Kinetic and molecular analysis of nuclear export factor CRM1 association with its cargo in vivo

Molecular and Cellular Biology

Volumn 25, Issue 2, 2005, Pages 728-739

  Daelemans, Dirk ^a,c   Costes, Sylvain V ^b   Lockett, Stephen ^b   Pavlakis, George N ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SAIC FREDERICK INC   (United States)

^c REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EXPORTIN 1; GREEN FLUORESCENT PROTEIN; LEPTOMYCIN B; RAN PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL NUCLEUS MEMBRANE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE DELETION; HUMAN; HUMAN CELL; IN VIVO STUDY; KINETICS; MOLECULAR INTERACTION; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL NUCLEOLUS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE PRODUCTS, REV; HELA CELLS; HUMANS; KARYOPHERINS; LUMINESCENT PROTEINS; MULTIPROTEIN COMPLEXES; RAN GTP-BINDING PROTEIN; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECOMBINANT FUSION PROTEINS;

EID: 11844272621     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.2.728-739.2005     Document Type: Article

References (61)

1. Adachi, Y., and M. Yanagida. 1989. Higher order chromosome structure is affected by cold-sensitive mutations in a Schizosaccharomyces pombe gene crm1+ which encodes a 115-kD protein preferentially localized in the nucleus and its periphery. J. Cell Biol. 108:1195-1207.
2. Askjaer, P., A. Bachi, M. Wilm, F. R. Bischoff, D. L. Weeks, V. Ogniewski, M. Ohno, C. Niehrs, J. Kjems, I. W. Mattaj, and M. Fornerod. 1999. RanGTP-regulated interactions of CRM1 with nucleoporins and a shuttling DEAD-box helicase. Mol. Cell. Biol. 19:6276-6285.
3. Askjaer, P., T. H. Jensen, J. Nilsson, L. Englmeier, and J. Kjems. 1998. The specificity of the CRM1-Rev nuclear export signal interaction is mediated by RanGTP. J. Biol. Chem. 273:33414-33422.
4. Bastiaens, P. I., and T. M. Jovin. 1996. Microspectroscopic imaging tracks the intracellular processing of a signal transduction protein: fluorescent-labeled protein kinase C beta 1. Proc. Natl. Acad. Sci. USA 93:8407-5412.
5. Bastiaens, P. I., I. V. Majoul, P. J. Verveer, H. D. Soling, and T. M. Jovin. 1996. Imaging the intracellular trafficking and state of the AB5 quaternary structure of cholera toxin. EMBO J. 15:4246-4253.
6. Bischoff, F. R., and H. Ponstingl. 1991. Catalysis of guanine nucleotide exchange on Ran by the mitotic regulator RCC1. Nature 354:80-82.
7. Chi, N. C., E. J. Adam, and S. A. Adam. 1997. Different binding domains for Ran-GTP and Ran-GDP/RanBP1 on nuclear import factor p97. J. Biol. Chem. 272:6818-6822.
8. Connor, M. K., R. Kotchetkov, S. Cariou, A. Resch, R. Lupetti, R. G. Beniston, F. Melchior, L. Hengst, and J. M. Slingerland. 2003. CRM1/Ran-mediated nuclear export of p27(Kip1) involves a nuclear export signal and links p27 export and proteolysis. Mol. Biol. Cell 14:201-213.
9. Daelemans, D., E. Afonina, J. Nilsson, G. Werner, J. Kjems, E. De Clercq, G. N. Pavlakis, and A. M. Vandamme. 2002. A synthetic HIV-1 Rev inhibitor interfering with the CRM1-mediated nuclear export. Proc. Natl. Acad. Sci. USA 99:14440-14445.
10. Dundr, M., U. Hoffmann-Rohrer, Q. Hu, I. Grummt, L. I. Rothblum, R. D. Phair, and T. Misteli. 2002. A kinetic framework for a mammalian RNA polymerase in vivo. Science 298:1623-1626.
11. Dundr, M., and T. Misteli. 2001. Functional architecture in the cell nucleus. Biochem. J. 356:297-310.
12. Edidin, M., Y. Zagyansky, and T. J. Lardner. 1976. Measurement of membrane protein lateral diffusion in single cells. Science 191:466-468.
13. Felber, B. K., M. Hadzopoulou-Cladaras, C. Cladaras, T. Copeland, and G. N. Pavlakis. 1989. rev protein of human immunodeficiency virus type 1 affects the stability and transport of the viral mRNA. Proc. Natl. Acad. Sci. USA 86:1495-1499.
14. Fischer, U., J. Huber, W. C. Boelens, I. W. Mattaj, and R. Luhrmann. 1995. The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell 82:475-483.
15. Floer, M., and G. Blobel. 1999. Putative reaction intermediates in Crm1-mediated nuclear protein export. J. Biol. Chem. 274:16279-16286.
