The Nup358-RanGAP complex is required for efficient importin α/β-dependent nuclear import

Molecular Biology of the Cell

Volumn 19, Issue 5, 2008, Pages 2300-2310

  Hutten, Saskia ^a   Flotho, Annette ^a   Melchior, Frauke ^a   Kehlenbach, Ralph H ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; KARYOPHERIN ALPHA; KARYOPHERIN BETA; MEMBRANE PROTEIN; NUCLEOPORIN NUP358; PROTEIN RANBP1; PROTEIN RANGAP1; RAN PROTEIN; SUMO PROTEIN;

ANTIBODY INHIBITION METHOD; ARTICLE; CELL NUCLEUS MEMBRANE; COMPLEX FORMATION; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NUCLEAR IMPORT; NUCLEAR PORE; NUCLEAR PORE COMPLEX; NUCLEOCYTOPLASMIC TRANSPORT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; RNA INTERFERENCE; TECHNIQUE; VERTEBRATE;

ACTIVE TRANSPORT, CELL NUCLEUS; ALPHA KARYOPHERINS; ANIMALS; ANTIBODY SPECIFICITY; BETA KARYOPHERINS; CELL NUCLEUS; CELL SURVIVAL; GTPASE-ACTIVATING PROTEINS; HELA CELLS; HUMANS; MICE; MODELS, BIOLOGICAL; MOLECULAR CHAPERONES; NUCLEAR LOCALIZATION SIGNALS; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; SOLUBILITY;

VERTEBRATA;

EID: 48249150289     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-12-1279     Document Type: Article

References (58)

1. Allen, N. P., Huang, L., Burlingame, A., and Rexach, M. (2001). Proteomic analysis of nucleoporin interacting proteins. J. Biol. Chem. 276, 29268-29274.
2. Askjaer, P. et al. (1999). RanGTP-regulated interactions of CRM1 with nucleoporins and a shuttling DEAD-box helicase. Mol. Cell. Biol. 19, 6276-6285.
3. Baake, M., Bauerle, M., Doenecke, D., and Albig, W. (2001). Core histones and linker histones are imported into the nucleus by different pathways. Eur. J. Cell Biol. 80, 669-677.
4. Bernad, R., van der Velde, H., Fornerod, M., and Pickersgill, H. (2004). Nup358/RanBP2 attaches to the nuclear pore complex via association with Nup88 and Nup214/CAN and plays a supporting role in CRM1-mediated nuclear protein export. Mol. Cell. Biol. 24, 2373-2384.
5. Bischoff, F. R., and Görlich, D. (1997). RanBP1 is crucial for the release of RanGTP from importin beta-related nuclear transport factors. FEBS Lett. 419, 249-254.
6. Bischoff, F. R., Krebber, H., Smirnova, E., Dong, W., and Ponstingl, H. (1995). Co-activation of RanGTPase and inhibition of GTP dissociation by Ran-GTP binding protein RanBP1. EMBO J. 14, 705-715.
7. Charneau, P., Mirambeau, G., Roux, P., Paulous, S., Buc, H., and Clavel, F. (1994). HIV-1 reverse transcription. A termination step at the center of the genome. J. Mol. Biol. 241, 651-662.
8. Chi, N. C., Adam, E. J., Visser, G. D., and Adam, S. A. (1996). RanBP1 stabilizes the interaction of Ran with p97 nuclear protein import. J. Cell Biol. 135, 559-569.
9. Chi, N. C., and Adam, S. A. (1997). Functional domains in nuclear import factor p97 for binding the nuclear localization sequence receptor and the nuclear pore. Mol. Biol. Cell 8, 945-956.
10. Dargemont, C., and Kuhn, L. C. (1992). Export of mRNA from microinjected nuclei of Xenopus laevis oocytes. J. Cell Biol. 118, 1-9.
11. Delphin, C., Guan, T., Melchior, F., and Gerace, L. (1997). RanGTP Targets p97 to RanBP2, a filamentous protein localized at the cytoplasmic periphery of the nuclear pore complex. Mol. Biol. Cell 8, 2379-2390.
12. 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.
13. Fischer, U., Huber, J., Boelens, W. C., Mattaj, I. W., and Lührmann, R. (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.
14. Floer, M., Blobel, G., and Rexach, M. (1997). Disassembly of RanGTP-karyopherin beta complex, an intermediate in nuclear protein import. J. Biol. Chem. 272, 19538-19546.
15. Forler, D., Rabut, G., Ciccarelli, F. D., Herold, A., Kocher, T., Niggeweg, R., Bork, P., Ellenberg, J., and Izaurralde, E. (2004). RanBP2/Nup358 provides a major binding site for NXF1-p15 dimers at the nuclear pore complex and functions in nuclear mRNA export. Mol. Cell. Biol. 24, 1155-1167.
16. 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.
17. Freedman, N. D., and Yamamoto, K. R. (2004). Importin 7 and importin alpha/importin beta are nuclear import receptors for the glucocorticoid receptor. Mol. Biol. Cell 15, 2276-2286.
18. Fried, H., and Kutay, U. (2003). Nucleocytoplasmic transport: taking an inventory. Cell. Mol. Life Sci. 60, 1659-1688.
19. Fukuda, M., Asano, S., Nakamura, T., Adachi, M., Yoshida, M., Yanagida, M., and Nishida, E. (1997). CRM1 is responsible for intracellular transport mediated by the nuclear export signal. Nature 390, 308-311.
20. Gasteier, J. E., Madrid, R., Krautkramer, E., Schroder, S., Muranyi, W., Benichou, S., and Fackler, O. T. (2003). Activation of the Rac-binding partner FHOD1 induces actin stress fibers via a ROCK-dependent mechanism. J. Biol. Chem. 278, 38902-38912.
21. Görlich, D., Seewald, M. J., and Ribbeck, K. (2003). Characterization of Ran-driven cargo transport and the RanGTPase system by kinetic measurements and computer simulation. EMBO J. 22, 1088-1100.
22. Hu, T., Guan, T., and Gerace, L. (1996). Molecular and functional characterization of the p62 complex, an assembly of nuclear pore complex glycoproteins. J. Cell Biol. 134, 589-601.
23. Hutten, S., and Kehlenbach, R. H. (2006). Nup214 is required for CRM1-dependent nuclear protein export in vivo. Mol. Cell. Biol. 26, 6772-6785.
24. Kehlenbach, R. H., Assheuer, R., Kehlenbach, A., Becker, J., and Gerace, L. (2001). Stimulation of nuclear export and inhibition of nuclear import by a Ran mutant deficient in binding to Ran-binding protein 1. J. Biol. Chem. 276, 14524-14531.
25. Kehlenbach, R. H., Dickmanns, A., and Gerace, L. (1998). Nucleocytoplasmic shuttling factors including Ran and CRM1 mediate nuclear export of NFAT in vitro. J. Cell Biol. 141, 863-874.
26. Kehlenbach, R. H., Dickmanns, A., Kehlenbach, A., Guan, T., and Gerace, L. (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.
27. Kehlenbach, R. H., and Gerace, L. (2002). Analysis of nuclear protein import and export in vitro using fluorescent cargoes. Methods Mol. Biol. 189, 231-245.
28. Love, D. C., Sweitzer, T. D., and Hanover, J. A. (1998). Reconstitution of HIV-1 rev nuclear export: independent requirements for nuclear import and export. Proc. Natl. Acad. Sci. USA 95, 10608-10613.
29. 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.
