Distinct nuclear import and export pathways mediated by members of the karyopherin β family

Journal of Cellular Biochemistry

Volumn 70, Issue 2, 1998, Pages 231-239

  Moroianu, Junona ^a  

^a BOSTON COLLEGE   (United States)

Author keywords

Nuclear export signals; Nuclear localization signals; Nuclear pore complexes

Indexed keywords

BINDING PROTEIN; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATASE; KARYOPHERIN BETA; MESSENGER RNA; NUCLEOPORIN; NUCLEOPROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

CELL NUCLEUS MATRIX; DROSOPHILA; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; INTRACELLULAR TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW; VIRUS INFECTION;

ALPHA KARYOPHERINS; ANIMALS; BETA KARYOPHERINS; BIOLOGICAL TRANSPORT; CELL NUCLEUS; NUCLEAR PROTEINS; RIBOSOMAL PROTEINS; RNA, MESSENGER; RNA-BINDING PROTEINS;

HUMAN IMMUNODEFICIENCY VIRUS; NES;

EID: 0031858902     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4644(19980801)70:2<231::AID-JCB9>3.0.CO;2-P     Document Type: Review

References (86)

1. Adachi Y, Yanagida M (1989): Higher order chromosome structure is affected by cold-sensitive mutations in a Schizosaccharomyces pombe gene crm1+ which encodes a 115 kd protein preferentially localized in the nucleus and its periphery. J Cell Biol 108:1195-1207.
2. Adam EDH, Adam SA (1994): Identification of cytosolic factors required for nuclear location sequence-mediated binding to the nuclear envelope. J Cell Biol 125:547-555.
3. Aitchison JD, Blobel G, Rout MP (1996): Kap104p: A karyopherin involved in the nuclear transport of messenger RNA binding proteins. Science 274:624-627.
4. Becker J, Melchior F, Gerke V, Bischoff FR, Ponstingl H, Wittighofer A (1995): RNA1 encodes a GTPase-activating protein specific for Gsplp, the Ran/TC4 homologue of Saccharomyces cerevisiae. J Biol Chem 270:11860-11865.
5. Belhumeur P, Lee A, Tam R, DiPaolo T, Fortin N, Clark M (1993): 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 13:2152-2161.
6. Bischoff FR, Ponstingl H (1991): Catalysis of guanine nucleotide exchange on Ran by the mitotic regulator RCC1. Nature 354:80-82.
7. Bischoff FR, Kreber H, Kempf T, Hermes I, Ponstingl H (1995a): Human RanGTPase-activating protein Ran-GAP1 is a homologue of yeast RNA1p involved in mRNA processing and transport. Proc Natl Acad Sci USA 92: 1749-1753.
8. Bischoff R, Krebber H, Smirnova E, Dong W, Ponstingl H (1995b): Coactivation of RanGTPase and inhibition of GTP dissociation by Ran-GTP protein RanBP1. EMBO J 14:705-715.
9. Bonifaci N, Moroianu J, Radu A, Blobel G (1997): Karyopherin β2 mediates nuclear import of a mRNA binding protein. Proc Natl Acad Sci USA 94:5055-5060.
10. Brinkmann U, Brinkmann E, Gallo M, Pastan I (1995): Cloning and characterization of a cellular apoptosis susceptibility gene, the human homologue to the yeast chromosome segregation gene CSE1. Proc Natl Acad Sci USA 92:10427-10431.
11. Bukrinsky MI, Haggerty S, Dempsey MP, Sharova N, Adzhubel A, et al. (1993): A nuclear localization signal within HIV1 matrix protein that governs infection of non-dividing cells. Nature 365:666-669.
12. Carey KL, Richards SA, Lounsbury KM, Macara IG (1996): Evidence using a green fluorescent protein-glucocorticoid receptor chimera that the RanTC4 GTPase mediates an essential function independent of nuclear protein import. J Cell Biol 133:985-996.
13. Chi NC, Adam SA (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.
14. Chi NC, Adam EJH, Visser GD, Adam SA (1996): RanBP1 stabilizes the interaction of Ran with p97 in nuclear protein import. J Cell Biol 135:559-569.
15. Corbett AH, Silver PA (1996): The NTF2 gene encodes an essential, highly conserved protein that functions in nuclear transport in vivo. J Biol Chem 271:18477-18484.
