Kinetic analysis of Smad nucleocytoplasmic shuttling reveals a mechanism for transforming growth factor β-dependent nuclear accumulation of Smads

Molecular and Cellular Biology

Volumn 25, Issue 22, 2005, Pages 9845-9858

  Schmierer, Bernhard ^a   Hill, Caroline S ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; SMAD PROTEIN; SMAD2 PROTEIN; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; CELL NUCLEUS; COMPLEX FORMATION; CONTROLLED STUDY; CYTOPLASM; FLUORESCENCE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; NUCLEOCYTOPLASMIC TRANSPORT; PHOTOACTIVATION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; TRANSPORT KINETICS;

ANIMALS; BIOLOGICAL TRANSPORT; CELL LINE, TUMOR; CELL NUCLEUS; CYTOPLASM; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; KINETICS; LIGHT; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; PHOSPHORYLATION; PLASMIDS; SIGNAL TRANSDUCTION; SMAD PROTEINS; SMAD2 PROTEIN; TIME FACTORS; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA2; XENOPUS;

EID: 27644583784     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.22.9845-9858.2005     Document Type: Article

References (27)

1. Angel, P., I. Baumann, B. Stein, H. Delius, H. J. Rahmsdorf, and P. Herrlich. 1987. 12-O-Tetradecanoyl-phorbol-13-acetate induction of the human collagenase gene is mediated by an inducible enhancer element located in the 5′-flanking region. Mol. Cell. Biol. 7:2256-2266.
2. Chen, H. B., J. G. Rud, K. Lin, and L. Xu. 2005. Nuclear targeting of TGF-β-activated Smad complexes. J. Biol. Chem. 280:21329-21336.
3. De Bosscher, K., C. S. Hill, and F. J. Nicolas. 2004. Molecular and functional consequences of Smad4 C-terminal missense mutations in colorectal tumour cells. Biochem. J. 379:209-216.
4. Germain, S., M. Howell, G. M. Esslemont, and C. S. Hill. 2000. Homeodomain and winged-helix transcription factors recruit activated Smads to distinct promoter elements via a common Smad interaction motif. Genes Dev. 14:435-451.
5. Hager, G. L., C. Elbi, and M. Becker. 2002. Protein dynamics in the nuclear compartment. Curr. Opin. Genet. Dev. 12:137-141.
6. Inman, G. J., F. J. Nicolas, J. F. Callahan, J. D. Harling, L. M. Gaster, A. D. Reith, N. J. Laping, and C. S. Hill. 2002. SB-431542 is a potent and specific inhibitor of Transforming Growth Factor-β superfamily type I activin receptor-like kinase receptors, ALK4, ALK5 and ALK7. Mol. Pharmacol. 62:65-72.
7. Inman, G. J., F. J. Nicolas, and C. S. Hill. 2002. Nucleocytoplasmic shuttling of Smads 2, 3 and 4 permits sensing of TGF-β receptor activity. Mol. Cell 10:283-294.
8. Kurisaki, A., S. Kose, Y. Yoneda, C. H. Heldin, and A. Moustakas. 2001. Transforming growth factor-β induces nuclear import of Smad3 in an importin-β1 and Ran-dependent manner. Mol. Biol. Cell 12:1079-1091.
9. Laping, N. J., E. Grygielko, A. Mathur, S. Butter, J. Bomberger, C. Tweed, J. Fornwald, R. Lehr, J. D. Harling, L. M. Gaster, J. F. Callahan, and B. A. Olson. 2002. Inhibition of transforming growth factor (TGF)-β1-induced extracellular matrix with a novel inhibitor of the TGF-β type I receptor kinase activity. Mol. Pharmacol. 62:58-64.
10. Nicolás, F. J., K. De Bosscher, B. Schmierer, and C. S. Hill. 2004. Analysis of Smad nucleocytoplasmic shuttling in living cells. J. Cell Sci. 117:4113-4125.
11. Nicolas, F. J., and C. S. Hill. 2003. Attenuation of the TGFβ-Smad signaling pathway in pancreatic tumor cells confers resistance to TGFβ-induced growth arrest. Oncogene 22:3698-3711.
12. Patterson, G. H., and J. Lippincott-Schwartz. 2002. A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297:1873-1877.
13. Pierreux, C. E., F. J. Nicolas, and C. S. Hill. 2000. Transforming growth factor β-independent shuttling of Smad4 between the cytoplasm and nucleus. Mol. Cell. Biol. 20:9041-9054.
14. Randall, R. A., S. Germain, G. J. Inman, P. A. Bates, and C. S. Hill. 2002. Different Smad2 partners bind a common hydrophobic pocket in Smad2 via a defined proline-rich motif. EMBO J. 21:145-156.
15. Randall, R. A., M. Howell, C. S. Page, A. Daly, P. A. Bates, and C. S. Hill. 2004. Recognition of phosphorylated-Smad2-containing complexes by a novel Smad interaction motif. Mol. Cell. Biol. 24:1106-1121.
16. Ribbeck, K., and D. Gorlich. 2001. Kinetic analysis of translocation through nuclear pore complexes. EMBO J. 20:1320-1330.
17. Shi, Y., and J. Massagué. 2003. Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113:685-700.
18. Sprague, B. L., and J. G. McNally. 2005. FRAP analysis of binding: proper and fitting. Trends Cell. Biol. 15:84-91.
19. Swanson, J. A., M. Lee, and P. E. Knapp. 1991. Cellular dimensions affecting the nucleocytoplasmic volume ratio. J. Cell. Biol. 115:941-948.
20. Watanabe, M., N. Masuyama, M. Fukuda, and E. Nishida. 2000. Regulation of intracellular dynamics of Smad4 by its leucine-rich nuclear export signal. EMBO Rep. 1:176-182.
21. Wu, J. W., R. Fairman, J. Penry, and Y. Shi. 2001. Formation of a stable heterodimer between Smad2 and Smad4. J. Biol. Chem. 276:20688-20694.
22. Xiao, Z., R. Latek, and H. F. Lodish. 2003. An extended bipartite nuclear localization signal in Smad4 is required for its nuclear import and transcriptional activity. Oncogene 22:1057-1069.
23. Xiao, Z., X. Liu, and H. F. Lodish. 2000. Importin β mediates nuclear translocation of Smad3. J. Biol. Chem. 275:23425-23428.
24. Xu, L., C. Alarcon, S. Col, and J. Massagué. 2003. Distinct domain utilization by Smad3 and Smad4 for nucleoporin interaction and nuclear import. J. Biol. Chem. 278:42569-42577.
25. Xu, L., Y. G. Chen, and J. Massagué. 2000. The nuclear import function of Smad2 is masked by SARA and unmasked by TGFβ-dependent phosphorylation. Nat. Cell. Biol. 2:559-562.
26. Xu, L., Y. Kang, S. Col, and J. Massagué. 2002. Smad2 nucleocytoplasmic shuttling by nucleoporins CAN/Nup214 and Nup153 feeds TGFβ signaling complexes in the cytoplasm and nucleus. Mol. Cell 10:271-282.
27. Xu, L., and J. Massagué. 2004. Nucleocytoplasmic shuttling of signal transducers. Nat. Rev. Mol. Cell. Biol. 5:209-219.