Abstract
The Ran-GTPase cycle is important for nucleus-cytosol exchange of macromolecules and other nuclear processes. We employed the two-hybrid method to identify proteins interacting with Ran and the Ran GTP/GDP exchange factor. Using PRP20, encoding the Ran GTP/GDP exchange factor, we identified YRB1, previously identified as a protein able to interact with human Ran GTP/GDP exchange factor RCC1 in the two-hybrid system. Using GSP1, encoding the yeast Ran, as bait, we isolated YRB2. YRB2 encodes a protein containing a Ran-binding motif similar to that found in Yrb1p and Nup2p. Yrb1p is located in the cytosol whereas Nup2p is nuclear. Similar to Yrb1p, Yrb2p bound to GTP-Gsp1p but not to GDP-Gsp1p and enhanced the GTPase-activating activity of Rna1p. However, unlike Yrb1p, Yrb2p did not inhibit the nucleotide-releasing activity of Prp20p. While overproduction of Yrb1p inhibited the growth of a mutant possessing a PRP20 mutation (srm1-1) and suppressed the rna1-1 mutation, overproduction of Yrb2p showed no effect on the growth of these mutants. Disruption of YRB2 made yeast cold sensitive and was synthetically lethal with rna1-1 but not with nup2delta. Nuclear protein import and the mRNA export were normal in strains possessing mutations of YRB2. We propose that Yrb2p is involved in the nuclear processes of the Ran-GTPase cycle which are not related to nucleus-cytosol exchange of macromolecules.
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Selected References
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- Aebi M., Clark M. W., Vijayraghavan U., Abelson J. A yeast mutant, PRP20, altered in mRNA metabolism and maintenance of the nuclear structure, is defective in a gene homologous to the human gene RCC1 which is involved in the control of chromosome condensation. Mol Gen Genet. 1990 Oct;224(1):72–80. doi: 10.1007/BF00259453. [DOI] [PubMed] [Google Scholar]
- Amberg D. C., Fleischmann M., Stagljar I., Cole C. N., Aebi M. Nuclear PRP20 protein is required for mRNA export. EMBO J. 1993 Jan;12(1):233–241. doi: 10.1002/j.1460-2075.1993.tb05649.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Amberg D. C., Goldstein A. L., Cole C. N. Isolation and characterization of RAT1: an essential gene of Saccharomyces cerevisiae required for the efficient nucleocytoplasmic trafficking of mRNA. Genes Dev. 1992 Jul;6(7):1173–1189. doi: 10.1101/gad.6.7.1173. [DOI] [PubMed] [Google Scholar]
- Atkinson N. S., Dunst R. W., Hopper A. K. Characterization of an essential Saccharomyces cerevisiae gene related to RNA processing: cloning of RNA1 and generation of a new allele with a novel phenotype. Mol Cell Biol. 1985 May;5(5):907–915. doi: 10.1128/mcb.5.5.907. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Becker J., Melchior F., Gerke V., Bischoff F. R., Ponstingl H., Wittinghofer A. RNA1 encodes a GTPase-activating protein specific for Gsp1p, the Ran/TC4 homologue of Saccharomyces cerevisiae. J Biol Chem. 1995 May 19;270(20):11860–11865. doi: 10.1074/jbc.270.20.11860. [DOI] [PubMed] [Google Scholar]
- Belanger K. D., Kenna M. A., Wei S., Davis L. I. Genetic and physical interactions between Srp1p and nuclear pore complex proteins Nup1p and Nup2p. J Cell Biol. 1994 Aug;126(3):619–630. doi: 10.1083/jcb.126.3.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Belhumeur P., Lee A., Tam R., DiPaolo T., Fortin N., Clark M. W. GSP1 and GSP2, genetic suppressors of the prp20-1 mutant in Saccharomyces cerevisiae: GTP-binding proteins involved in the maintenance of nuclear organization. Mol Cell Biol. 1993 Apr;13(4):2152–2161. doi: 10.1128/mcb.13.4.2152. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bischoff F. R., Klebe C., Kretschmer J., Wittinghofer A., Ponstingl H. RanGAP1 induces GTPase activity of nuclear Ras-related Ran. Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2587–2591. doi: 10.1073/pnas.91.7.2587. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bischoff F. R., Krebber H., Kempf T., Hermes I., Ponstingl H. Human RanGTPase-activating protein RanGAP1 is a homologue of yeast Rna1p involved in mRNA processing and transport. Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1749–1753. doi: 10.1073/pnas.92.5.1749. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bischoff F. R., Krebber H., Smirnova E., Dong W., Ponstingl H. Co-activation of RanGTPase and inhibition of GTP dissociation by Ran-GTP binding protein RanBP1. EMBO J. 1995 Feb 15;14(4):705–715. doi: 10.1002/j.1460-2075.1995.tb07049.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bischoff F. R., Ponstingl H. Catalysis of guanine nucleotide exchange on Ran by the mitotic regulator RCC1. Nature. 1991 Nov 7;354(6348):80–82. doi: 10.1038/354080a0. [DOI] [PubMed] [Google Scholar]
- Bischoff F. R., Ponstingl H. Mitotic regulator protein RCC1 is complexed with a nuclear ras-related polypeptide. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10830–10834. doi: 10.1073/pnas.88.23.10830. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boeke J. D., LaCroute F., Fink G. R. A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet. 1984;197(2):345–346. doi: 10.1007/BF00330984. [DOI] [PubMed] [Google Scholar]
- Bogerd A. M., Hoffman J. A., Amberg D. C., Fink G. R., Davis L. I. nup1 mutants exhibit pleiotropic defects in nuclear pore complex function. J Cell Biol. 1994 Oct;127(2):319–332. doi: 10.1083/jcb.127.2.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boguski M. S., McCormick F. Proteins regulating Ras and its relatives. Nature. 1993 Dec 16;366(6456):643–654. doi: 10.1038/366643a0. [DOI] [PubMed] [Google Scholar]
- Cheng Y., Dahlberg J. E., Lund E. Diverse effects of the guanine nucleotide exchange factor RCC1 on RNA transport. Science. 1995 Mar 24;267(5205):1807–1810. doi: 10.1126/science.7534442. [DOI] [PubMed] [Google Scholar]
- Clark K. L., Ohtsubo M., Nishimoto T., Goebl M., Sprague G. F., Jr The yeast SRM1 protein and human RCC1 protein share analogous functions. Cell Regul. 1991 Oct;2(10):781–792. doi: 10.1091/mbc.2.10.781. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clark K. L., Sprague G. F., Jr Yeast pheromone response pathway: characterization of a suppressor that restores mating to receptorless mutants. Mol Cell Biol. 1989 Jun;9(6):2682–2694. doi: 10.1128/mcb.9.6.2682. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Corbett A. H., Koepp D. M., Schlenstedt G., Lee M. S., Hopper A. K., Silver P. A. Rna1p, a Ran/TC4 GTPase activating protein, is required for nuclear import. J Cell Biol. 1995 Sep;130(5):1017–1026. doi: 10.1083/jcb.130.5.1017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Coutavas E., Ren M., Oppenheim J. D., D'Eustachio P., Rush M. G. Characterization of proteins that interact with the cell-cycle regulatory protein Ran/TC4. Nature. 1993 Dec 9;366(6455):585–587. doi: 10.1038/366585a0. [DOI] [PubMed] [Google Scholar]
- Dasso M. RCC1 in the cell cycle: the regulator of chromosome condensation takes on new roles. Trends Biochem Sci. 1993 Mar;18(3):96–101. doi: 10.1016/0968-0004(93)90161-f. [DOI] [PubMed] [Google Scholar]
- DeGregori J., Russ A., von Melchner H., Rayburn H., Priyaranjan P., Jenkins N. A., Copeland N. G., Ruley H. E. A murine homolog of the yeast RNA1 gene is required for postimplantation development. Genes Dev. 1994 Feb 1;8(3):265–276. doi: 10.1101/gad.8.3.265. [DOI] [PubMed] [Google Scholar]
- Dickmanns A., Bischoff F. R., Marshallsay C., Lührmann R., Ponstingl H., Fanning E. The thermolability of nuclear protein import in tsBN2 cells is suppressed by microinjected Ran-GTP or Ran-GDP, but not by RanQ69L or RanT24N. J Cell Sci. 1996 Jun;109(Pt 6):1449–1457. doi: 10.1242/jcs.109.6.1449. [DOI] [PubMed] [Google Scholar]
