Monoclonal antibodies to NTF2 inhibit nuclear protein import by preventing nuclear translocation of the GTPase Ran

Molecular Biology of the Cell

Volumn 11, Issue 2, 2000, Pages 703-719

  Steggerda, Susanne M ^a   Black, Ben E ^a   Paschal, Bryce M ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; CYCLOHEXIMIDE; DIGITONIN; GUANOSINE TRIPHOSPHATASE; MONOCLONAL ANTIBODY; NUCLEAR PROTEIN; NUCLEAR TRANSPORT FACTOR 2; RAN PROTEIN; STREPTAVIDIN; UNCLASSIFIED DRUG;

ANTIBODY COMBINING SITE; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL NUCLEUS MEMBRANE; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN TRANSPORT; XENOPUS;

EID: 0033999820     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.11.2.703     Document Type: Article

References (55)

1. Adam, E.J., and Adam, S.A. (1994). Identification of cytosolic factors required for nuclear location sequence-mediated binding to the nuclear envelope. J. Cell Biol. 125, 547-555.
2. Adam, S.A., and Gerace, L. (1991). Cytosolic proteins that specifically bind nuclear location signals are receptors for nuclear import. Cell 66, 837-847.
3. Adam, S.A., Sterne-Marr, R.E., and Gerace, L. (1990). Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J. Cell Biol. 111, 807-816.
4. Bischoff, F.R., and Ponstingl, H. (1991). Mitotic regulator protein RCC1 is complexed with a nuclear ras-related polypeptide. Proc. Natl. Acad. Sci. USA 88, 10830-10834.
5. Black, B.E., Lévesque, L., Holaska, J.M., Wood, T.C., and Paschal, B.M. (1999). Identification of an NTF2-related factor that binds Ran-GTP and regulates nuclear protein export. Mol. Cell. Biol. 19, 8616-8624.
6. Carey, K.L., Richards, S.A., Lounsbury, K.M., and Macara, I.G. (1996). Evidence using a green fluorescent protein-glucocorticoid receptor chimera that the Ran/TC4 GTPase mediates an essential function independent of nuclear protein import. J. Cell Biol. 133, 985-996.
7. Chi, N.C., Adam, E.J., and Adam, S.A. (1995). Sequence and characterization of cytoplasmic nuclear protein import factor p97. J. Cell Biol. 130, 265-274.
8. Clarkson, W.D., Corbett, A.H., Paschal, B.M., Kent, H.M., McCoy, A., Gerace, L., Silver, P., and Stewart, M. (1997). Nuclear protein import is decreased by engineered mutants of nuclear transport factor 2 (NTF2) that do not bind GDP-Ran. J. Mol. Biol. 272, 716-730.
9. Clarkson, W.D., Kent, H.M., and Stewart, M. (1996). Separate binding sites on nuclear transport factor 2 (NTF2) for GDP-Ran and the phenylalanine-rich repeat regions of nucleoporins p62 and Nsp1p. J. Mol. Biol. 263, 517-524.
10. Cole, C.N., and Hammell, C.M. (1998). Nucleocytoplasmic transport - driving and directing transport. Curr. Biol. 8, R368-R372.
11. Corbett, A.M., and Silver, P.A. (1996). The NTF2 gene encodes an essential, highly conserved protein that functions in nuclear transport in vivo. J. Biol. Chem. 271, 18477-18484.
12. Feldherr, C., Akin, D., and Moore, M.S. (1998). The nuclear import factor p10 regulates the functional size of the nuclear pore complex during oogenesis. J. Cell Sci. 111, 1889-1896.
13. Fornerod, M., Ohno, M., Yoshida, M., and Mattaj, I.W. (1997). Crm1 is an export receptor for leucine-rich nuclear export signals. Cell 90, 1051-1060.
14. Goldfarb, D.S., Gariepy, J., Schoolnik, G., and Kornberg, R.D. (1986). Synthetic peptides as nuclear location signals. Nature 326, 641-644.
15. Gorlich, D., Dabrowski, M., Bischoff, F.R., Kutay, U., Bork, P., Hartmann, E., Prehn, S., and Izaurralde, E. (1997). A novel class of RanGTP binding proteins. J. Cell Biol. 138, 65-80.
16. Gorlich, D., Kostka, S., Kraft, R., Dingwall, C., Laskey, R.A., Hartmann, E., and Prehn, S. (1995). Two different subunits of importin cooperate to recognize nuclear localization signals and bind them to the nuclear envelope. Curr. Biol. 5, 383-392.
