Evolution of the karyopherin-β family of nucleocytoplasmic transport factors; ancient origins and continued specialization

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  O'Reilly, Amanda J ^a   Dacks, Joel B ^b   Field, Mark C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

KARYOPHERIN BETA; NUCLEOCYTOPLASMIC TRANSPORT PROTEIN; PROTEOME;

AMINO ACID SEQUENCE; ARCHAEPLASTIDA; ARTICLE; EUKARYOTE; HISTORY; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENY; PREDICTION; PROTEIN FAMILY; TAXONOMY; CELL NUCLEUS; CLASSIFICATION; CYTOPLASM; GENETICS; HUMAN; METABOLISM; PROTEOMICS;

ARCHAEPLASTIDA; EUKARYOTA;

BETA KARYOPHERINS; CELL NUCLEUS; CYTOPLASM; EVOLUTION, MOLECULAR; HUMANS; PHYLOGENY; PROTEOMICS;

EID: 79955679956     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019308     Document Type: Article

References (90)

1. Martin W, Koonin EV, (2006) Introns and the origin of nucleus-cytosol compartmentalization. Nature 440: 41-45.
2. Dacks JB, Field MC, (2007) Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode. J Cell Sci 120: 2977-2985.
3. Devos D, Dokudovskaya S, Alber F, Williams R, Chait BT, et al. (2004) Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol 2: e380.
4. Field MC, Dacks JB, (2009) First and last ancestors: reconstructing evolution of the endomembrane system with ESCRTs, vesicle coat proteins, and nuclear pore complexes. Curr Opin Cell Biol 21: 4-13.
5. Mason DA, Stage DE, Goldfarb DS, (2009) Evolution of the metazoan-specific importin alpha gene family. J Mol Evol 68: 351-365.
6. Kappel C, Zachariae U, Dolker N, Grubmuller H, (2010) An unusual hydrophobic core confers extreme flexibility to HEAT repeat proteins. Biophys J 99: 1596-1603.
7. Groves MR, Hanlon N, Turowski P, Hemmings BA, Barford D, (1999) The structure of the protein phosphatase 2A PR65/A subunit reveals the conformation of its 15 tandemly repeated HEAT motifs. Cell 96: 99-110.
8. Cook A, Bono F, Jinek M, Conti E, (2007) Structural biology of nucleocytoplasmic transport. Annu Rev Biochem 76: 647-671.
9. Strom AC, Weis K, (2001) Importin-beta-like nuclear transport receptors. Genome Biol 2: REVIEWS3008.
10. Gorlich D, Prehn S, Laskey RA, Hartmann E, (1994) Isolation of a protein that is essential for the first step of nuclear protein import. Cell 79: 767-778.
11. Stade K, Ford CS, Guthrie C, Weis K, (1997) Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 90: 1041-1050.
12. Gorlich D, Kostka S, Kraft R, Dingwall C, Laskey RA, et al. (1995) Two different subunits of importin cooperate to recognize nuclear localization signals and bind them to the nuclear envelope. Curr Biol 5: 383-392.
13. Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, et al. (2007) The molecular architecture of the nuclear pore complex. Nature 450: 695-701.
14. Ribbeck K, Lipowsky G, Kent HM, Stewart M, Gorlich D, (1998) NTF2 mediates nuclear import of Ran. Embo J 17: 6587-6598.
15. Gorlich D, Kutay U, (1999) Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol 15: 607-660.
16. Mosammaparast N, Pemberton LF, (2004) Karyopherins: from nuclear-transport mediators to nuclear-function regulators. Trends Cell Biol 14: 547-556.
17. Meier I, (2005) Nucleocytoplasmic trafficking in plant cells. Int Rev Cytol 244: 95-135.
18. Rout MP, Aitchison JD, Suprapto A, Hjertaas K, Zhao Y, et al. (2000) The yeast nuclear pore complex: composition, architecture, and transport mechanism. J Cell Biol 148: 635-651.
19. Ribbeck K, Gorlich D, (2001) Kinetic analysis of translocation through nuclear pore complexes. EMBO J 20: 1320-1330.
20. Macara IG, (2001) Transport into and out of the nucleus. Microbiol Mol Biol Rev 65: 570-594.
21. Peters R, (2005) Translocation through the nuclear pore complex: selectivity and speed by reduction-of-dimensionality. Traffic 6: 421-427.
22. Patel SS, Belmont BJ, Sante JM, Rexach MF, (2007) Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex. Cell 129: 83-96.
23. Zilman A, Di Talia S, Chait BT, Rout MP, Magnasco MO, (2007) Efficiency, selectivity, and robustness of nucleocytoplasmic transport. PLoS Comput Biol 3: e125.
24. Bayliss R, Littlewood T, Stewart M, (2000) Structural basis for the interaction between FxFG nucleoporin repeats and importin-beta in nuclear trafficking. Cell 102: 99-108.
25. Jovanovic-Talisman T, Tetenbaum-Novatt J, McKenney AS, Zilman A, Peters R, et al. (2009) Artificial nanopores that mimic the transport selectivity of the nuclear pore complex. Nature 457: 1023-1027.
26. Gorlich D, Mattaj IW, (1996) Nucleocytoplasmic transport. Science 271: 1513-1518.
27. Chook YM, Suel KE, (2010) Nuclear import by karyopherin-betas: Recognition and inhibition. Biochim Biophys Acta doi:10.1016/j.bbamcr.2010.10.014.
28. Sydorskyy Y, Dilworth DJ, Yi EC, Goodlett DR, Wozniak RW, et al. (2003) Intersection of the Kap123p-mediated nuclear import and ribosome export pathways. Mol Cell Biol 23: 2042-2054.
29. Muhlhausser P, Muller EC, Otto A, Kutay U, (2001) Multiple pathways contribute to nuclear import of core histones. EMBO Rep 2: 690-696.
30. Rout MP, Blobel G, Aitchison JD, (1997) A distinct nuclear import pathway used by ribosomal proteins. Cell 89: 715-725.
31. Strawn LA, Shen T, Shulga N, Goldfarb DS, Wente SR, (2004) Minimal nuclear pore complexes define FG repeat domains essential for transport. Nat Cell Biol 6: 197-206.
32. DeGrasse JA, DuBois KN, Devos D, Siegel TN, Sali A, et al. (2009) Evidence for a shared nuclear pore complex architecture that is conserved from the last common eukaryotic ancestor. Mol Cell Proteomics 8: 2119-2130.
33. Cingolani G, Petosa C, Weis K, Muller CW, (1999) Structure of importin-beta bound to the IBB domain of importin-alpha. Nature 399: 221-229.
34. Cingolani G, Bednenko J, Gillespie MT, Gerace L, (2002) Molecular basis for the recognition of a nonclassical nuclear localization signal by importin beta. Mol Cell 10: 1345-1353.
35. Lee SJ, Sekimoto T, Yamashita E, Nagoshi E, Nakagawa A, et al. (2003) The structure of importin-beta bound to SREBP-2: nuclear import of a transcription factor. Science 302: 1571-1575.
36. Devos D, Dokudovskaya S, Williams R, Alber F, Eswar N, et al. (2006) Simple fold composition and modular architecture of the nuclear pore complex. Proc Natl Acad Sci U S A 103: 2172-2177.
37. Neumann N, Lundin D, Poole AM, (2010) Comparative genomic evidence for a complete nuclear pore complex in the last eukaryotic common ancestor. PLoS One 5: e13241.
38. Adl SM, Simpson AG, Farmer MA, Andersen RA, Anderson OR, et al. (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52: 399-451.
39. Burki F, Shalchian-Tabrizi K, Minge M, Skjaeveland A, Nikolaev SI, et al. (2007) Phylogenomics reshuffles the eukaryotic supergroups. PLoS One 2: e790.
40. Goldfarb DS, Corbett AH, Mason DA, Harreman MT, Adam SA, (2004) Importin alpha: a multipurpose nuclear-transport receptor. Trends Cell Biol 14: 505-514.
41. Mans BJ, Anantharaman V, Aravind L, Koonin EV, (2004) Comparative genomics, evolution and origins of the nuclear envelope and nuclear pore complex. Cell Cycle 3: 1612-1637.
42. Quan Y, Ji ZL, Wang X, Tartakoff AM, Tao T, (2008) Evolutionary and transcriptional analysis of karyopherin beta superfamily proteins. Mol Cell Proteomics 7: 1254-1269.
43. Frankel MB, Knoll LJ, (2009) The ins and outs of nuclear trafficking: unusual aspects in apicomplexan parasites. DNA Cell Biol 28: 277-284.
44. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
45. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
46. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, et al. (2008) The Pfam protein families database. Nucleic Acids Res 36: D281-288.
47. Roger AJ, Simpson AG, (2009) Evolution: revisiting the root of the eukaryote tree. Curr Biol 19: R165-167.
48. Yoshida K, Blobel G, (2001) The karyopherin Kap142p/Msn5p mediates nuclear import and nuclear export of different cargo proteins. J Cell Biol 152: 729-740.
49. Mingot JM, Kostka S, Kraft R, Hartmann E, Gorlich D, (2001) Importin 13: a novel mediator of nuclear import and export. Embo J 20: 3685-3694.
50. Calado A, Treichel N, Muller EC, Otto A, Kutay U, (2002) Exportin-5-mediated nuclear export of eukaryotic elongation factor 1A and tRNA. Embo J 21: 6216-6224.
51. Wild T, Horvath P, Wyler E, Widmann B, Badertscher L, et al. (2010) A protein inventory of human ribosome biogenesis reveals an essential function of exportin 5 in 60 S subunit export. PLoS Biol 8: e1000522.
52. Lund E, Guttinger S, Calado A, Dahlberg JE, Kutay U, (2004) Nuclear export of microRNA precursors. Science 303: 95-98.
53. Bohnsack MT, Czaplinski K, Gorlich D, (2004) Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA 10: 185-191.
54. Shibata S, Sasaki M, Miki T, Shimamoto A, Furuichi Y, et al. (2006) Exportin-5 orthologues are functionally divergent among species. Nucleic Acids Res 34: 4711-4721.
55. Ploski JE, Shamsher MK, Radu A, (2004) Paired-type homeodomain transcription factors are imported into the nucleus by karyopherin 13. Mol Cell Biol 24: 4824-4834.
56. Kataoka N, Bachorik JL, Dreyfuss G, (1999) Transportin-SR, a nuclear import receptor for SR proteins. J Cell Biol 145: 1145-1152.
57. Pemberton LF, Rosenblum JS, Blobel G, (1997) A distinct and parallel pathway for the nuclear import of an mRNA-binding protein. J Cell Biol 139: 1645-1653.
58. Lipowsky G, Bischoff FR, Schwarzmaier P, Kraft R, Kostka S, et al. (2000) Exportin 4: a mediator of a novel nuclear export pathway in higher eukaryotes. Embo J 19: 4362-4371.
59. Kurisaki A, Kurisaki K, Kowanetz M, Sugino H, Yoneda Y, et al. (2006) The mechanism of nuclear export of Smad3 involves exportin 4 and Ran. Mol Cell Biol 26: 1318-1332.
60. Gontan C, Guttler T, Engelen E, Demmers J, Fornerod M, et al. (2009) Exportin 4 mediates a novel nuclear import pathway for Sox family transcription factors. J Cell Biol 185: 27-34.
61. Mingot JM, Bohnsack MT, Jakle U, Gorlich D, (2004) Exportin 7 defines a novel general nuclear export pathway. Embo J 23: 3227-3236.
62. Stuven T, Hartmann E, Gorlich D, (2003) Exportin 6: a novel nuclear export receptor that is specific for profilin.actin complexes. Embo J 22: 5928-5940.
63. Cock JM, Sterck L, Rouze P, Scornet D, Allen AE, et al. (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465: 617-621.
64. Gobler CJ, Berry DL, Dyhrman ST, Wilhelm SW, Salamov A, et al. (2011) Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics. Proc Natl Acad Sci U S A 108: 4352-4357.
65. Wada A, Fukuda M, Mishima M, Nishida E, (1998) Nuclear export of actin: a novel mechanism regulating the subcellular localization of a major cytoskeletal protein. Embo J 17: 1635-1641.
66. Nozaki H, Takano H, Misumi O, Terasawa K, Matsuzaki M, et al. (2007) A 100%-complete sequence reveals unusually simple genomic features in the hot-spring red alga Cyanidioschyzon merolae. BMC Biol 5: 28.
67. Koumandou VL, Dacks JB, Coulson RM, Field MC, (2007) Control systems for membrane fusion in the ancestral eukaryote; evolution of tethering complexes and SM proteins. BMC Evol Biol 7: 29.
68. Leung KF, Dacks JB, Field MC, (2008) Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage. Traffic 9: 1698-1716.
69. Nevin WD, Dacks JB, (2009) Repeated secondary loss of adaptin complex genes in the Apicomplexa. Parasitol Int 58: 86-94.
70. Lal K, Field MC, Carlton JM, Warwicker J, Hirt RP, (2005) Identification of a very large Rab GTPase family in the parasitic protozoan Trichomonas vaginalis. Mol Biochem Parasitol 143: 226-235.
71. Carlton JM, Hirt RP, Silva JC, Delcher AL, Schatz M, et al. (2007) Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315: 207-212.
72. Dacks JB, Carlton J, Hirt RP, Embley TM, (2005) Massive differential expansion of the Trichomonas vaginalis adaptin genomic complement. Journal of Eukaryotic Microbiology 52: 7S-27S.
73. Titov AA, Blobel G, (1999) The karyopherin Kap122p/Pdr6p imports both subunits of the transcription factor IIA into the nucleus. J Cell Biol 147: 235-246.
74. pfam website.Available: http://pfam.sanger.ac.uk/. Accessed: 2011 Apr 4.
75. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
76. Clamp M, Cuff J, Searle SM, Barton GJ, (2004) The Jalview Java alignment editor. Bioinformatics 20: 426-427.
77. The UniProt Consortium, (2009) The Universal Protein Resource (UniProt) 2009. Nucleic Acids Res 37: D169-174.
78. Mulder NJ, Apweiler R, Attwood TK, Bairoch A, Bateman A, et al. (2007) New developments in the InterPro database. Nucleic Acids Res 35: D224-228.
79. hmmer website. Available: http://hmmer.janelia.org/. Accessed: 2011 Apr.
80. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
81. Rice P, Longden I, Bleasby A, (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16: 276-277.
82. Shi J, Blundell TL, Mizuguchi K, (2001) FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J Mol Biol 310: 243-257.
83. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
84. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
85. camgrid website. Available: http://www.escience.cam.ac.uk/projects/camgrid/. Accessed: 2011 Apr.
86. Abascal F, Zardoya R, Posada D, (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105.
87. perl website. Available: http://www.cpan.org. Accessed: 2011 Apr.
88. Stajich JE, Block D, Boulez K, Brenner SE, Chervitz SA, et al. (2002) The Bioperl toolkit: Perl modules for the life sciences. Genome Res 12: 1611-1618.
89. Jordan GE, Piel WH, (2008) PhyloWidget: web-based visualizations for the tree of life. Bioinformatics 24: 1641-1642.
90. Field MC, Gabernet-Castello C, Dacks JB, (2007) Reconstructing the evolution of the endocytic system: insights from genomics and molecular cell biology. Adv Exp Med Biol 607: 84-96.