Kinetic and Molecular Analysis of Nuclear Export Factor CRM1 Association with Its Cargo In Vivo

REFERENCES

• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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 I. Proc. Natl. Acad. Sci. USA 93:8407–8412.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Bischoff, F. R., and H. Ponstingl. 1991. Catalysis of guanine nucleotide exchange on Ran by the mitotic regulator RCC1. Nature 354:80–82.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Dundr, M., and T. Misteli. 2001. Functional architecture in the cell nucleus. Biochem. J. 356:297–310.
   PubMed Web of Science ®Google Scholar
• Edidin, M., Y. Zagyansky, and T. J. Lardner. 1976. Measurement of membrane protein lateral diffusion in single cells. Science 191:466–468.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Floer, M., and G. Blobel. 1999. Putative reaction intermediates in Crm1-mediated nuclear protein export. J. Biol. Chem. 274:16279–16286.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Gorlich, D. 1998. Transport into and out of the cell nucleus. EMBO J. 17:2721–2727.
   PubMed Web of Science ®Google Scholar
• 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. 138:65–80.
   PubMed Web of Science ®Google Scholar
• Gorlich, D., and U. Kutay. 1999. Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell Dev. Biol. 15:607–660.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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. 141:863–874.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Kenworthy, A. K. 2001. Imaging protein-protein interactions using fluorescence resonance energy transfer microscopy. Methods 24:289–296.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Lippincott-Schwartz, J., E. Snapp, and A. Kenworthy. 2001. Studying protein dynamics in living cells. Nat. Rev. Mol. Cell Biol. 2:444–456.
   PubMed Web of Science ®Google Scholar
• Macara, I. G. 2001. Transport into and out of the nucleus. Microbiol. Mol. Biol. Rev. 65:570–594.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Mattaj, I. W., and L. Englmeier. 1998. Nucleocytoplasmic transport: the soluble phase. Annu. Rev. Biochem. 67:265–306.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Misteli, T. 2001. Protein dynamics: implications for nuclear architecture and gene expression. Science 291:843–847.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Nigg, E. A. 1997. Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature 386:779–787.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• Pemberton, L. F., G. Blobel, and J. S. Rosenblum. 1998. Transport routes through the nuclear pore complex. Curr. Opin. Cell Biol. 10:392–399.
   PubMedGoogle Scholar
• Phair, R. D., and T. Misteli. 2001. Kinetic modelling approaches to in vivo imaging. Nat. Rev. Mol. Cell Biol. 2:898–907.
   PubMed Web of Science ®Google Scholar
• 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.
   Google Scholar
• 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.
   PubMedGoogle Scholar
• Selvin, P. R. 2000. The renaissance of fluorescence resonance energy transfer. Nat. Struct. Biol. 7:730–734.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Stade, K., C. S. Ford, C. Guthrie, and K. Weis. 1997. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 90:1041–1050.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Wozniak, R. W., M. P. Rout, and J. D. Aitchison. 1998. Karyopherins and kissing cousins. Trends Cell Biol. 8:184–188.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar