Transport routes through the nuclear pore complex

Current Opinion in Cell Biology

Volumn 10, Issue 3, 1998, Pages 392-399

  Pemberton, Lucy F ^a   Blobel, Günter ^a   Rosenblum, Jonathan S ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; GUANOSINE TRIPHOSPHATASE;

CELL NUCLEUS MEMBRANE; CYTOPLASM; HUMAN; MEMBRANE TRANSPORT; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; REVIEW; SEQUENCE HOMOLOGY;

EID: 0031861932     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(98)80016-1     Document Type: Article

References (69)

1. Corbett AH, Silver PA. Nucleocytoplasmic transport of macromolecules. Microbiol Mol Biol Rev. 61:1997;193-211.
2. Yokoyama N, Hayashi N, Seki T, Pante N, Ohba T, Nishii K, Kuma K, Hayashida T, Miyata T, Aebi U, et al. A giant nucleopore protein that binds Ran/TC4. Nature. 376:1995;184-188.
3. Wu J, Matunis MJ, 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. 270:1995;14209-14213.
4. Doye V, Hurt E. From nucleoporins to nuclear pore complexes. Curr Opin Cell Biol. 9:1997;401-411.
5. Aitchison JD, Blobel G, Rout MP. Kap104p: a karyopherin involved in the nuclear transport of messenger RNA binding proteins. Science. 274:1996;624-627.
6. Kohler M, Ansieau S, Prehn S, Leutz A, Haller H, Hartmann E. Cloning of two novel human importin-alpha subunits and analysis of the expression pattern of the importin-alpha protein family. FEBS Lett. 417:1997;104-108.
7. Nachury MV, Ryder UW, Lamond AI, Weis K. Cloning and characterization of hSRP1γ, a tissue-specific nuclear transport factor. Proc Natl Acad Sci USA. 95:1998;582-587.
8. Gallay P, Hope T, Chin D, Trono D. HIV-1 infection of nondividing cells through the recognition of integrase by the importin/karyopherin pathway. Proc Natl Acad Sci USA. 94:1997;9825-9830.
9. Fischer N, Kremmer E, Lautscham G, Mueller-Lantzsch N, Grasser FA. Epstein-Barr virus nuclear antigen 1 forms a complex with the nuclear transporter karyopherin alpha2. J Biol Chem. 272:1997;3999-4005.
10. Nadler SG, Tritschler D, Haffar OK, Blake J, Bruce AG, Cleaveland JS. Differential expression and sequence-specific interaction of karyopherin alpha with nuclear localization sequences. J Biol Chem. 272:1997;4310-4315.
11. Sekimoto T, Imamoto N, Nakajima K, Hirano T, Yoneda Y. Extracellular signal-dependent nuclear import of Stat1 is mediated by nuclear pore-targeting complex formation with NPI-1, but not Rch1. of special interest EMBO J. 16:1997;7067-7077 Stat1, which does not appear to have a conventional NLS, is shown to interact with karyopherin α1, but not α2, in vitro and only antibodies to α1 block its import. The interaction between a1 and Stat1 could not be competed with SV40 large T antigen - NLS, suggesting that α1 has at least two distinct substrate-binding sites.
12. Henderson BR, Percipalle P. 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. 274:1997;693-707.
13. Palacios I, Hetzer M, Adam SA, Mattaj IW. Nuclear import of U snRNPs requires importin beta. EMBO J. 16:1997;6783-6792.
14. Fornerod M, van Deursen J, van Baal S, Reynolds A, Davis D, Murti KG, Fransen J, Grosveld G. The human homologue of yeast CRM1 is in a dynamic subcomplex with CAN/Nup214 and a novel nuclear pore component Nup88. of outstanding interest EMBO J. 16:1997;807-816 The existence of a large family of proteins related to karyopherin β1 was first suggested. Crm1, a member of this family, was shown to bind to Nup214 and to shuttle into and out of the nucleus.