30. 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.
31. Matunis, M. J., Wu, J., and Blobel, G. (1998). SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex. J. Cell Biol. 140, 499-509.
32. Melchior, F., Sweet, D. J., and Gerace, L. (1995). Analysis of Ran/TC4 function in nuclear protein import. Methods Enzymol. 257, 279-291.
33. Nachury, M. V., and Weis, K. (1999). The direction of transport through the nuclear pore can be inverted. Proc. Natl Acad Sci. USA 96, 9622-9627.
34. Ossareh-Nazari, B., Bachelerie, F., and Dargemont, C. (1997). Evidence for a role of CRM1 in signal-mediated nuclear protein export. Science 278, 141-144.
35. 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.
36. Pichler, A., Gast, A., Seeler, J. S., Dejean, A., and Melchior, F. (2002). The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell. 108, 109-120.
37. Rexach, M., and Blobel, G. (1995). Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell 83, 683-692.
38. Richards, S. A., Carey, K. L., and Macara, I. G. (1997). Requirement of guanosine triphosphate-bound ran for signal-mediated nuclear protein export. Science 276, 1842-1844.
39. Rose, A., and Meier, I. (2001). A domain unique to plant RanGAP is responsible for its targeting to the plant nuclear rim. Proc. Natl. Acad. Sci. USA 98, 15377-15382.
40. Sabri, N., Roth, P., Xylourgidis, N., Sadeghifar, F., Adler, J., and Samakovlis, C. (2007). Distinct functions of the Drosophila Nup153 and Nup214 FG domains in nuclear protein transport. J. Cell Biol. 178, 557-565.
41. Salina, D., Enarson, P., Rattner, J. B., and Burke, B. (2003). Nup358 integrates nuclear envelope breakdown with kinetochore assembly. J. Cell Biol. 162, 991-1001.
42. Schwoebel, E. D., Talcott, B., Cushman, I., and Moore, M. S. (1998). Ran-dependent signal-mediated nuclear import does not require GTP hydrolysis by Ran. J. Biol. Chem. 273, 35170-35175.
43. Shah, S., and Forbes, D. J. (1998). Separate nuclear import pathways converge on the nucleoporin Nup153 and can be dissected with dominant-negative inhibitors. Curr. Biol. 8, 1376-1386.
44. Stade, K., Ford, C. S., Guthrie, C., and Weis, K. (1997). Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 90, 1041-1050.
45. Stade, K., Vogel, F., Schwienhorst, I., Meusser, B., Volkwein, C., Nentwig, B., Dohmen, R. J., and Sommer, T. (2002). A lack of SUMO conjugation affects cNLS-dependent nuclear protein import in yeast. J. Biol. Chem. 277, 49554-49561.
46. Swaminathan, S., Kiendl, F., Korner, R., Lupetti, R., Hengst, L., and Melchior, F. (2004). RanGAP1*SUMO1 is phosphorylated at the onset of mitosis and remains associated with RanBP2 upon NPC disassembly. J. Cell Biol. 164, 965-971.
47. Tao, T., Lan, J., Lukacs, G. L., Hache, R. J., and Kaplan, F. (2006). Importin 13 regulates nuclear import of the glucocorticoid receptor in airway epithelial cells. Am. J. Respir. Cell. Mol. Biol. 35, 668-680.
48. Terry, L. J., and Wente, S. R. (2007). Nuclear mRNA export requires specific FG nucleoporins for translocation through the nuclear pore complex. J. Cell Biol. 178, 1121-1132.
49. Timney, B. L., Tetenbaum-Novatt, J., Agate, D. S., Williams, R., Zhang, W., Chait, B. T., and Rout, M. P. (2006). Simple kinetic relationships and nonspecific competition govern nuclear import rates in vivo. J. Cell Biol. 175, 579-593.
50. Tran, E. J., and Wente, S. R. (2006). Dynamic nuclear pore complexes: life on the edge. Cell 125, 1041-1053.
51. Walther, T. C., Pickersgill, H. S., Cordes, V. C., Goldberg, M. W., Allen, T. D., Mattaj, I. W., and Fornerod, M. (2002). The cytoplasmic filaments of the nuclear pore complex are dispensable for selective nuclear protein import. J. Cell Biol. 158, 63-77.
52. Weis, K. (2007). The nuclear pore complex: oily spaghetti or gummy bear? Cell 130, 405-407.
53. Wu, J., Matunis, M. J., Kraemer, D., Blobel, G., and Coutavas, E. (1995). Nup358, a cytoplasmically exposed nucleoporin with peptide repeats, Ran-GTP binding sites, zinc fingers, a cyclophilin A homologous domain, and a leucine-rich region. J. Biol. Chem. 270, 14209-14213.
54. Yang, W., and Musser, S. M. (2006). Nuclear import time and transport efficiency depend on importin beta concentration. J. Cell Biol. 174, 951-961.
55. Yaseen, N. R., and Blobel, G. (1999). GTP hydrolysis links initiation and termination of nuclear import on the nucleoporin nup358. J. Biol. Chem. 274, 26493-26502.
56. Yokoyama, N., Hayashi, N., Seki, T., Pante, N., Ohba, T., Nishii, K., Kuma, K., Hayashida, T., Miyata, T., Aebi, U., Fukui, M., and Nishimoto, T. (1995). A giant nucleopore protein that binds Ran/TC4. Nature 376, 184-188.
57. Yoneda, Y., Imamoto-Sonobe, N., Yamaizumi, M., and Uchida, T. (1987). Reversible inhibition of protein import into the nucleus by wheat germ agglutinin injected into cultured cells. Exp. Cell Res. 173, 586-595.
58. Zhang, H., Saitoh, H., and Matunis, M. J. (2002). Enzymes of the SUMO modification pathway localize to filaments of the nuclear pore complex. Mol. Cell. Biol. 22, 6498-6508.