16. Fornerod, M., M. Ohno, M. Yoshida, and I. W. Mattaj. 1997. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90:1051-1060.
17. Fornerod, M., J. van Deursen, S. van Baal, A. Reynolds, D. Davis, K. G. Murti, J. Fransen, and G. Grosveld. 1997. The human homologue of yeast CRM1 is in a dynamic subcomplex with CAN/Nup214 and a novel nuclear pore component Nup88. EMBO J. 16:807-816.
18. Fukuda, M., S. Asano, T. Nakamura, M. Adachi, M. Yoshida, M. Yanagida, and E. Nishida. 1997. CRM1 is responsible for intracellular transport mediated by the nuclear export signal. Nature 390:308-311.
19. Gorlich, D. 1998. Transport into and out of the cell nucleus. EMBO J. 17:2721-2727.
20. Gorlich, D., M. Dabrowski, F. R. Bischoff, U. Kutay, P. Bork, E. Hartmann, S. Prehn, and E. Izaurralde. 1997. A novel class of RanGTP binding proteins. J. Cell Biol. 138:65-50.
21. Gorlich, D., and U. Kutay. 1999. Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell Dev. Biol. 15:607-660.
22. Guan, T., R. H. Kehlenbach, E. C. Schirmer, A. Kehlenbach, F. Fan, B. E. Clurman, N. Arnheim, and L. Gerace. 2000. Nup50, a nucleoplasmically oriented nucleoporin with a role in nuclear protein export. Mol. Cell. Biol. 20:5619-5630.
23. Ha, T., T. Enderle, D. F. Ogletree, D. S. Chemla, P. R. Selvin, and S. Weiss. 1996. Probing the interaction between two single molecules: fluorescence resonance energy transfer between a single donor and a single acceptor. Proc. Natl. Acad. Sci. USA 93:6264-6268.
24. Houtsmuller, A. B., S. Rademakers, A. L. Nigg, D. Hoogstraten, J. H. Hoeijmakers, and W. Vermeulen. 1999. Action of DNA repair endonuclease ERCC1/XPF in living cells. Science 284:958-961.
25. Izaurralde, E., U. Kutay, C. von Kobbe, I. W. Mattaj, and D. Gorlich. 1997. The asymmetric distribution of the constituents of the Ran system is essential for transport into and out of the nucleus. EMBO J. 16:6535-6547.
26. Kehlenbach, R. H., A. Dickmanns, and L. Gerace. 1998. Nucleocytoplasmic shuttling factors including Ran and CRM1 mediate nuclear export of NFAT in vitro. J. Cell Biol. 141:863-574.
27. Kehlenbach, R. H., A. Dickmanns, A. Kehlenbach, T. Guan, and L. Gerace. 1999. A role for RanBP1 in the release of CRM1 from the nuclear pore complex in a terminal step of nuclear export. J. Cell Biol. 145:645-657.
28. Kenworthy, A. K. 2001. Imaging protein-protein interactions using fluorescence resonance energy transfer microscopy. Methods 24:289-296.
29. Kenworthy, A. K., and M. Edidin. 1998. Distribution of a glycosylphosphatidylinositol-anchored protein at the apical surface of MDCK cells examined at a resolution of <100 A using imaging fluorescence resonance energy transfer. J. Cell Biol. 142:69-84.
30. Kudo, N., N. Matsumori, H. Taoka, D. Fujiwara, E. P. Schreiner, B. Wolff, M. Yoshida, and S. Horinouchi. 1999. Leptomycin B inactivates CRM1/ exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc. Natl. Acad. Sci. USA 96:9112-9117.
31. Kudo, N., B. Wolff, T. Sekimoto, E. P. Schreiner, Y. Yoneda, M. Yanagida, S. Horinouchi, and M. Yoshida. 1998. Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp. Cell Res. 242:540-547.
32. Kutay, U., E. Izaurralde, F. R. Bischoff, I. W. Mattaj, and D. Gorlich. 1997. Dominant-negative mutants of importin-beta block multiple pathways of import and export through the nuclear pore complex. EMBO J. 16:1153-1163.
33. Leonhardt, H., H. P. Rahn, P. Weinzierl, A. Sporbert, T. Cremer, D. Zink, and M. C. Cardoso. 2000. Dynamics of DNA replication factories in living cells. J. Cell Biol. 149:271-280.
34. Lippincott-Schwartz, J., E. Snapp, and A. Kenworthy. 2001. Studying protein dynamics in living cells. Nat. Rev. Mol. Cell Biol. 2:444-456.
35. Macara, I. G. 2001. Transport into and out of the nucleus. Microbiol. Mol. Biol. Rev. 65:570-594.
36. Malim, M. H., J. Hauber, S. Y. Le, J. V. Maizel, and B. R. Cullen. 1989. The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature 338:254-257.
37. Mattaj, I. W., and L. Englmeier. 1998. Nucleocytoplasmic transport: the soluble phase. Annu. Rev. Biochem. 67:265-306.
