Nuclear import of RPA in Xenopus egg extracts requires a novel protein XRIPα but not importin α

EMBO Journal

Volumn 18, Issue 15, 1999, Pages 4348-4358

  Jullien, Denis ^a   Görlich, Dirk ^b   Laemmli, Ulrich K ^c   Adachi, Yasuhisa ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Importin; Nuclear transport; Ran; RPA; XRIP

Indexed keywords

KARYOPHERIN; NUCLEOPLASMIN; PROTEIN SUBUNIT; RECOMBINANT PROTEIN; REPLICATION PROTEIN A;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN TRANSPORT; XENOPUS;

ALPHA KARYOPHERINS; AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CELL NUCLEUS; CLONING, MOLECULAR; DNA-BINDING PROTEINS; GTP-BINDING PROTEINS; HUMANS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; OVUM; RAN GTP-BINDING PROTEIN; RECOMBINANT FUSION PROTEINS; REPLICATION PROTEIN A; SEQUENCE HOMOLOGY, AMINO ACID; XENOPUS; XENOPUS PROTEINS;

ANIMALIA; EUKARYOTA; VERTEBRATA;

EID: 0345540684     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.15.4348     Document Type: Article

References (86)

1. Adachi, Y. and Laemmli, U.K. (1992) Identification of nuclear pre-replication centers poised for DNA synthesis in Xenopus egg extracts: immunolocalization study of replication protein A. J. Cell Biol., 119, 1-15.
2. Adachi, Y. and Laemmli, U.K. (1994) Study of the cell cycle-dependent assembly of the DNA pre-replication centers in Xenopus egg extracts. EMBO J., 13, 4153-4164.
3. + which encodes a 115-kD protein preferentially localized in the nucleus and its periphery. J. Cell Biol., 108, 1195-1207.
4. Adam, S.A., Marr, R.S. and Gerace, L. (1990) Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J. Cell Biol., 11 1, 807-816.
5. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402.
6. Bochkarev, A., Pfuetzner, R.A., Edwards, A.M. and Frappier, L. (1997) Structure of the single-stranded-DNA-binding domain of replication protein A bound to DNA. Nature, 385, 176-181.
7. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
8. Brill, S.J. and Stillman, B. (1991) Replication factor-A from Saccharomyces cerevisiae is encoded by three essential genes coordinately expressed at S phase. Genes Dev., 5, 1589-1600.
9. Chi, N.C., Adam, E.J.H., Visser, G.D. and Adam, S.A. (1996) RanBP1 stabilizes the interaction of Ran with p97 in nuclear protein import. J. Cell Biol., 135, 559-569.
10. Conti, E., Uy, M., Leighton, L., Blobel, G. and Kuriyan, J. (1998) Cryslallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin alpha. Cell, 94, 193-204.
11. Coutavas, E., Ren, M., Oppenheim, J.D., D'Eustachio, P. and Rush, M.G. (1993) Characterization of proteins that interact with the cell-cycle regulatory protein Ran/TC4. Nature, 366, 585-587.
12. Coverley, D., Kenny, M.K., Munn, M., Rupp, W.D., Lane, D.P. and Wood, R.D. (1991) Requirement for the replication protein SSB in human DNA excision repair. Nature, 349, 538-541.
13. Dingwall, C. and Laskey, R.A. (1991) Nuclear targeting sequences - a consensus? Trends Biochem. Sci., 16, 478-481.
14. Dornreiter, I., Erdile, L.F., Gilbert, I.U., von Winkler, D., Kelly, T.J. and Fanning, E. (1992) Interaction of DNA polymerase alpha-primase with cellular replication protein A and SV40 T antigen. EMBO J., 11, 769-776.
15. Dutta, A., Ruppert, J.M., Aster, J.C. and Winchester, E. (1993) Inhibition of DNA replication factor RPA by p53. Nature, 365, 79-82.
16. Erdile, L.F., Heyer, W.D., Kolodner, R. and Kelly, T.J. (1991) Characterization of a cDNA encoding the 70-kDa single-stranded DNA-binding subunit of human replication protein A and the role of the protein in DNA replication [published erratum appears in J. Biol. Chem., 1993 Jan 25; 268 (3): 2268]. J. Biol. Chem., 266, 12090-12098.