15. + which encodes a 115-kD protein preferentially localized in the nucleus and its periphery. J Cell Biol. 108:1989;1195-1207.
16. Nishi K, Yoshida M, Fujiwara D, Nishikawa M, Horinouchi S, Beppu T. Leptomycin B targets a regulatory cascade of crm1, a fission yeast nuclear protein, involved in control of higher order chromosome structure and gene expression. J Biol Chem. 269:1994;6320-6324.
17. Wolff B, Sanglier JJ, Wang Y. Leptomycin B is an inhibitor of nuclear export: inhibition of nucleo-cytoplasmic translocation of the human immunodeficiency virus type 1 (HIV-1) Rev protein and Rev-dependent mRNA. of outstanding interest Chem Biol. 4:1997;139-147 In a screen for small molecules that could interfere with the nuclear export of Rev, leptomycin B was identified. Leptomycin B was shown to affect RevNES export but not NLS protein import.
18. of special interest Fornerod M, Ohno M, Yoshida M, Mattaj IW. CRM1 is an export receptor for leucine-rich nuclear export signals. of outstanding interest Cell. 90:1997;1051-1060 Xenopus Crm1 was shown to bind cooperatively to NES and RanGTP. Over-expression of Crm1 overcame leptomycin B action. One of several papers that showed that Crm1 mediates nuclear export of NES-containing proteins. Distinguishing features of these papers are listed in the individual annotations. See also Fukuda, 1997 [19], Kudo, 1997 [20], Ossareh-Nazari, 1997 [22], Stade, 1997 [23].
19. Fukuda M, Asano S, Nakamura T, Adachi M, Yoshida M, Yanagida M, Nishida E. CRM1 is responsible for intracellular transport mediated by the nuclear export signal. of outstanding interest Nature. 390:1997;308-311 Crm1 was identified from Xenopus cytosol as a protein able to bind immobilized NES in a leptomycin B-sensitive manner. Recombinant human Crm1 was shown to bind directly to wild-type NES but not to mutant NES.
20. Kudo N, Khochbin S, Nishi K, Kitano K, Yanagida M, Yoshida M, Horinouchi S. Molecular cloning and cell cycle-dependent expression of mammalian CRM1, a protein involved in nuclear export of proteins. of special interest J Biol Chem. 272:1997;29742-29751 A mutation in Crm1 in S. pombe was shown to affect the export of an NES reporter. Transcription of Crm1 varies during the cell cycle although protein levels remain constant.
21. Neville M, Stutz F, Lee L, Davis LI, Rosbash M. The importin-beta family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export. of special interest Curr Biol. 7:1997;767-775 The interactions between several nucleoporins and β karyophenins were studied by two-hybrid assays. Three viable crm1 mutant yeast strains were analyzed that showed a decrease in Rev activity but no mRNA-export defect.
22. Ossareh-Nazari B, Bachelerie F, Dargemont C. Evidence for a role of CRM1 in signal-mediated nuclear protein export. of outstanding interest Science. 278:1997;141-144 Interactions between human Crm1 and an NES-containing protein, 1κBα, were studied in reticulocyte lysates. A novel export assay using semipermeabilized cells was developed to characterize the export of NES-containing proteins.
23. Stade K, Ford CS, Guthrie C, Weis K. Exportin 1 (Crm1p) is an essential nuclear export factor. of outstanding interest Cell. 90:1997;1041-1050 A temperature-sensitive mutant of CRM1 was generated. Using a creative export assay in live yeast, strains harboring this mutant accumulated a shuttling NES/NLS-reporter in the nucleus at the restrictive temperature. Defects in mRNA export were also seen in this strain.
24. Boche I, Fanning E. Nucleocytoplasmic recycling of the nuclear localization signal receptor alpha subunit in vivo is dependent on a nuclear export signal, energy, and RCC1. of special interest J Cell Biol. 139:1997;313-325 The recycling of karyopherin α2 was characterized using microinjection into living cells.