38. Meyer, B. E., J. L. Meinkoth, and M. H. Malim. 1996. Nuclear transport of human immunodeficiency virus type 1, visna virus, and equine infectious anemia virus Rev proteins: identification of a family of transferable nuclear export signals. J. Virol. 70:2350-2359.
39. Michienzi, A., L. Cagnon, I. Bahner, and J. J. Rossi. 2000. Ribozyme-mediated inhibition of HIV 1 suggests nucleolar trafficking of HIV-1 RNA. Proc. Natl. Acad. Sci. USA 97:8955-8960.
40. Misteli, T. 2001. Protein dynamics: implications for nuclear architecture and gene expression. Science 291:843-847.
41. Neville, M., F. Stutz, L. Lee, L. I. Davis, and M. Rosbash. 1997. The importin-beta family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export. Curr. Biol. 7:767-775.
42. Nigg, E. A. 1997. Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature 386:779-787.
43. Ossareh-Nazari, B., F. Bachelerie, and C. Dargemont. 1997. Evidence for a role of CRM1 in signal-mediated nuclear protein export. Science 278:141-144.
44. Ossareh-Nazari, B., and C. Dargemont. 1999. Domains of Crm1 involved in the formation of the Crm1, RanGTP, and leucine-rich nuclear export sequences trimeric complex. Exp. Cell Res. 252:236-241.
45. Paraskeva, E., E. Izaurralde, F. R. Bischoff, J. Huber, U. Kutay, E. Hartmann, R. Luhrmann, and D. Gorlich. 1999. CRM1-mediated recycling of snurportin 1 to the cytoplasm. J. Cell Biol. 145:255-264.
46. Pemberton, L. F., G. Blobel, and J. S. Rosenblum. 1998. Transport routes through the nuclear pore complex. Curr. Opin. Cell Biol. 10:392-399.
47. Phair, R. D., and T. Misteli. 2001. Kinetic modelling approaches to in vivo imaging. Nat. Rev. Mol. Cell Biol. 2:898-907.
48. Reits, E. A., and J. J. Neefjes. 2001. From fixed to FRAP: measuring protein mobility and activity in living cells. Nat. Cell Biol. 3:E145-E147.
49. Richards, S. A., K. M. Lounsbury, K. L. Carey, and I. G. Macara. 1996. A nuclear export signal is essential for the cytosolic localization of the Ran binding protein, RanBP1. J. Cell Biol. 134:1157-1168.
50. Selvin, P. R. 2000. The renaissance of fluorescence resonance energy transfer. Nat. Struct. Biol. 7:730-734.
51. Smith, A. E., B. M. Slepchenko, J. C. Schaff, L. M. Loew, and I. G. Macara. 2002. Systems analysis of Ran transport. Science 295:488-491.
52. Stade, K., C. S. Ford, C. Guthrie, and K. Weis. 1997. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 90:1041-1050.
53. Stauber, R. H., E. Afonina, S. Gulnik, J. Erickson, and G. N. Pavlakis. 1998. Analysis of intracellular trafficking and interactions of cytoplasmic HIV-1 Rev mutants in living cells. Virology 251:38-48.
54. Terwilliger, E., R. Burghoff, R. Sia, J. Sodroski, W. Haseltine, and C. Rosen. 1988. The art gene product of human immunodeficiency virus is required for replication. J. Virol. 62:655-658.
55. Thomas, F., and U. Kutay. 2003. Biogenesis and nuclear export of ribosomal subunits in higher eukaryotes depend on the CRM1 export pathway. J. Cell Sci. 116:2409-2419.
56. Wen, W., J. L. Meinkoth, R. Y. Tsien, and S. S. Taylor. 1995. Identification of a signal for rapid export of proteins from the nucleus. Cell 82:463-473.
57. Wolff, B., J. J. Sanglier, and Y. Wang. 1997. Leptomycin B is an inhibitor of nuclear export: inhibition of nucleo-cytoplasmic translocation of the human immunodeficiency virus type 1 (HIV-1) Rev protein and Rev-dependent mRNA. Chem. Biol. 4:139-147.
58. Wouters, F. S., P. I. Bastiaens, K. W. Wirtz, and T. M. Jovin. 1998. FRET microscopy demonstrates molecular association of non-specific lipid transfer protein (nsL-TP) with fatty acid oxidation enzymes in peroxisomes. EMBO J. 17:7179-7189.
59. Wozniak, R. W., M. P. Rout, and J. D. Aitchison. 1998. Karyopherins and kissing cousins. Trends Cell Biol. 8:184-188.
60. Yan, C., L. H. Lee, and L. I. Davis. 1998. Crm1p mediates regulated nuclear export of a yeast AP-1-like transcription factor. EMBO J. 17:7416-7429.
61. Zolotukhin, A. S., and B. K. Felber. 1999. Nucleoporins nup98 and nup214 participate in nuclear export of human immunodeficiency virus type 1 Rev. J. Virol. 73:120-127.