17. Fairman, M.P. and Stillman, B. (1988) Cellular factors required for multiple stages of SV40 DNA replication in vitro. EMBO J., 7, 1211-1218.
18. Fang, F. and Newport, J.W. (1993) Distinct roles of cdk2 and cdc2 in RP-A phosphorylation during the cell cycle. J. Cell Sci., 106, 983-994.
19. Fields, S. and Song, O. (1989) A novel genetic system to detect protein-protein interactions. Nature, 340, 245-246.
20. Finlay, D.R. and Forbes, D.J. (1990) Reconstitution of biochemically altered nuclear pores: transport can be eliminated and restored. Cell, 60, 17-29.
21. Fornerod, M., van Deursen, J., van Baal, S., Reynolds, A., Davis, D., Murti, K.G., Fransen, J. and Grosveld, G. (1997) The human homologue of yeast CRM1 is in a dynamic subcomplex with CAN/Nup214 and a novel nuclear pore component Nup88. EMBO J., 17, 807-816.
22. Gomes, X.V. and Wold, M.S. (1995) Structural analysis of human replication protein A. J. Biol. Chem., 270, 4534-4543.
23. Gomes, X.V., Henricksen, L.A. and Wold, M.S. (1996) Proteolytic mapping of human replication protein A: evidence for multiple structural domains and a conformational change upon interaction with single-stranded DNA. Biochemistry, 35, 5586-5595.
24. Görlich, D. and Mattaj, I.W. (1996) Nucleocytoplasmic transport. Science, 271, 1513-1518.
25. Görlich, 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.
26. Görlich, 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.
27. Görlich, D., Henklein, P., Laskey, R.A. and Hartman, E. (1996a) A 41 amino acid motif in importin-α confers binding to importin-β and hence transit into the nucleus. EMBO J., 15, 1810-1817.
28. Görlich, D., Pante, N., Kutay, U., Aebi, U. and Bishoff, F.R. (1996b) Identification of different roles for RanGDP and RanGTP in nuclear protein import. EMBO J., 15, 5584-5594.
29. Görlich, 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.
30. Harlow, E. and Lane, D. (1988) Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
31. Harper, J.W., Adami, G.R., Wei, N., Keyomarsi, K. and Elledge, S.J. (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell, 75, 805-816.
32. He, Z., Brinton, B.T., Greenblatt, J., Hassell, J.A. and Ingles, C.J. (1993) The transactivator proteins VP16 and GAL4 bind replication factor A. Cell, 73, 1223-1232.
33. He, Z., Henricksen, L.A., Wold, M.S. and Ingles, C.J. (1995) RPA involvement in the damage-recognition and incision steps of nucleotide excision repair. Nature, 376, 566-569.
34. Henderson, B.R. and Percipalle, P. (1997) Interactions between HIV Rev and nuclear import and export factors: the Rev nuclear localisation signal mediates specific binding to human importin-beta. J. Mol. Biol., 274, 693-707.
35. Henricksen, L.A., Umbricht, C.B. and Wold, M.S. (1994) Recombinant replication protein A: expression, complex formation and functional characterization. J. Biol. Chem., 15, 11121-11132.
36. Heyer, W.D., Rao, M.R., Erdile, L.F., Kelly, T.J. and Kolodner, R.D. (1990) An essential Saccharomyces cerevisiae single-stranded DNA binding protein is homologous to the large subunit of human RP-A. EMBO J., 9, 2321-2329.
37. Hovanessian, A.G., Galabru, J., Riviere, Y. and Montagnier, L. (1988) Efficiency of poly(A)·poly(U) as an adjuvant. Immunol. Today, 9, 161-162.
38. 3G-cap-specific nuclear import receptor with a novel domain structure. EMBO J., 17, 4114-4126.
39. Imamoto, N., Tachibana, J., Matsubae, M. and Yoneda, Y. (1995) A karyophilic protein forms a stable complex with cytoplasmic components prior to nuclear pore binding. J. Biol. Chem., 270, 8559-8565.
40. Ito, H., Fukuda, Y., Murata, K. and Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol., 153, 163-168.
