. (Pubitemid 34575667)
84. Siomi MC, Eder PS, Kataoka N, Wan L, Liu Q, Dreyfuss G: Transportin-mediated nuclear import of heterogeneous nuclear RNP proteins. J Cell Biol 1997, 138:1181-92. (Pubitemid 27415046)
85. Pollard VW, Michael WM, Nakielny S, Siomi MC, Wang F, Dreyfuss G: A novel receptor-mediated nuclear protein import pathway. Cell 1996, 86:985-94. (Pubitemid 26336802)
86. Bonifaci N, Moroianu J, Radu A, Blobel G: Karyopherin beta2 mediates nuclear import of a mRNA binding protein. Proc Natl Acad Sci U S A 1997, 94:5055-60. (Pubitemid 27214735)
87. Zakaryan RP, Gehring H: Identification and characterization of the nuclear localization/retention signal in the EWS protooncoprotein. J Mol Biol 2006, 363:27-38. (Pubitemid 44414847)
88. Güttinger S, Mühlhäusser P, Koller-Eichhorn R, Brennecke J, Kutay U: Transportin2 functions as importin and mediates nuclear import of HuR. Proc Natl Acad Sci U S A 2004, 101:2918-23. (Pubitemid 38327711)
89. Jäkel S, Görlich D: Importin beta, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J 1998, 17:4491-502. (Pubitemid 28362637)
90. van der Giessen K, Gallouzi I: Involvement of transportin 2-mediated HuR import in muscle cell differentiation. Mol Biol Cell 2007, 18:2619-29. (Pubitemid 47025726)
91. Rebane A, Aab A, Steitz JA: Transportins 1 and 2 are redundant nuclear import factors for hnRNP A1 and HuR. RNA 2004, 10:590-9. (Pubitemid 38405937)
92. Heese K, Yamada T, Akatsu H, Yamamoto T, Kosaka K, Nagai Y, Sawada T: Characterizing the new transcription regulator protein p60TRP. J Cell Biochem 2004, 91:1030-42.
93. Ross AE, Vuica M, Desiderio S: Overlapping signals for protein degradation and nuclear localization define a role for intrinsic RAG-2 nuclear uptake in dividing cells. Mol Cell Biol 2003, 23:5308-19. (Pubitemid 36950886)
94. Lubert EJ, Sarge KD: Interaction between protein phosphatase 2A and members of the importin beta superfamily. Biochem Biophys Res Commun 2003, 303:908-13. (Pubitemid 36384941)
95. Lin W, Ye W, Cai L, Meng X, Ke G, Huang C, Peng Z, Yu Y, Golden JA, Tartakoff AM, Tao T: The roles of multiple importins for nuclear import of murine aristaless-related homeobox protein. J Biol Chem 2009, 284:20428-39.
96. Plafker SM, Macara IG: Importin-11, a nuclear import receptor for the ubiquitin-conjugating enzyme, UbcM2. EMBO J 2000, 19:5502-13.
97. Lai M, Kuo H, Chang W, Tarn W: A novel splicing regulator shares a nuclear import pathway with SR proteins. EMBO J 2003, 22:1359-69. (Pubitemid 36362699)
98. Tao T, Lan J, Lukacs GL, Haché RJG, Kaplan F: Importin 13 regulates nuclear import of the glucocorticoid receptor in airway epithelial cells. Am J Respir Cell Mol Biol 2006, 35:668-80. (Pubitemid 44901856)
99. Bono F, Cook AG, Grünwald M, Ebert J, Conti E: Nuclear import mechanism of the EJC component Mago-Y14 revealed by structural studies of importin 13. Mol Cell 2010, 37:211-22.