- Dingwall C., Kandels-Lewis S., Séraphin B. A family of Ran binding proteins that includes nucleoporins. Proc Natl Acad Sci U S A. 1995 Aug 1;92(16):7525–7529. doi: 10.1073/pnas.92.16.7525. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Drivas G. T., Shih A., Coutavas E., Rush M. G., D'Eustachio P. Characterization of four novel ras-like genes expressed in a human teratocarcinoma cell line. Mol Cell Biol. 1990 Apr;10(4):1793–1798. doi: 10.1128/mcb.10.4.1793. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Durfee T., Becherer K., Chen P. L., Yeh S. H., Yang Y., Kilburn A. E., Lee W. H., Elledge S. J. The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev. 1993 Apr;7(4):555–569. doi: 10.1101/gad.7.4.555. [DOI] [PubMed] [Google Scholar]
- Fleischmann M., Clark M. W., Forrester W., Wickens M., Nishimoto T., Aebi M. Analysis of yeast prp20 mutations and functional complementation by the human homologue RCC1, a protein involved in the control of chromosome condensation. Mol Gen Genet. 1991 Jul;227(3):417–423. doi: 10.1007/BF00273932. [DOI] [PubMed] [Google Scholar]
- Forrester W., Stutz F., Rosbash M., Wickens M. Defects in mRNA 3'-end formation, transcription initiation, and mRNA transport associated with the yeast mutation prp20: possible coupling of mRNA processing and chromatin structure. Genes Dev. 1992 Oct;6(10):1914–1926. doi: 10.1101/gad.6.10.1914. [DOI] [PubMed] [Google Scholar]
- Gietz R. D., Sugino A. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene. 1988 Dec 30;74(2):527–534. doi: 10.1016/0378-1119(88)90185-0. [DOI] [PubMed] [Google Scholar]
- Guan K. L., Dixon J. E. Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal Biochem. 1991 Feb 1;192(2):262–267. doi: 10.1016/0003-2697(91)90534-z. [DOI] [PubMed] [Google Scholar]
- Hagan I. M., Hyams J. S. The use of cell division cycle mutants to investigate the control of microtubule distribution in the fission yeast Schizosaccharomyces pombe. J Cell Sci. 1988 Mar;89(Pt 3):343–357. doi: 10.1242/jcs.89.3.343. [DOI] [PubMed] [Google Scholar]
- Harper J. W., Adami G. R., Wei N., Keyomarsi K., Elledge S. J. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell. 1993 Nov 19;75(4):805–816. doi: 10.1016/0092-8674(93)90499-g. [DOI] [PubMed] [Google Scholar]
- Hartmann E., Görlich D. A Ran-binding motif in nuclear pore proteins. Trends Cell Biol. 1995 May;5(5):192–193. doi: 10.1016/s0962-8924(00)88992-8. [DOI] [PubMed] [Google Scholar]
- Hayashi N., Yokoyama N., Seki T., Azuma Y., Ohba T., Nishimoto T. RanBP1, a Ras-like nuclear G protein binding to Ran/TC4, inhibits RCC1 via Ran/TC4. Mol Gen Genet. 1995 Jun 25;247(6):661–669. doi: 10.1007/BF00290397. [DOI] [PubMed] [Google Scholar]
- Hill J. E., Myers A. M., Koerner T. J., Tzagoloff A. Yeast/E. coli shuttle vectors with multiple unique restriction sites. Yeast. 1986 Sep;2(3):163–167. doi: 10.1002/yea.320020304. [DOI] [PubMed] [Google Scholar]
- Hill J., Donald K. A., Griffiths D. E., Donald G. DMSO-enhanced whole cell yeast transformation. Nucleic Acids Res. 1991 Oct 25;19(20):5791–5791. doi: 10.1093/nar/19.20.5791. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hopper A. K., Banks F. A yeast mutant which accumulates precursor tRNAs. Cell. 1978 Jun;14(2):211–219. doi: 10.1016/0092-8674(78)90108-3. [DOI] [PubMed] [Google Scholar]
- Hopper A. K., Traglia H. M., Dunst R. W. The yeast RNA1 gene product necessary for RNA processing is located in the cytosol and apparently excluded from the nucleus. J Cell Biol. 1990 Aug;111(2):309–321. doi: 10.1083/jcb.111.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hutchison H. T., Hartwell L. H., McLaughlin C. S. Temperature-sensitive yeast mutant defective in ribonucleic acid production. J Bacteriol. 1969 Sep;99(3):807–814. doi: 10.1128/jb.99.3.807-814.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ichihara Y., Kurosawa Y. Construction of new T vectors for direct cloning of PCR products. Gene. 1993 Aug 16;130(1):153–154. doi: 10.1016/0378-1119(93)90361-6. [DOI] [PubMed] [Google Scholar]
- Kadowaki T., Goldfarb D., Spitz L. M., Tartakoff A. M., Ohno M. Regulation of RNA processing and transport by a nuclear guanine nucleotide release protein and members of the Ras superfamily. EMBO J. 1993 Jul;12(7):2929–2937. doi: 10.1002/j.1460-2075.1993.tb05955.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Koepp D. M., Wong D. H., Corbett A. H., Silver P. A. Dynamic localization of the nuclear import receptor and its interactions with transport factors. J Cell Biol. 1996 Jun;133(6):1163–1176. doi: 10.1083/jcb.133.6.1163. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Loeb J. D., Davis L. I., Fink G. R. NUP2, a novel yeast nucleoporin, has functional overlap with other proteins of the nuclear pore complex. Mol Biol Cell. 1993 Feb;4(2):209–222. doi: 10.1091/mbc.4.2.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matsumoto T., Beach D. Premature initiation of mitosis in yeast lacking RCC1 or an interacting GTPase. Cell. 1991 Jul 26;66(2):347–360. doi: 10.1016/0092-8674(91)90624-8. [DOI] [PubMed] [Google Scholar]
- Matsuzaki H., Nakajima R., Nishiyama J., Araki H., Oshima Y. Chromosome engineering in Saccharomyces cerevisiae by using a site-specific recombination system of a yeast plasmid. J Bacteriol. 1990 Feb;172(2):610–618. doi: 10.1128/jb.172.2.610-618.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Melchior F., Guan T., Yokoyama N., Nishimoto T., Gerace L. GTP hydrolysis by Ran occurs at the nuclear pore complex in an early step of protein import. J Cell Biol. 1995 Nov;131(3):571–581. doi: 10.1083/jcb.131.3.571. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Melchior F., Paschal B., Evans J., Gerace L. 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. 1993 Dec;123(6 Pt 2):1649–1659. doi: 10.1083/jcb.123.6.1649. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Melchior F., Weber K., Gerke V. 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. 1993 Jun;4(6):569–581. doi: 10.1091/mbc.4.6.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mitchell D. A., Marshall T. K., Deschenes R. J. Vectors for the inducible overexpression of glutathione S-transferase fusion proteins in yeast. Yeast. 1993 Jul;9(7):715–722. doi: 10.1002/yea.320090705. [DOI] [PubMed] [Google Scholar]
- Moore M. S., Blobel G. The GTP-binding protein Ran/TC4 is required for protein import into the nucleus. Nature. 1993 Oct 14;365(6447):661–663. doi: 10.1038/365661a0. [DOI] [PubMed] [Google Scholar]
- Moreland R. B., Langevin G. L., Singer R. H., Garcea R. L., Hereford L. M. Amino acid sequences that determine the nuclear localization of yeast histone 2B. Mol Cell Biol. 1987 Nov;7(11):4048–4057. doi: 10.1128/mcb.7.11.4048. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nishimoto T., Eilen E., Basilico C. Premature of chromosome condensation in a ts DNA- mutant of BHK cells. Cell. 1978 Oct;15(2):475–483. doi: 10.1016/0092-8674(78)90017-x. [DOI] [PubMed] [Google Scholar]
- Nishiwaki K., Hayashi N., Irie S., Chung D. H., Harashima S., Oshima Y. Structure of the yeast HIS5 gene responsive to general control of amino acid biosynthesis. Mol Gen Genet. 1987 Jun;208(1-2):159–167. doi: 10.1007/BF00330437. [DOI] [PubMed] [Google Scholar]
- Noguchi E., Hayashi N., Azuma Y., Seki T., Nakamura M., Nakashima N., Yanagida M., He X., Mueller U., Sazer S. Dis3, implicated in mitotic control, binds directly to Ran and enhances the GEF activity of RCC1. EMBO J. 1996 Oct 15;15(20):5595–5605. [PMC free article] [PubMed] [Google Scholar]
- Ohba T., Seki T., Azuma Y., Nishimoto T. Premature chromatin condensation induced by loss of RCC1 is inhibited by GTP- and GTPgammaS-Ran, but not GDP-Ran. J Biol Chem. 1996 Jun 21;271(25):14665–14667. doi: 10.1074/jbc.271.25.14665. [DOI] [PubMed] [Google Scholar]
