Dbp5, a DEAD-box protein required for mRNA export, is recruited to the cytoplasmic fibrils of nuclear pore complex via a conserved interaction with CAN/Nup159p

EMBO Journal

Volumn 18, Issue 15, 1999, Pages 4332-4347

  Schmitt, Christel ^a   Von Kobbe, Cayetano ^a   Bachi, Angela ^b   Panté, Nelly ^c   Rodrigues, João P ^d   Boscheron, Cécile ^a   Rigaut, Guillaume ^b   Wilm, Matthias ^b   Séraphin, Bertrand ^b   Carmo Fonseca, Maria ^d   Izaurralde, Elisa ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c ETH ZURICH   (Switzerland)

^d INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

Author keywords

DEAD box protein; Nuclear pore complex; RNA helicase; RNA nuclear export

Indexed keywords

ADENOSINE TRIPHOSPHATASE; COMPLEMENTARY DNA; MESSENGER RNA; MUTANT PROTEIN; NUCLEOPORIN; RNA BINDING PROTEIN;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; IMMUNOELECTRON MICROSCOPY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RNA TRANSPORT; TEMPERATURE; XENOPUS;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; BIOLOGICAL TRANSPORT; CLONING, MOLECULAR; CONSERVED SEQUENCE; CYTOPLASM; DEAD-BOX RNA HELICASES; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEAR ENVELOPE; NUCLEAR PORE COMPLEX PROTEINS; NUCLEAR PROTEINS; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; RNA HELICASES; RNA, MESSENGER; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 0033517108     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.15.4332     Document Type: Article

References (65)