17. Gorlich, D., Pante, N., Kutay, U., Aebi, U., and Bischoff, F.R. (1996). Identification of different roles for RanGDP and RanGTP in nuclear protein import. EMBO J. 15, 5584-5594.
18. Gorlich, D., Prehn, S., Laskey, R.A., and Hartmann, E. (1994). Isolation of a protein that is essential for the first step of nuclear protein import. Cell 79, 767-778.
19. Hopper, A.K., Traglia, H.M., and Dunst, R.W. (1990). The yeast RNA1 gene product necessary for RNA processing is located in the cytosol and apparently excluded from the nucleus. J. Cell Biol. 111, 309-321.
20. Hu, W., and Jans, D.A. (1999). Efficiency of importin α/β-mediated nuclear localization sequence recognition and nuclear import. J. Biol. Chem. 274, 15820-15827.
21. Imamoto, N., Shimamoto, T., Takao, T., Tachibana, T., Kose, S., Matsubae, M., Sekimoto, T., Shimonishi, Y., and Yoneda, Y. (1995). In vivo evidence for involvement of a 58 kDa component of nuclear pore-targeting complex in nuclear protein import. EMBO J. 14, 3617-3626.
22. Izaurralde, E., Kutay, U., Vonkobbe, C., Mattaj, I.W., and Gorlich, D. (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.
23. Kose, S., Imamoto, N., Tachibana, T., Shimamoto, T., and Yoneda, Y. (1997). Ran-unassisted nuclear migration of a 97-kDa component of the nuclear pore-targeting complex. J. Cell Biol. 139, 841-849.
24. Kose, S., Imamoto, N., Tachibana, T., Yoshida, M., and Yoneda, Y. (1999). Beta-subunit of nuclear pore-targeting complex (importin-beta) can be exported from the nucleus in a Ran-independent manner. J. Biol. Chem. 274, 3946-3952.
25. Lam, M.H.C., Briggs, L.J., Hu, W., Martin, T.J., Gillespie, M.T., and Jans, D.A. (1999). Importin β recognizes parathyroid hormone-related protein with high affinity and mediates its nuclear import in the absence of importin α. J. Biol. Chem. 274, 7391-7398.
26. Mattaj, I.W., and Englmeier, L. (1998). Nucleocytoplasmic transport - the soluble phase. Annu. Rev. Biochem. 67, 265-306.
27. Melchior, F., Guan, T., Yokoyama, N., Nishimoto, T., and Gerace, L. (1995). GTP hydrolysis by Ran occurs at the nuclear pore complex in an early step of protein import. J. Cell Biol. 131, 571-581.
28. Melchior, F., Paschal, B., Evans, J., and Gerace, L. (1993a). Inhibition of nuclear protein import by nonhydrolyzable analogues of GTP and identification of the small GTPase Ran/TC4 as an essential transport factor. J. Cell Biol. 223, 1649-1659.
29. Melchior, F., Weber, K., and Gerke, V. (1993b). A functional homologue of the RNA1 gene product in Schizosaccharomyces pombe: purification, biochemical characterization, and identification of a leucine-rich repeat motif. Mol. Biol. Cell. 4, 569-581.
30. Michael, W.M., Eder, P.S., and Dreyfuss, G. (1997). The K nuclear shuttling domain: a novel signal for nuclear import and nuclear export in the hnRNP K protein. EMBO J. 16, 3587-3598.
31. Moore, M.S., and Blobel, G. (1993). The GTP-binding protein Ran/TC4 is required for protein import into the nucleus. Nature 365, 661-663.
32. Moore, M.S., and Blobel, G. (1994). Purification of a Ran-interacting protein that is required for protein import into the nucleus. Proc. Natl. Acad. Sci., USA 91, 10212-10216.
33. Moroianu, J., Hijikata, M., Blobel, G., and Radu, A. (1995). Mammalian karyopherin alpha 1 beta and alpha 2 beta heterodimers: alpha 1 or alpha 2 subunit binds nuclear localization signal and beta subunit interacts with peptide repeat-containing nucleoporins. Proc. Natl. Acad. Sci. USA 92, 6532-6536.
34. Nakielny, S., and Dreyfuss, G. (1997). Import and export of the nuclear protein import receptor transportin by a mechanism independent of GTP hydrolysis. Curr. Biol. 8, 89-95.
