Characterization of Ran-driven cargo transport and the RanGTPase system by kinetic measurements and computer simulation

EMBO Journal

Volumn 22, Issue 5, 2003, Pages 1088-1100

  Görlich, Dirk ^b   Seewald, Michael J ^a   Ribbeck, Katharina ^c  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b TU DORTMUND UNIVERSITY   (Germany)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Importin; Kinetics; Nuclear transport; Translocation

Indexed keywords

GUANOSINE TRIPHOSPHATASE; NUCLEOTIDE; RAN PROTEIN; RECEPTOR; RECEPTOR NTF2; UNCLASSIFIED DRUG;

ARTICLE; CELL ENERGY; CELL LEVEL; CELL MEMBRANE PERMEABILITY; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL TRANSPORT; COMPUTER MODEL; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; HELA CELL; HUMAN; HUMAN CELL; MITOSIS SPINDLE; NUCLEAR PORE; PRIORITY JOURNAL; PROTEIN ANALYSIS; SOMATIC CELL; TRANSPORT KINETICS;

ACTIVE TRANSPORT, CELL NUCLEUS; BETA KARYOPHERINS; COMPUTER SIMULATION; GTPASE-ACTIVATING PROTEINS; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; HELA CELLS; HUMANS; KINETICS; NUCLEAR PORE; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; RAN GTP-BINDING PROTEIN;

EID: 0037416225     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg113     Document Type: Article

References (43)