25. Moroianu J, Blobel G, Radu A. RanGTP-mediated nuclear export of karyopherin alpha involves its interaction with the nucleoporin Nup153. of special interest Proc Natl Acad Sci USA. 94:1997;9699-9704 An interaction between karyopherin α2 and Nup153 was identified. The interacting domains were mapped and peptides representing these domains inhibited RanGTP-mediated export of endogenous karyopherin α from nuclei in the permeabilized-cell assay.
26. Izaurralde E, Kutay U, von Kobbe C, Mattaj IW, Gorlich D. The asymmetric distribution of the constituents of the Ran system is essential for transport into and out of the nucleus. of special interest EMBO J. 16:1997;6535-6547 Injection of RanGAP into Xenopus nuclei inhibited RNA export. Co-injection of hydrolysis-deficient Ran restored export.
27. Richards SA, Carey KL, Macara IG. Requirement of guanosine triphosphate-bound Ran for signal-mediated nuclear protein export. of special interest Science. 276:1997;1842-1844 Microinjection of Ran mutants into mammalian cell lines was seen to affect nuclear export. The effects of other Ran modulators were also characterized to further define the role of RanGTP in NES-mediated protein export.
28. Schneiter R, Kadowaki T, Tartakoff AM. mRNA transport in yeast: time to reinvestigate the functions of the nucleolus. Mol Biol Cell. 6:1995;357-370.
29. Kutay U, Bischoff FR, Kostka S, Kraft R, Görlich D. Export of importin α from the nucleus is mediated by a specific nuclear transport factor. of special interest Cell. 90:1997;1061-1071 CAS and karyopherin α were isolated with an immobilized, GTP hydrolysis-deficient Ran mutant. Addition of recombinant CAS, but not of karyopherins β1 or β2, led to the export of nuclear karyopherin α in a permeabilized-cell assay. See also Görlich 1996 [31], for an alternative pathway for karyopherin α export.
30. Bischoff FR, Gorlich D. RanBP1 is crucial for the release of RanGTP from importin beta-related nuclear transport factors. FEBS Lett. 419:1997;249-254.
31. Görlich D, Kraft R, Kostka S, Vogel F, Hartmann E, Laskey RA, Mattaj IW, Izaurralde E. Importin provides a link between nuclear protein import and U snRNA export. Cell. 87:1996;21-32.
32. Iovine MK, Wente SR. A nuclear export signal in Kap95p is required for both recycling the import factor and interaction with the nucleoporin GLFG repeat regions of Nup116p and Nup100p. of special interest J Cell Biol. 137:1997;797-811 Kap95p bound Nup100p and Nup116p via a leucine-rich domain that could act as an NES. Mutation of the NES inhibited recycling, causing accumulation of Kap95p in the nucleus.
33. Richards SA, Lounsbury KM, Carey KL, Macara IG. A nuclear export signal is essential for the cytosolic localization of the Ran binding protein, RanBP1. J Cell Biol. 134:1996;1157-1168.
34. Pollard VW, Michael WM, Nakielny S, Siomi MC, Wang F, Dreyfuss G. A novel receptor-mediated nuclear protein import pathway. Cell. 86:1996;985-994.
35. Fridell RA, Truant R, Thorne L, Benson RE, Cullen BR. Nuclear import of hnRNP A1 is mediated by a novel cellular cofactor related to karyopherin-beta. J Cell Sci. 110:1997;1325-1331.
36. Bonifaci N, Moroianu J, Radu A, Blobel G. Karyopherin beta2 mediates nuclear import of a mRNA binding protein. Proc Natl Acad Sci USA. 94:1997;5055-5060.
37. Siomi MC, Eder PS, Kataoka N, Wan L, Liu Q, Dreyfuss G. Transportin-mediated nuclear import of heterogeneous nuclear RNP proteins. J Cell Biol. 138:1997;1181-1192.
38. Michael WM, Choi M, Dreyfuss G. A nuclear export signal in hnRNP A1: a signal-mediated, temperature-dependent nuclear protein export pathway. Cell. 83:1995;415-422.