1. Askjaer, P. et al. (1999) RanGTP-regulated interactions of CRM1 with nucleoporins and a shuttling DEAD-box helicase. Mol. Cell. Biol., in press.
2. Belgareh, N., Snay-Hodge, C., Pasteau, F., Dagher, S., Cole, C. and Doye, V. (1998) Functional characterization of a Nup159p-containing nuclear pore subcomplex. Mol. Biol. Cell., 9, 3475-3492.
3. 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.
4. Boer, J.M., Van Deursen, J.M.A., Croes, H.J., Fransen, J.A.M. and Grosveld, G.C. (1997) The nucleoporin CAN/Nup214 binds to both the cytoplasmic and the nucleoplasmic sides of the nuclear pore complex in overexpressing cells. Exp. Cell Res., 232, 182-185.
5. Boer, J.M, Bonten-Surtel, J. and Grosveld, G. (1998) Overexpression of the nucleoporin CAN/Nup214 induces growth arrest, nucleocytoplasmic transport defects, and apoptosis. Mol. Cell. Biol., 18, 1236-1247.
6. Chang, T.-H., Arenas, J. and Abelson, J. (1990) Identification of five putative yeast RNA helicase genes. Proc. Natl Acad. Sci. USA, 87, 1571-1575.
7. Cho, H.-S., Ha, N.-C., Kang, L.-W., Chung, K.M., Back, S.H., Jang, S.K. and Oh, B.-H. (1998) Crytal structure of RNA helicase from genotype 1b hepatitis C virus. J. Biol. Chem., 273, 15045-15052.
8. Daneholt, B. (1997) A look at messenger RNP moving through the nuclear pore. Cell, 88, 585-588.
9. de la Cruz, J., Kressler, D. and Linder, P. (1999) Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families. Trends Biochem. Sci., 24, 192-198.
10. Del Priore, V., Heath, C.V., Snay-Hodge, C.A., MacMillan, A., Gorsch, L.C., Dagher, S. and Cole, C.N. (1997) A structure/function analysis of Rat7p/Nup159p, an essential nucleoporin of Saccharomyces cerevisiae. J. Cell Sci., 110, 2987-2999.
11. Dignam, J., Lebowitz, R. and Roeder, R. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from mammalian nuclei. Nucleic Acids Res., 11, 1475-1589.
12. Fahrenkrog, B., Hurt, E., Aebi, U. and Panté, N. (1998) Molecular architecture of the yeast nuclear pore complex: localization of Nsp1p subcomplexes. J. Cell Biol., 143, 577-588.
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. Fornerod, M. et al. (1995) Relocation of the carboxyterminal part of CAN from the nuclear envelope to the nucleus as a result of leukemia-specific chromosome rearrangements. Oncogene, 10, 1739-1748.
15. Fornerod, M., Ohno, M., Yoshida, M. and Mattaj, I.W. (1997a) CRM1 is an export receptor for leucine-rich nuclear export signals. Cell, 90, 1051-1060.
16. Fornerod, M., Vandeursen, J., van Baal, S., Reynolds, A., Davis, D., Gopal Murti, K., Fransen, J. and Grosveld, G. (1997b) The human homologue of yeast Crm1 is in a dynamic subcomplex with CAN/Nup214 and a novel nuclear pore component Nup88. EMBO J., 16, 807-816.
17. Fuller-Pace, F.V. (1994) RNAs helicases: modulators of RNA structure. Trends Cell Biol., 4, 271-274.
18. Gorbalenya, A.E. and Koonin, E.V. (1994) Helicases: amino acid sequence comparisons and structure-function relationships. Curr. Opin. Struct. Biol., 3, 419-429.
19. Gorsch, L.C., Dockendorff, T.C. and Cole, C.N. (1995) A conditional allele of a novel repeat containing yeast nucleoporin Rat7/Nup159 causes both rapid cessation of mRNA export and reversible clustering in nuclear pore complexes. J. Cell. Biol., 4, 939-955.
20. Grüter, P., Tabernero, C., von Kobbe, C., Schmitt, C., Saavedra, C., Bachi, A., Wilm, M., Felber, B.K. and Izaurralde, E. (1998) TAP, the human homologue of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol. Cell, 1, 649-659.
21. Hamm, J. and Mattaj, I.W. (1990) Monomethylated cap structures facilitate RNA export from the nucleus. Cell, 63, 109-118.
22. Hurwitz, M.E., Strambio-de-Castillia, C. and Blobel, G. (1998) Two yeast nuclear pore complex proteins involved in mRNA export from cytoplasmically oriented subcomplex. Proc. Natl Acad. Sci. USA, 95, 11242-11245.
23. Jarmolowski, A., Boelens, W., Izaurralde, E. and Mattaj, I.W. (1994) Nuclear export of different classes of RNA is mediated by specific factors. J. Cell Biol., 124, 627-635.