- Ouspenski I. I., Mueller U. W., Matynia A., Sazer S., Elledge S. J., Brinkley B. R. Ran-binding protein-1 is an essential component of the Ran/RCC1 molecular switch system in budding yeast. J Biol Chem. 1995 Feb 3;270(5):1975–1978. doi: 10.1074/jbc.270.5.1975. [DOI] [PubMed] [Google Scholar]
- Parent S. A., Fenimore C. M., Bostian K. A. Vector systems for the expression, analysis and cloning of DNA sequences in S. cerevisiae. Yeast. 1985 Dec;1(2):83–138. doi: 10.1002/yea.320010202. [DOI] [PubMed] [Google Scholar]
- Ren M., Drivas G., D'Eustachio P., Rush M. G. Ran/TC4: a small nuclear GTP-binding protein that regulates DNA synthesis. J Cell Biol. 1993 Jan;120(2):313–323. doi: 10.1083/jcb.120.2.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sazer S., Nurse P. A fission yeast RCC1-related protein is required for the mitosis to interphase transition. EMBO J. 1994 Feb 1;13(3):606–615. doi: 10.1002/j.1460-2075.1994.tb06298.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sazer S. The search for the primary function of the Ran GTPase continues. Trends Cell Biol. 1996 Mar;6(3):81–85. doi: 10.1016/0962-8924(96)80992-5. [DOI] [PubMed] [Google Scholar]
- Schlenstedt G., Saavedra C., Loeb J. D., Cole C. N., Silver P. A. The GTP-bound form of the yeast Ran/TC4 homologue blocks nuclear protein import and appearance of poly(A)+ RNA in the cytoplasm. Proc Natl Acad Sci U S A. 1995 Jan 3;92(1):225–229. doi: 10.1073/pnas.92.1.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schlenstedt G., Wong D. H., Koepp D. M., Silver P. A. Mutants in a yeast Ran binding protein are defective in nuclear transport. EMBO J. 1995 Nov 1;14(21):5367–5378. doi: 10.1002/j.1460-2075.1995.tb00221.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tachibana T., Imamoto N., Seino H., Nishimoto T., Yoneda Y. Loss of RCC1 leads to suppression of nuclear protein import in living cells. J Biol Chem. 1994 Oct 7;269(40):24542–24545. [PubMed] [Google Scholar]
- Tanaka K., Matsumoto K., Toh-e A. Dual regulation of the expression of the polyubiquitin gene by cyclic AMP and heat shock in yeast. EMBO J. 1988 Feb;7(2):495–502. doi: 10.1002/j.1460-2075.1988.tb02837.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tani T., Derby R. J., Hiraoka Y., Spector D. L. Nucleolar accumulation of poly (A)+ RNA in heat-shocked yeast cells: implication of nucleolar involvement in mRNA transport. Mol Biol Cell. 1995 Nov;6(11):1515–1534. doi: 10.1091/mbc.6.11.1515. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Traglia H. M., O'Connor J. P., Tung K. S., Dallabrida S., Shen W. C., Hopper A. K. Nucleus-associated pools of Rna1p, the Saccharomyces cerevisiae Ran/TC4 GTPse activating protein involved in nucleus/cytosol transit. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7667–7672. doi: 10.1073/pnas.93.15.7667. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Van Hoy M., Leuther K. K., Kodadek T., Johnston S. A. The acidic activation domains of the GCN4 and GAL4 proteins are not alpha helical but form beta sheets. Cell. 1993 Feb 26;72(4):587–594. doi: 10.1016/0092-8674(93)90077-4. [DOI] [PubMed] [Google Scholar]
- Winston F., Chumley F., Fink G. R. Eviction and transplacement of mutant genes in yeast. Methods Enzymol. 1983;101:211–228. doi: 10.1016/0076-6879(83)01016-2. [DOI] [PubMed] [Google Scholar]
- Wu J., Matunis M. J., Kraemer D., Blobel G., Coutavas E. 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. 1995 Jun 9;270(23):14209–14213. doi: 10.1074/jbc.270.23.14209. [DOI] [PubMed] [Google Scholar]
- Yokoyama N., Hayashi N., Seki T., Panté N., Ohba T., Nishii K., Kuma K., Hayashida T., Miyata T., Aebi U. A giant nucleopore protein that binds Ran/TC4. Nature. 1995 Jul 13;376(6536):184–188. doi: 10.1038/376184a0. [DOI] [PubMed] [Google Scholar]