39. Rosenblum JS, Pemberton LF, Blobel G. A nuclear import pathway for a protein involved in tRNA maturation. of outstanding interest J Cell Biol. 139:1997;1655-1661 A complex containing Kap108p (Sxm1p), Lhp1p and three ribosomal proteins was purified from yeast cytosol. A new nuclear import pathway for Lhp1p, mediated by Kap108p, was characterized.
40. Pemberton LF, Rosenblum JS, Blobel G. A distinct and parallel pathway for the nuclear import of an mRNA- binding protein. of outstanding interest J Cell Biol. 139:1997;1645-1653 A new import pathway for mRNA-binding proteins was discovered. Kap111p (Mtr10p) was shown to mediate the import of the mRNA-binding protein, Npl3p. In a Kap111p-deletion strain, Npl3p is mislocalized, but Kap104p import substrates are not, suggesting that the new import pathway mediated by Kap111p is independent of the Kap104p pathway.
41. Rout MP, Blobel G, Aitchison JD. A distinct nuclear import pathway used by ribosomal proteins. of outstanding interest Cell. 89:1997;715-725 Kap123p was identified on the basis of homology with Kap95p and co-enrichment with the nuclear pore complex. This karyopherin was shown to be able to bind many ribosomal proteins and was suggested to be the major ribosomal import pathway in yeast. Overexpression of another karyopherin, Kap121p, was able to partially complement deletion of Kap123p.
42. Lee MS, Henry M, Silver PA. A protein that shuttles between the nucleus and the cytoplasm is an important mediator of RNA export. Genes Dev. 10:1996;1233-1246.
43. Kadowaki T, Chen S, Hitomi M, Jacobs E, Kumagai C, Liang S, Schneiter R, Singleton D, Wisniewska J, Tartakoff AM. Isolation and characterization of Saccharomyces cerevisiae mRNA transport-defective (mtr) mutants. J Cell Biol. 126:1994;649-659.
44. Yoo CJ, Wolin SL. The yeast La protein is required for the 3′ endonucleolytic cleavage that matures tRNA precursors. Cell. 89:1997;393-402.
45. Seedorf M, Silver PA. Importin/karyopherin protein family members required for mRNA export from the nucleus. Proc Natl Acad Sci USA. 94:1997;8590-8595.
46. Görlich D, Dabrowski M, Bischoff FR, Kutay U, Bork P, Hartmann E, Prehn S, Izaurralde E. A novel class of RanGTP binding proteins. J Cell Biol. 138:1997;65-80.
47. Schlenstedt G, Smirnova E, Deane R, Solsbacher J, Kutay U, Gorlich D, Ponstingl H, Bischoff FR. Yrb4p, a yeast Ran-GTP-binding protein involved in import of ribosomal protein L25 into the nucleus. of special interest EMBO J. 16:1997;6237-6249 RanGTP, but not RanGDP, is shown to disassociate both Kap123p and Pse1p from Rpl25p.
48. Yaseen NR, Blobel G. Cloning and characterization of human karyopherin beta3. Proc Natl Acad Sci USA. 94:1997;4451-4456.
49. Deane R, Schafer W, Zimmermann HP, Mueller L, Görlich D, Prehn S, Ponstingl H, Bischoff FR. Ran-binding protein 5 (RanBP5) is related to the nuclear transport factor importin-beta but interacts differently with RanBP1. Mol Cell Biol. 17:1997;5087-5096.
50. Simos G, Tekotte H, Grosjean H, Segref A, Sharma K, Tollervey D, Hurt EC. Nuclear pore proteins are involved in the biogenesis of functional tRNA. EMBO J. 15:1996;2270-2284.
51. Rexach M, Blobel G. Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell. 83:1995;683-692.
52. Floer M, Blobel G. The nuclear transport factor karyopherin beta binds stoichiometrically to Ran-GTP and inhibits the Ran GTPase activating protein. J Biol Chem. 271:1996;5313-5316.