16. Corbett AH, Koepp DM, Schlenstedt G, Lee MS, Hooper AK, Silver PA (1995): Rna1p, a Ran/TC4 GTPase activating protein, is required for nuclear import. J Cell Biol 130:1017-1026.
17. Coutavas E, Ren M, Oppenheim JD, D'Eustachio P, Rush MG (1993): Characterization of proteins that interact with the cell-cycle regulatory protein Ran/TC4. Nature 366:585-587.
18. Dasso M (1993): RCC1 in cell cycle: The regulator of chromosome condensation takes on new roles. Trends Biochem Sci 18:96-101.
19. Dingwall C, Laskey RA (1991): Nuclear targeting sequences - A consensus? Trends Biochem Sci 16:478-481.
20. Drivas GT, Shih A, Coutavas E, Rush MG, D'Eustachio P (1990): Characterization of four novel ras-like genes expressed in a human teratocarcinoma cell line. Mol Cell Biol 10:1793-1798.
21. Fischer N, Kremmer E, Lautscham G, Mueller-Lantzsch N, Grasser FA (1997): Epstein-Barr virus nuclear antigen 1 forms a complex with the nuclear transporter karyopherin α2. J Biol Chem 272:3999-4005.
22. Fisher U, Huber J, Boelens WC, Mattaj IW, Lührmann R (1995): The HFV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell 82:475-483.
23. Floer M, Blobel G, Rexach M (1997): Disassembly of RanGTP-karyopherin β complex, an intermediate in nuclear protein import. J Biol Chem 272:19538-19546.
24. Fornerod M, van Deursen J, van Ball S, Murti KG, Fransen J, Grosveld G (1997a): 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.
25. Fornerod M, Ohno M, Yoshida M, Mattaj IW (1997b): CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90:1051-1060.
26. Gallay P, Stitt V, Mundy C, Oettinger M, Trono D (1996): Role of karyopherin pathway in human immunodeficiency virus type 1 nuclear import. J Virol 70:1027-1032.
27. Garcia-Bustos J, Heitman J, Hall MN (1991): Nuclear protein localization. Biochem Biophys Acta 1071:83-101.
28. Görlich D, Mattaj IW (1996): Nucleocytoplasmic transport. Science 271:1513-1517.
29. Görlich D, Vogel F, Mills AD, Hartmann E, Laskey RA (1995): Distinct functions for the two importin subunits in nuclear protein import. Nature 377:246-248.
30. Görlich D, Henklein P, Laskey RA, Hartmann E (1996a): A 41 amino acid motif in importin alpha confers binding to importin beta and hence transit into the nucleus. EMBO J 15:1810-1817.
31. Görlich D, Pante N, Kutay U, Aebi U, Bischoff FR (1996b): Identification of different roles for RanGDP and RanGTP in nuclear protein import. EMBO J 15:5584-5594.
32. Görlich D, Dabrowski M, Bischoff FR, Kutay U, Bork P, Hartmann E, Prehn S, Izaurralde E (1997): A novel class of RanGTP binding proteins. J Cell Biol 138:65-80.
33. Hopper AK, Traglia HM, Dunst RW (1990): The yeast RNA1 gene product necessary for RNA processing is located in the cytosol and apparently excluded from the nucleus. J Cell Biol 111:309-321.
34. Imamoto N, Shimamoto T, Takao T, Tachibana T, Kose S, Matsubae M, Sekimoto T, Shimonishi Y, Yoneda Y (1995): In vivo evidence for involvement of a 58 kDa component of nuclear pore-targeting complex in nuclear protein import. EMBO J 14:3617-3626.
35. Iovine MK, Wente SR (1997): A nuclear export signal in Kap 95p is required for both recycling the import factor and interaction with the nucleoporin GLFG repeat regions of Nup 116p and Nup 100p. J Cell Biol 137:1-15.
36. Irniger S, Piatti S, Michaelis C, Nasmyth K (1995): Genes involved in sister chromatid separation are needed for B-type cyclin proteolysis in budding yeast. Cell 81:269-278.
37. Izaurralde E, Jarmolowski A, Beise C, Mattaj IW, Dreyfuss G (1997a): Arole for the M9 transport signal of hnRNP A1 in mRNA nuclear export. J Cell Biol 137:27-35.
38. Izaurralde E, Kutay U, Mattaj IW, Gorlich D (1998): 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.
39. Koepp D, Wong A, Corbett A, Silver PA (1996): Dynamic localization of the nuclear import receptor and its interactions with transport factors. J Cell Biol 133:1163-1176.