24. Katahira, J., Strasser, K., Podtelejnikov, A., Mann, M., Jung, J.U. and Hurt, E. (1999) The Mex67p-mediated nuclear mRNA export pathway is conserved from yeast to human. EMBO J., 18, 2593-2609.
25. 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.
26. Kim, J.L., Morgenstern, K.A., Griffith, J.P., Dwyer, M.D., Thomson, J.A., Murcko, M.A., Lin, C. and Caron, P.R. (1998) Hepatitis C virus NS3 RNA helicase domain with a bound oligonucleotide: the crystal structure provides insights into the mode of unwinding. Structure, 6, 89-100.
27. Kraemer, D., Wozniak, R.W., Blobel, G. and Radu, A. (1994) The human CAN protein, a putative oncogene product associated with myeloid leukemogenesis, is a nuclear pore complex protein that faces the cytoplasm. Proc. Natl Acad. Sci. USA, 91, 1519-1523.
28. Kraemer, D.M., Strambio-de-Castillia, C., Blobel, G. and Rout, M.P. (1995) The essential yeast nucleoporin NUP159 is located on the cytoplasmic side of the nuclear pore complex and serves in karyopherin-mediated binding of transport substrate. J. Biol. Chem., 270, 19017-19021.
29. Linder, P., Lasko, P.F., Ashburner, M., Leroy, P., Nielsen, P.J., Nishi K. and Slonimski, P. (1989) Birth of the D-E-A-D box. Nature, 337, 121-122.
30. Lorsch, J.R. and Herschlag, D. (1998a) The DEAD box protein eIF4A. 1. A minimal kinetic and thermodynamic framework reveals coupled binding of RNA and nucleotide. Biochemistry, 37, 2180-2193.
31. Lorsch, J.R. and Herschlag, D. (1998b) The DEAD box protein eIF4A. 2. A cycle of nucleotide and RNA-dependent conformational changes. Biochemistry, 37, 2194-2206.
32. Mann, M. and Wilm, M. (1994) Error-tolerant identification of peptides in sequence databases by peptide sequence tags. Anal. Chem., 66, 4390-4399.
33. Neville, M., Stutz, F., Lee, L., Davis, L.I. and Rosbash, M. (1997) The importin-β family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export. Curr. Biol., 7, 767-775.
34. Panté, N. and Aebi, U. (1996) Import ligand complexes sequentially bind to two distinct nucleopore sites before translocation into the nucleus. Science, 273, 1729-1732.
35. Panté, N., Bastos, R., McMorrow, I., Burke, B. and Aebi, U. (1994) Interactions and three-dimensional localization of a group of pore complex proteins. J. Cell Biol., 126, 603-617.
36. Paraskeva, E., Izaurralde, E., Bischoff, F.R., Huber, J., Kutay, U., Hartmann, E., Lührmann, R. and Görlich, D. (1999) CRM1-mediated recycling of snurportin 1 to the cytoplasm. J. Cell Biol., 145, 255-264.
37. Parks, T.D., Leuther, K.K., Howard, E.D., Johnston, S.A. and Dougherty, W.G. (1994) Release of proteins and peptides from fusion proteins with a recombinant plant virus proteinase. Anal. Biochem., 216, 413-417.
38. Pasquinelli, A.E., Ernst, R.K., Lund, E., Grimm, C., Zapp, M.L., Rekosh, D., Hammarskjold, M.-L. and Dahlberg, J.E. (1997) The constitutive transport element (CTE) of Mason-Pfizer monkey virus (MPMV) accesses an RNA export pathway utilized by cellular messenger RNAs. EMBO J., 16, 7500-7510.
39. Pause, A., Méthot, N. and Sonenberg, N. (1993) The HRIGRXXR region of the DEAD box RNA helicase eukaryotic initiation factor 4A is required for RNA binding and ATP hydrolysis. Mol. Cell Biol., 13, 6789-6798.
40. Pause, A., Méthot, N., Svitkin, Y., Merrick, W.C. and Sonenberg, N. (1994) Dominant negative mutants of mammalian translation initiation factor eIF-4A define a critical role for eIF-4A in cap-dependent and cap-independent initiation of translation. EMBO J., 13, 1205-1215.
41. Portman, D.S., O'Connor, P. and Dreyfuss, G. (1997) YRA1, an essential Saccharomyces cerevisiae gene, encodes a novel nuclear protein with RNA annealing activity. RNA, 3, 527-537.
42. Puig, O., Rutz, B., Luukkonen, B.G., Kandels-Lewis, S., Bragado-Nilsson, E. and Séraphin, B. (1998) New constructs and strategies for efficient PCR-based manipulations in yeast. Yeast, 14, 1139-1146