53. Floer M, Blobel G, Rexach M. Disassembly of RanGTP-karyopherin beta complex, an intermediate in nuclear protein import. of special interest J Biol Chem. 272:1997;19538-19546 Karyopherin α and RanBP1 are shown to be capable of disassembling the RanGTP/karyopherin β complex.
54. Pu RT, Dasso M. The balance of RanBP1 and RCC1 is critical for nuclear assembly and nuclear transport. Mol Biol Cell. 8:1997;1955-1970.
55. Bischoff FR, 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. 14:1995;705-715.
56. 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. 247:1995;661-669.
57. Delphin C, Guan T, Melchior F, Gerace L. RanGTP targets p97 to RanBP2, a filamentous protein localized at the cytoplasmic periphery of the nuclear pore complex. of special interest Mol Biol Cell. 8:1997;2379-2390 By blot overlay on isolated nuclear envelopes, RanGTP, but not RanGDP, was shown to lead to the exclusive interaction between karyopherin β1 and Nup358. Also, by electron microscopy of nuclear envelopes, RanGTP, but not RanGDP, was shown to lead to the redistribution of karyopherin β1 from both sides of the NPC to only the cytoplasmic side, on the cytoplasmic fibrils.
58. Mahajan R, Delphin C, Guan T, Gerace L, Melchior F. A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell. 88:1997;97-107.
59. Matunis MJ, Coutavas E, Blobel G. 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. 135:1996;1457-1470.
60. Saitoh H, Pu R, Cavenagh M, Dasso M. RanBP2 associates with Ubc9p and a modified form of RanGAP1. Proc Natl Acad Sci USA. 94:1997;3736-3741.
61. Nehrbass U, Blobel G. Role of the nuclear transport factor p10 in nuclear import. Science. 272:1996;120-122.
62. Clarkson WD, Corbett AH, Paschal BM, Kent HM, McCoy AJ, Gerace L, Silver PA, Stewart M. Nuclear protein import is decreased by engineered mutants of nuclear transport factor 2 (NTF2) that do not bind GDP-Ran. J Mol Biol. 272:1997;716-730.
63. Wong DH, Corbett AH, Kent HM, Stewart M, Silver PA. Interaction between the small GTPase Ran/Gsp1p and Ntf2p is required for nuclear transport. Mol Cell Biol. 17:1997;3755-3767.
64. Paschal BM, Fritze C, Guan T, Gerace L. High levels of the GTPase Ran/TC4 relieve the requirement for nuclear protein transport factor 2. J Biol Chem. 272:1997;21534-21539.
65. Feldherr C, Akin D. The location of the transport gate in the nuclear pore complex. of outstanding interest J Cell Sci. 110:1997;3065-3070 11 nm-27 nm PEG-gold particles were shown to migrate very slowly in the nucleoplasm, unless conjugated to NES peptides, suggesting that NESs lead not only to export, but to specific intranuclear transport.
66. Ris H. High-resolution field-emission scanning electron microscopy of nuclear pore complex. of outstanding interest Scanning. 19:1997;368-375 New intranuclear structures are described that consist of branching hollow cables connecting the nuclear interior to NPCs.
67. Cordes VC, Reidenbach S, Rackwitz HR, Franke WW. Identification of protein p270/Tpr as a constitutive component of the nuclear pore complex-attached intranuclear filaments. of outstanding interest J Cell Biol. 136:1997;515-529 The nucleoporin Tpr was shown to be a component of long filaments emanating from the NPC into the nuclear interior. In some cases these filaments appeared to link the NPC and the nucleolus.
68. Arts GJ, Fornerod M, Mataj IW. Identification of a nuclear export receptor for tRNA. Curr Biol. 8:1998;305-314.
69. Kutay U, Lipowsky G, Izzauralde E, Bischoff FR, Schwarzmaier P, Hartmann E, Görlich D. Identification of a tRNA-specific nuclear export receptor. Mol Cell. 1:1998;359-369.