40. Kutay U, Izaurralde E, Bischoff FR, Mattaj IW, Görlich D (1997a): Dominant-negative mutants of importin-β block multiple pathways of import and export through the nuclear pore complex. EMBO J 16:1153-1163.
41. Kutay U, Bischoff FR, Kosthka S, Kraft R, Gorlich D (1997b): Export of importin a from the nucleus is mediated by a specific nuclear transport factor. Cell 90:1061-1071.
42. Lee MS, Henry M, Silver PA (1996): A protein that shuttles between the nucleus and the cytoplasm is an important mediator of RNA export. Genes Dev 10:1233-1246.
43. Mahajan R, Delphin C, Guan T, Gerace L, Melchior F (1997): A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 88:97-107.
44. Matunis MJ, Coutavas E, Blobel G (1997): Anovel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein between cytosol and nuclear pore complex. J Cell Biol 135:1457-1470.
45. Melchior F, Paschal B, Evans J, 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.
46. Melchior F, Guan T, Yokoyama N, Nishimoto T, Gerace L (1995): GTP hydrolysis by Ran occurs at the nuclear pore complex in an early step of protein import. J Cell Biol 131:571-581.
47. Michael WM, Choi M, Dreyfuss G (1995): A nuclear export signal in hnRNP A1: A signal-mediated, temperature-dependent nuclear protein export pathway. Cell 83:415-422.
48. Michael WM, Eder PS, Dreyfuss G (1997): The K nuclear shuttling domain: A novel signal for nuclear import and nuclear export in the hnRNP K protein. EMBO J 16:3587-3598.
49. Moore MS, Blobel G (1993): The GTP-binding protein Ran/ TC4 is required for protein import into the nucleus. Nature 365:661-663.
50. Moore MS, Blobel G (1994): Purification of a Ran-interacting protein that is required for protein import into the nucleus. Proc Natl Acad Sci USA 91:10212-10216.
51. Moroianu J (1997): Molecular mechanisms of nuclear protein transport. Crit Rev Eukaryotic Gene Expression 7:61-72.
52. Moroianu J, Blobel G, Radu A (1995a): Previously identified protein of uncertain function is karyopherin α and together with karyopherin ß docks import substrate at nuclear pore complexes. Proc Natl Acad Sci USA 92:2008-2011.
53. Moroianu J, Hijikata M, Blobel G, Radu A (1995b): Mammalian karyopherin α1β and α2β heterodimers: α1 or α2 subunits binds nuclear localization signal and β subunit interacts with peptide repeat-containing nucleoporins. Proc Natl Acad Sci USA 92:6532-6536.
54. Moroianu J, Blobel G, Radu A (1996a): The binding site of karyopherin α for karyopherin β overlaps with a nuclear localization sequence. Proc Natl Acad Sci USA 93:6572-6576.
55. Moroianu J, Blobel G, Radu A (1996b): Nuclear protein import: Ran-GTP dissociates the karyopherin αβ heterodimer by displacing α from an overlapping binding site on β. Proc Natl Acad Sci USA 93:7059-7062.
56. Moroianu J, Blobel G, Radu A (1997): RanGTP-mediated nuclear export of karyopherin α involves its interaction with the nucleoporin Nup153. Proc Natl Acad Sci USA 94:9699-9704.
57. Nakielny S, Fischer U, Michael WM, Dreyfuss G (1997): RNA transport. Annu Rev Neurosci 20:269-301.
58. Nehrbass U, Blobel G (1996): Role of the nuclear transport factor p10 in nuclear import. Science 272:120-122.
59. Ohtsubo M, Okazaki H, Nishimoto T (1989): The RCC1 protein, a regulator for the onset of chromosome condensation locates in the nucleus and binds to DNA. J Cell Biol 109:1389-1397.
60. O'Neill RE, Palese P (1994): NPI-1, the human homologue of SRP-1, interacts with influenza virus nucleoprotein. Virology 206:116-125.
61. O'Neill RE, Jaskunas R, Blobel G, Palese P, Moroianu J (1995): Nuclear import of influenza virus RNA can be mediated by viral nucleoprotein and transport factors required for protein import. J Biol Chem 270:22701-22704.