41. Izaurralde, E., Kutay, U., von Kobbe, C., Mattaj, I.W. and Görlich, 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.
42. Jäkel, S. and Görlich, D. (1998) Importin beta, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J., 17, 4491-4502.
43. Kenny, M.K., Schlegel, U., Furneaux, H. and Hurwitz, J. (1990) The role of human single-stranded DNA binding protein and its individual subunits in simian virus 40 DNA replication. J. Biol. Chem., 265, 7693-7700.
44. Kim, C., Snyder, R.O. and Wold, M.S. (1992) Binding properties of replication protein A from human and yeast cells. Mol. Cell. Biol., 12, 3050-3059.
45. rcc1 and fluorescence measurements of their interaction. Biochemistry, 32, 11923-11928.
46. Klebe, C., Bishoff, F.R., Ponstingl, H. and Wittinghofer, A. (1995) Interaction of nuclear GTP-binding protein Ran with its regulatory proteins RCC1 and RanGAP1. Biochemistry, 34, 639-647.
47. Kutay, U., Izaurralde, E., Bischoff, F.R., Mattaj, I.W. and Görlich, D. (1997) Dominant-negative mutants of importin-β block multiple pathways of import and export through the nuclear pore complex. EMBO J., 16, 1153-1163.
48. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
49. Li, R. and Botchan, M.R. (1993) The acidic transcriptional activation domains of VP16 and p53 bind the cellular replication protein A and stimulate in vitro BPV-1 DNA replication. Cell, 73, 1207-1221.
50. Lin, Y.-L., Chen, C., Keshav, K.F., Winchester, E. and Dutta, A. (1996) Dissection of functional domains of the human DNA replication protein complex replication protein A. J. Biol. Chem., 271, 17190-17198.
51. Lin, Y.-L., Shivji, K.K., Chen, C., Kolodner, R., Wood, R.D. and Dutta, A. (1998) The evolutionarily conserved zinc finger motif in the largest subunit of human replication protein A is required for DNA replication and mismatch repair but not for nucleotide excision repair. J. Biol. Chem., 273, 1453-1461.
52. Longhese, M.P., Plevani, P. and Lucchini, G. (1994) Replication factor A is required in vivo for DNA replication, repair and recombination. Mol. Cell. Biol., 14, 7884-7890.
53. Maniar, H.S., Wilson, R. and Brill, S.J. (1997) Role of replication protein-A subunits 2 and 3 in DNA replication fork movement in Saccharomyces cerevisiae. Genetics, 145, 891-902.
54. Matsuda, R. et al. (1995) DNA repair protein XPA binds replication protein A (RPA). J. Biol. Chem., 270, 4152-4157.
55. Melchior, F. and Gerace, L. (1998) Two-way trafficking with Ran. Trends Cell Biol., 8, 175-179.
56. Melchior, F., Paschal, B., Evans, J. and Gerace, L. (1993) 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., 123, 1649-1659.
57. Miller, J.H. (1972) Experiments in Molecular Genetics, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
58. Miyamoto, Y., Imamoto, N., Sekimoto, T., Tachibana, T., Seki, T., Tada, S., Enomoto, T. and Yoneda, Y. (1997) Differential modes of nuclear localization signal (NLS) recognition by three distinct classes of NLS receptors. J. Biol. Chem., 272, 26375-26381.
59. Moore, J.D., Yang, J., Truant, R. and Kornbluth, S. (1999) Nuclear import of cdk/cyclin complexes: identification of distinct mechanisms for import of cdk2/cyclin E and cdc2/cyclin B1. J. Cell Biol., 144, 213-224.
60. 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.
61. Moore, M.S. and Blobel, G. (1994) A G protein involved in nucleocytoplasmic transport: the role of Ran. Trends Biochem. Sci., 19, 211-216.
62. Moore, S.P., Erdile, L., Kelly, T. and Fishel, R. (1991) The human homologous pairing protein HPP-1 is specifically stimulated by the cognate single-stranded binding protein hRP-A. Proc. Natl Acad. Sci. USA, 88, 9067-9071.