35. Nehrbass, U., and Blobel, G. (1996). Role of the nuclear transport factor p10 in nuclear import. Science 272, 120-122.
36. Nigg, E.A. (1997). Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature 386, 779-787.
37. Ohtsubo, M., et al. (1987). Isolation and characterization of the active cDNA of the human cell cycle gene (RCC1) involved in the regulation of onset of chromosome condensation. Genes Dev. 1, 585-593.
38. Paschal, B.M., Delphin, C., and Gerace, L. (1996). Nucleotide-specific interaction of Ran/TC4 with nuclear transport factors NTF2 and p97. Proc. Natl. Acad. Sci. USA 93, 7679-7683.
39. Paschal, B.M., Fritze, C., Guan, T., and Gerace, L. (1997). High levels of the GTPase Ran/TC4 relieve the requirement for nuclear protein transport factor 2. J. Biol. Chem. 272, 21534-21539.
40. Paschal, B.M., and Gerace, L. (1995). Identification of NTF2, a cytosolic factor for nuclear import that interacts with nuclear pore complex protein p62. J. Cell Biol. 129, 925-937.
41. Pollard, V.W., Michael, W.M., Nakielny, S., Siomi, M.C., Wang, F., and Dreyfuss, G. (1996). A novel receptor-mediated nuclear protein import pathway. Cell 86, 985-994.
42. Radu, A., Blobel, G., and Moore, M.S. (1995). Identification of a protein complex that is required for nuclear protein import and mediates docking of import substrate to distinct nucleoporins. Proc. Natl. Acad. Sci. USA 92, 1769-1773.
43. Ren, M., Drivas, G., D'Eustachio, P., and Rush, M.G. (1993). Ran/TC4: a small nuclear GTP-binding protein that regulates DNA synthesis. J. Cell Biol. 120, 313-323.
44. Ribbeck, K., Lipowsky, G., Kent, H.M., Stewart, M., and Gorlich, D. (1998). NTF2 mediates nuclear import of Ran. EMBO J. 17, 6587-6598.
45. Scheffzek, K., Klebe, C., Fritz-Wolf, K., Kabsch, W., and Wittinghofer, A. (1995). Crystal structure of the nuclear Ras-related protein Ran in its GDP-bound form. Nature 374, 378-381.
46. Siomi, H., and Dreyfuss, G. (1995). A nuclear localization domain in the hnRNP A1 protein. J. Cell Biol. 129, 551-560.
47. 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.
48. Snow, C.M., Senior, A., and Gerace, L. (1987). Monoclonal antibodies identify a group of nuclear pore complex glycoproteins. J. Cell. Biol. 104, 1143-1156.
49. Stewart, M., Kent, H.M., and McCoy, A.J. (1998). Structural basis for molecular recognition between nuclear transport factor 2 (NTF2) and the GDP-bound form of the Ras-family GTPase Ran. J. Mol. Biol. 277, 635-646.
50. Tachibana, T., Hieda, M., Sekimoto, T., and Yoneda, Y. (1996). Exogenously injected nuclear import factor p10/NTF2 inhibits signal-mediated nuclear import and export of proteins in living cells. FEBS Lett. 397, 177-182.
51. Tachibana, T., Imamoto, N., Seino, H., Nishimoto, T., and Yoneda, Y. (1994). Loss of RCC1 leads to suppression of nuclear protein import in living cells. J. Biol. Chem. 269, 24542-24545.
52. Vetter, I.R., Nowak, C., Nishimoto, T., Kuhlmann, J., and Wittinghofer, A. (1999). Structure of a Ran-binding domain complexed with Ran bound to a GTP analogue: implications for nuclear transport. Nature 398, 39-46.
53. Wilkinson, M.G., and Millar, J.B. (1998). SAPKs and transcription factors do the nucleocytoplasmic tango. Genes Dev. 12, 1391-1397.
54. Wong, D.H., Corbett, A.H., Kent, H.M., Stewart, M., and Silver, P.A. (1997). Interaction between the small GTPase Ran/Gsp1p and Ntf2p is required for nuclear transport. Mol. Cell. Biol. 17, 3755-3767.
55. Yamada, M., Tachibana, T., Imamoto, N., and Yoneda, Y. (1998). Nuclear transport factor p10/NTF2 functions as a Ran-GDP dissociation inhibitor (Ran-GDI). Curr. Biol. 8, 1339-1342.