62. Palacios I, Weis K, Klebe C, Dingwall C (1996): Ran/TC4 mutants identify a common requirement for snRNP and protein import into the nucleus. J Cell Biol 133:485-494.
63. Paschal BM, 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.
64. Paschal BM, Delphin C, Gerace L (1996) Nucleotide-specific interaction of Ran/TC4 with nuclear transport factor NTF2 and p97. Proc Natl Acad Sci USA 93:7679-7683.
65. Peifer M, Berg S, Reynolds AB (1994): A repeating amino acid motif shared by proteins with diverse cellular roles. Cell 76:789-791.
66. Pinol-Roma S, Dreyfuss G (1992): Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature 355:730-732.
67. Pollard VW, Michael WM, Nakielny S, Siomi MC, Wang F, Dreyfuss G (1996): A novel receptor-mediated nuclear protein import pathway. Cell 86:985-994.
68. Rexach M, Blobel G (1995): Protein import into nuclei: Association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell 83:683-692.
69. Richards SA, Lounsbury KM, Macara IG (1995): The C-terminus of the nuclear Ran/TC4 GTPase stabilises the GDP bound state and mediates interactions with RCC1, RanGAP and HTF9A/RanBP1. J Biol Chem 270: 14405-14411.
70. Richards SA, Lounsbury KM, Carey KL, Macara IG (1996): A nuclear export signal is essential for the cytosolic localization of the Ran binding protein, RanBP1. J Cell Biol 134:1157-1168.
71. Richards SA, Carey KL, Macara IG (1997): Requirement of guanosine triphosphatase-bound Ran for signal-mediated nuclear protein export. Science 276:1842-1844.
72. Rout MP, Wente SR (1994): Pores for thought: Nuclear pore proteins. Trends Cell Biol 4:357-365.
73. Rout MP, Blobel G, Aitchison JD (1997): A distinct nuclear import pathway used by ribosomal proteins. Cell 89:715-725.
74. Schlenstedt G, Saavedra C, Loeb J, Cole C, Silver P (1995a): The GTP-bound form of yeast Ran/TC4 homologues blocks nuclear protein import and appearance of poly-(A)+ RNA in the cytoplasm. Proc Natl Acad Sci USA 92:225-229.
75. Schlenstedt G, Wong DH, Koepp DM, Silver PA (1995b): Mutants in a yeast Ran binding protein are defective in nuclear transport. EMBO J 14:5367-5378.
76. Simos G, Tekotte H, Grosjean H, Segref A, Sharma K, Tollervey D, Hurt EC (1996): Nuclear pore proteins are involved in the biogenesis of functional tRNA. EMBO J 15:2270-2284.
77. Siomi H, Dreyfuss G (1995): A nuclear localization domain in the hnRNP A1 protein. J Cell Biol 129:551-560.
78. Siomi MC, Eder PS, Kataoka N, Wan L, Liu Q, Dreyfuss G (1997): Transportin-mediated nuclear import of heterogenous nuclear RNP proteins. J Cell Biol 138:1181-1192.
79. Stade K, Ford CS, Guthrie C, Weis K (1997): Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 90: 1041-1050.
80. Tachibana T, Imamoto N, Seino H, Nishimoto H, Yoneda Y (1994): Loss of RCC1 leads to suppression of nuclear protein import in living cells. J Biol Chem 40:24542-24545.
81. von Schwedler U, Kornbluth RS, Trono D (1994): The nuclear localization signal of the matrix protein of human immunodeficiency virus type 1 allows the establishment of infection in macrophages and quiescent T lymphocytes. Proc Natl Acad Sci USA 91:6996-6999.
82. Weis K, Mattaj IW, Lamond AI (1995): Identification of hSRPα as a functional receptor for nuclear localization sequence. Science 268:1049-1053.
83. Weis K, Ryder U, Lamond AL (1996): The conserved amino terminal domain of hSRP1α is essential for nuclear protein import EMBO J 15:1818-1825.
84. Whittaker G, Bui M, Helenius A (1996): The role of nuclear import and export in influenza virus infection. Trends Cell Biol 6:67-71.
85. Yaseen NR, Blobel G (1997): Cloning and characterization of human karyopherin β3. Proc Natl Acad Sci USA 94: 4451-4456.
86. Xiao Z, McGrew JT, Schroeder AJ, Fitzgerald-Hayes M (1993): CSE1 and CSE2, two new genes required for accurate mitotic chromosome segregation in Saccharomyces cerevisiae. Mol Cell Biol 13:4691-4702.