63. Murray, A.W. (1991) Cell cycle extracts. Methods Cell Biol., 36, 581-605.
64. New, J.H., Sugiyama, T., Zaitseva, E. and Kowalczykowski, S.C. (1998) Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature, 391, 407-410.
65. Palacios, I., Hetzer, M., Adam, S.A. and Mattaj, I.W. (1997) Nuclear import of U snRNPs requires importin β. EMBO J., 16, 6783-6792.
66. Palmeri, D. and Malim, M.H. (1999) Importin β can mediate the nuclear import of an arginine-rich nuclear localization signal in the absence of importin α. Mol. Cell. Biol, 19, 1218-1225.
67. Pfuetzner, R.A., Bochkarev, A., Frappier, L. and Edwards, A.M. (1997) Replication protein A. Characterization and crystallization of the DNA binding domain. J. Biol. Chem., 272, 430-434.
68. 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.
69. 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.
70. Rebagliati, M.R., Weeks, D.L., Harvey, R.P. and Melton, D.A. (1985) Identification and cloning of localized maternal RNAs from Xenopus eggs. Cell, 42, 769-777.
71. 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.
72. Rout, M.P., Blobel, G. and Aitchison, J.D. (1997) A distinct nuclear import pathway used by ribosomal proteins. Cell, 89, 715-725.
73. Santocanale, C., Neecke, H., Longhese, M.P., Lucchini, G. and Plevani, P. (1995) Mutations in the gene encoding the 34 kD subunit of yeast replication protein A cause defective S phase progression. J. Mol. Biol., 254, 595-607.
74. Schlenstedt, G., Smirnova, E., Deane, R., Solsbacher, J., Kutay, U., Görlich, D., Ponstingl, H. and Bischoff, F.R. (1997) Yrb4p, a yeast ran-GTP-binding protein involved in import of ribosomal protein L25 into the nucleus. EMBO J., 16, 6237-6249.
75. Shinohara, A., Shinohara, M., Ohta, T., Matsuda, S. and Ogawa, T. (1998) Rad52 forms ring structures and co-operates with RPA in single-strand DNA annealing. Genes Cells, 3, 145-156.
76. Smith, D.E. and Fisher, P.A. (1984) Identification, developmental regulation and response to heat shock of two antigenically related forms of a major nuclear envelope protein in Drosophila embryo: application of an improved method for affinity purification of antibodies using polypeptides immobilized on nitrocellulose blots. J. Cell Biol., 99, 20-28.
77. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res., 22, 4673-4680.
78. Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl Acad. Sci. USA, 76, 4350-4354.
79. Truant, R. and Cullen, B.R. (1999) The arginine-rich domains present in human immunodeficiency virus type 1 Tat and Rev function as direct importin β-dependent nuclear localization signals. Mol. Cell Biol., 19, 1210-1217.
80. + RNA binding protein. Mol. Cell. Biol., 18, 1449-1458.
81. Weis, K. (1998) Importins and exportins: how to get in and out the nucleus. Trends Biochem. Sci., 23, 185-189.
82. Weis, K., Ryder, U. and Lamond, A.I. (1996) The conserved amino-terminal domain of hSRP1a is essential for nuclear protein import. EMBO J., 15, 1818-1825.
83. Wold, M.S. (1997) Replication protein A: heteromeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem., 66, 61-92.
84. Wold, M.S. and Kelly, T. (1988) Purification and characterization of replication protein A, a cellular protein required for in vitro replication of simian virus 40 DNA. Proc. Natl Acad. Sci. USA, U S A, 85, 2523-2527.
85. Wold, M.S., Weinberg, D.H., Virshup, D.M., Li, J.J. and Kelly, T.J. (1989) Identification of cellular proteins required for simian virus 40 DNA replication. J. Biol. Chem., 264, 2801-2809.
86. Wozniak, R.W., Rout, M.P. and Aitchison, J.D. (1998) Karyopherins and kissing cousins. Trends Cell Biol., 8, 184-188.