43. Rogers, G.W., Richter, N.J. and Merrick, W.C. (1999) Biochemical and kinetic characterization of the RNA helicase activity of eukaryotic initiation factor 4A. J. Biol. Chem., 274, 12236-12244.
44. Rozen, F., Pelletier, J., Trachel, H. and Sonenberg, N. (1989) A lysine substitution in the ATP binding site of eucaryotic initiation factor 4A abrogates nucleotides binding activity. Mol. Cell. Biol., 9, 4061-4063.
45. Rozen, F., Edery, I., Meerovitch, K., Dever, T.E., Merrick, W.C. and Sonenberg, N. (1990) Bidirectional RNA helicase activity of eukaryotic translation initiation factors 4A and 4E. Mol. Cell. Biol., 10, 1134-1144.
46. Saavedra, C., Felber, B.K. and Izaurralde, E. (1997) The simian retrovirus-1 constitutive transport element (CTE), unlike HIV-1 RRE, utilises factors required for cellular RNA export. Curr. Biol., 7, 619-628.
47. Schmid, S.R. and Linder, P. (1992) D-E-A-D protein family of putative RNA helicase. Mol. Microbiol., 6, 283-291.
48. Shevchenko, A., Wilm, M., Vorm, O. and Mann, M. (1996) Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem., 68, 850-858.
49. Snay-Hodge, C.A., Colot, H.V., Goldstein, A.L. and Cole, C.N. (1998) Dbp5p/Rat8p is a yeast nuclear pore-associated DEAD-box protein essential for RNA export. EMBO J., 17, 2663-2676.
50. Staley, J.P. and Guthrie, C. (1999) An RNA switch at the 5′ splice site requires ATP and the DEAD box protein Prp28p. Mol. Cell, 3, 55-64.
51. Subramanya, H.S., Bird, L.E., Brannigan, J.A. and Wigley, D.B. (1996) Crystal structure of a DExx box helicase. Nature. 384, 379-383.
52. Turner, D.H., Sugimoto, N. and Freier, S.M. (1988) RNA structure prediction. Annu. Rev. Biophys. Chem., 17, 167-192.
53. + RNA export. EMBO J., 17, 2651-2662.
54. 2 arrest and impaired nucleocytoplasmic transport in mouse embryos lacking the proto-oncogene CAN/Nup214. EMBO J., 15, 5574-5583.
55. Vankan, P., McGuigan, C. and Mattaj, I.W. (1992) Domains of U4 and U6 snRNAs required for snRNP assembly and splicing complementation in Xenopus oocytes. EMBO J., 11, 335-342.
56. Velankar, S.S., Soultanas, P., Dillinham, M.S., Subramanya, H.S. and Wigley, D.B. (1999) Crystal structure of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell, 97, 75-84.
57. Von Lindern, M., Fornerod, M., van Baal, S., Jaegle, M., de Wit, T., Bings, A. and Grosveld, G. (1992) The translocation (6;9), associated with a specific subtype of acute myeloid leukemia, results in the fusion of two genes, dek and can, and the expression of a chimeric, leukemia-specific dek-can mRNA. Mol. Cell. Biol., 12, 1687-1697.
58. Vorm, O., Roepstorff, P. and Mann, M. (1994) Improved resolution and very high sensitivity in MALDI TOF of matrix surfaces made by fast evaporation. Anal. Chem., 66, 3281-3287.
59. Wach, A., Brachat, A., Alberti-Segui, C., Rebischung, C. and Philippsen, P. (1997) Heterologous HIS3 marker and GFP reporter modules for PCR-targeting in Saccharomyces cerevisiae. Yeast, 13, 1065-1075.
60. Walker, J.E., Saraste, M., Runswick, M.J. and Gay, N.J. (1982) Distantly related sequences in the α-and β-subunits of ATP synthetase, myosin kinases and other enzymes requiring a common nucleotide binding fold. EMBO J., 1, 945-951.
61. Wang, Y. and Guthrie, C. (1998) PRP16, a DEAH-box RNA helicase, is recruited to the spliceosome primarily via its nonconserved N-terminal domain. RNA, 4, 1216-1229.
62. Wilm, M. and Mann, M. (1996) Analytical properties of the nano electrospray ion source. Anal. Chem., 66, 1-8.
63. Wilm, M., Shevchenko, A., Houthaeve, T., Breit, S., Schweigerer, L., Fotsis, T. and Mann, M. (1996) Femtomole sequencing of proteins from polyacrylamide gels by nano electrospray mass spectrometry. Nature, 379, 466-469.
64. Yao, N., Hessen, T., Cable, M., Hong, Z., Kwong, A.D., Le, H.V. and Weber, P.C. (1997) Structure of the hepatitis C virus RNA helicase domain. Nature Struct. Biol., 4, 463-467.
65. Yokoyama, N. et al. (1995) RanBP2, a giant nuclear pore protein which binds Ran/TC4. Nature, 376, 184-188.