1. Ben-Efraim. I. and Gerace, L. (2001) Gradient of increasing affinity of importin β for nucleoporins along the pathway of nuclear import. J. Cell Biol., 152, 411-417.
2. Bischoff, F.R. and Ponstingl, H. (1991a) Catalysis of guanine nucleotide exchange on Ran by the mitotic regulator RCC1. Nature, 354, 80-82.
3. Bischoff, F.R. and Ponstingl, H. (1991b) Mitotic regulator protein RCC1 is complexed with a nuclear ras-related polypeptide. Proc. Natl Acad. Sci. USA, 88, 10830-10834.
4. Bischoff, F.R. and Görlich, D. (1997) RanBP1 is crucial for the release of RanGTP from importin β-related nuclear transport factors. FEBS Lett., 419, 249-254.
5. Bischoff, F.R., Klebe, C., Kretschmer, J., Wittinghofer, A. and Ponstingl,H. (1994) RanGAP1 induces GTPase activity of nuclear ras-related Ran. Proc. Natl Acad. Sci. USA, 91, 2587-2591.
6. Bischoff, F.R., Krebber, H., Kempf, T., Hermes, I. and Ponstingl, H. (1995a) Human RanGTPase activating protein RanGAP1 is a homolog of yeast RNAlp involved in messenger RNA processing and transport. Proc. Natl Acad. Sci. USA., 92, 1749-1753.
7. Bischoff, F.R., Krebber, H., Smimova, E., Dong, W.H. and Ponstingl, H. (1995b) Coactivation of RanGTPase and inhibition of GTP dissociation by Ran GTP binding protein RanBP1. EMBO J., 14, 705-715.
8. Ellis, R.J. (2001) Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr. Opin. Struct. Biol., 11, 114-119.
9. Englmeier, L., Olivo, J.C. and Mattaj, I.W. (1999) Receptor-mediated substrate translocation through the nuclear pore complex without nucleotide triphosphate hydrolysis. Curr. Biol., 9, 30-41.
10. Floer, M., Blobel, G. and Rexach, M. (1997) Disassembly of RanGTP-karyopherin β complex, an intermediate in nuclear protein import. J. Biol. Chem., 272, 19538-19546.
11. Gilchrist, D., Mykytka, B. and Rexach, M. (2002) Accelerating the rate of disassembly of karyopherin cargo complexes. J. Biol. Chem., 277, 18161-18172.
12. Görlich, D. and Kutay, U. (1999) Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell. Dev. Biol., 15, 607-660.
13. Gruss, O.J. et al. (2001) Ran induces spindle assembly by reversing the inhibitory effect of importin α on TPX2 activity. Cell, 104, 83-93.
14. Hetzer, M., Bilbao-Cortes, D., Walther, T.C., Gruss, O.J. and Mattaj, I.W. (2000) GTP hydrolysis by Ran is required for nuclear envelope assembly. Mol. Cell, 5, 1013-1024.
15. Hetzer, M., Gruss, O.J. and Mattaj, I.W. (2002) The Ran GTPase as a marker of chromosome position in spindle formation and nuclear envelope assembly. Nat. Cell Biol., 4, E177-E184.
16. Holy, E.T. and Leibler, S. (1994). Dynamic instability of microtubules as an efficient way to search in space. Proc. Natl Acad. Sci. USA, 91, 5682-5685.
17. Kalab, P., Pu, R.T. and Dasso, M. (1999) The ran GTPase regulates mitotic spindle assembly. Curr. Biol., 9, 481-484.
18. Kalab, P., Weis, K. and Heald, R. (2002) Visualization of a Ran-GTP gradient in interphase and mitotic Xenopus egg extracts. Science, 295, 2452-2456.
19. Karsenti, E. and Vemos, I. (2001) The mitotic spindle: a self-made machine. Science, 294, 543-547.
20. Klebe, C., Biscoff, F.R., Ponstingl, H. and Wittinghofer, A. (1995a) Interaction of the nuclear GTP-binding protein Ran with its regulatory proteins RCC1 and RanGAP1. Biochemistry, 34, 639-647.
21. Klebe, C., Prinz, H., Wittinghofer, A. and Goody, R.S. (1995b) The kinetic mechanism of Ran-nucleotide exchange catalyzed by RCC1. Biochemistry, 34, 12543-12552.
22. Kose, S., Imamoto, N., Tachibana, T., Shimamoto, T. and Yoneda,Y. (1997) Ran-unassisted nuclear migration of a 97 kD component of nuclear pore-targeting complex. J. Cell Biol., 139, 841-849.
23. Lounsbury, K.M. and Macara, I.G. (1997) Ran-binding protein 1 (RanBP1) forms a ternary complex with Ran and karyopherin β and reduces Ran GTPase-activating protein (RanGAP) inhibition by karyopherin β. J. Biol. Chem., 272, 551-555.
24. Macara, I.G. (2001) Transport into and out of the nucleus. Microbiol. Mol. Biol. Rev., 65, 570-594.
25. Mahajan, R., Delphin, C., Guan, T., Gerace, L. and Melchior, F. (1997) A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell, 88, 97-107.
26. Mattaj, I.W. and Englmeier, L. (1998) Nucleocytoplasmic transport: the soluble phase. Annu. Rev. Biochem., 67, 265-306.
27. Matunis, M.J., Coutavas, E. and Blobel, G. (1996) A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J. Cell Biol., 135, 1457-1470.
28. Nachury, M.V., Maresca, T.J., Salmon, W.C., Waterman-Storer, C.M., Heald, R. and Weis, K. (2001) Importin β is a mitotic target of the small GTPase Ran in spindle assembly. Cell, 104, 95-106.
29. Nakielny, S., Shaikh, S., Burke, B. and Dreyfuss, G. (1999) Nup153 is an M9-containing mobile nucleoporin with a novel Ran-binding domain. EMBO J., 18, 1982-1995.
30. Ribbeck, K. and Görlich, D. (2001) Kinetic analysis of translocation through nuclear pore complexes. EMBO J., 20, 1320-1330.
31. Ribbeck, K., Lipowsky, G., Kent, H.M., Stewart, M. and Görlich, D. (1998) NTF2 mediates nuclear import of Ran. EMBO J., 17, 6587-6598.
32. Ribbeck, K., Kutay, U., Paraskeva, E. and Görlich, D. (1999) The translocation of transportin-cargo complexes through nuclear pores is independent of both Ran and energy. Curr. Biol., 9, 47-50.
33. Smith, A., Brownawell, A. and Macara, I.G. (1998) Nuclear import of ran is mediated by the transport factor NTF2. Curr. Biol., 8, 1403-1406.
34. Smith, A.E., Slepchenko, B.M., Schaff, J.C., Loew, L.M. and Macara, I.G. (2002) Systems analysis of Ran transport. Science, 295, 488-491.
35. Stryer, L. (1995) Biochemistry. 4th Edn. Freemann and Company, New York, NY, pp. 448.
36. Terasaki, M., Campagnola, P., Rolls, M.M., Stein, P.A., Ellenberg, J., Hinkle, B. and Slepchenko, B. (2001) A new model for nuclear envelope breakdown. Mol. Biol. Cell., 12, 503-510.
37. Villa Braslavsky, C.I., Nowak, C., Görlich, D., Wittinghofer, A. and Kuhlmann, J. (2000) Different structural and kinetic requirements for the interaction of ran with the ran-binding domains from RanBP2 and importin-β. Biochemistry, 39, 11629-11639.
38. Walther, T.C., Pickersgill, H.S., Cordes, V.C., Goldberg, M.W., Allen, T.D., Mattaj, I.W. and Fomerod, M. (2002) The cytoplasmic filaments of the nuclear pore complex are dispensable for selective nuclear protein import. J. Cell Biol., 158, 63-77.
39. Wiese, C., Wilde, A., Moore, M.S., Adam, S.A., Merdes, A. and Zheng, Y. (2001) Role of importin-β in coupling Ran to downstream targets in microtubule assembly. Science, 291, 653-656.
40. Weis, K. (2002) Nucleocytoplasmic transport: cargo trafficking across the border. Curr. Opin. Cell Biol., 14, 328-335.
41. Weis, K., Dingwall, C. and Lamond, A.I. (1996) Characterization of the nuclear protein import mechanism using Ran mutants with altered nucleotide binding specificities. EMBO J., 15, 7120-7128.
42. Yokoyama, N. et al. (1995) A giant nucleopore protein that binds Ran/TC4. Nature, 376, 184-188.
43. Zhang, C. and Clarke, P.R. (2000) Chromatin-independent nuclear envelope assembly induced by Ran GTPase in Xenopus egg extracts. Science, 288, 1429-1432.