Yeast importin-β is required for nuclear import of the Mig2 repressor

BMC Cell Biology

Volumn 13, Issue , 2012, Pages

  Fernández Cid, Alejandra ^a,b   Vega, Montserrat ^a   Herrero, Pilar ^a   Moreno, Fernando ^a  

^a UNIVERSITY OF OVIEDO   (Spain)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; ARGININE 37; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; KARYOPHERIN ALPHA; KARYOPHERIN BETA; LYSINE; LYSINE 32; MIG2 PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; BIOACCUMULATION; CONTROLLED STUDY; FUNGAL STRAIN; IN VITRO STUDY; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; WILD TYPE;

ACTIVE TRANSPORT, CELL NUCLEUS; ALPHA KARYOPHERINS; AMINO ACID MOTIFS; BETA KARYOPHERINS; CELL NUCLEUS; KARYOPHERINS; MONOMERIC GTP-BINDING PROTEINS; MUTATION; NUCLEAR PROTEINS; PROTEIN BINDING; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 84871657600     PISSN: None     EISSN: 14712121     Source Type: Journal    
DOI: 10.1186/1471-2121-13-31     Document Type: Article

References (49)

1. Cook A, Bono F, Jinek M, Conti E. Structural biology of nucleocytoplasmic transport. Annu Rev Biochem 2007, 76:647-671. 10.1146/annurev.biochem.76.052705.161529, 17506639.
2. Radu A, Blobel G, Moore MS. 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 U S A 1995, 92(5):1769-1773. 10.1073/pnas.92.5.1769, 42601, 7878057.
3. Gorlich D, Prehn S, Laskey RA, Hartmann E. Isolation of a protein that is essential for the first step of nuclear protein import. Cell 1994, 79(5):767-778. 10.1016/0092-8674(94)90067-1, 8001116.
4. Stade K, Ford CS, Guthrie C, Weis K. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 1997, 90(6):1041-1050. 10.1016/S0092-8674(00)80370-0, 9323132.
5. Gorlich D, Kostka S, Kraft R, Dingwall C, Laskey RA, Hartmann E, Prehn S. Two different subunits of importin cooperate to recognize nuclear localization signals and bind them to the nuclear envelope. Curr Biol 1995, 5(4):383-392. 10.1016/S0960-9822(95)00079-0, 7627554.
6. Pemberton LF, Paschal BM. Mechanisms of receptor-mediated nuclear import and nuclear export. Traffic 2005, 6(3):187-198. 10.1111/j.1600-0854.2005.00270.x, 15702987.
7. Weis K. Regulating access to the genome: nucleocytoplasmic transport throughout the cell cycle. Cell 2003, 112(4):441-451. 10.1016/S0092-8674(03)00082-5, 12600309.
8. Kalab P, Weis K, Heald R. Visualization of a Ran-GTP gradient in interphase and mitotic Xenopus egg extracts. Science 2002, 295(5564):2452-2456. 10.1126/science.1068798, 11923538.
9. Smith AE, Slepchenko BM, Schaff JC, Loew LM, Macara IG. Systems analysis of Ran transport. Science 2002, 295(5554):488-491. 10.1126/science.1064732, 11799242.
10. Kalderon D, Roberts BL, Richardson WD, Smith AE. A short amino acid sequence able to specify nuclear location. Cell 1984, 39(3 Pt 2):499-509.
11. Jakel S, Gorlich D. Importin beta, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J 1998, 17(15):4491-4502. 10.1093/emboj/17.15.4491, 1170780, 9687515.
12. Nagoshi E, Imamoto N, Sato R, Yoneda Y. Nuclear import of sterol regulatory element-binding protein-2, a basic helix-loop-helix-leucine zipper (bHLH-Zip)-containing transcription factor, occurs through the direct interaction of importin beta with HLH-Zip. Mol Biol Cell 1999, 10(7):2221-2233. 25438, 10397761.
13. Moore JD, Yang J, Truant R, Kornbluth S. Nuclear import of Cdk/cyclin complexes: identification of distinct mechanisms for import of Cdk2/cyclin E and Cdc2/cyclin B1. J Cell Biol 1999, 144(2):213-224. 10.1083/jcb.144.2.213, 2132890, 9922449.
14. Harley VR, Layfield S, Mitchell CL, Forwood JK, John AP, Briggs LJ, McDowall SG, Jans DA. Defective importin beta recognition and nuclear import of the sex-determining factor SRY are associated with XY sex-reversing mutations. Proc Natl Acad Sci U S A 2003, 100(12):7045-7050. 10.1073/pnas.1137864100, 165827, 12764225.
15. Lam MH, Briggs LJ, Hu W, Martin TJ, Gillespie MT, Jans DA. Importin beta recognizes parathyroid hormone-related protein with high affinity and mediates its nuclear import in the absence of importin alpha. J Biol Chem 1999, 274(11):7391-7398. 10.1074/jbc.274.11.7391, 10066803.
16. Strahl T, Hama H, DeWald DB, Thorner J. Yeast phosphatidylinositol 4-kinase, Pik1, has essential roles at the Golgi and in the nucleus. J Cell Biol 2005, 171(6):967-979. 10.1083/jcb.200504104, 1382337,1382337, 16365163.
17. Lutfiyya LL, Johnston M. Two zinc-finger-containing repressors are responsible for glucose repression of SUC2 expression. Mol Cell Biol 1996, 16(9):4790-4797. 231480, 8756637.
18. Lutfiyya LL, Iyer VR, DeRisi J, DeVit MJ, Brown PO, Johnston M. Characterization of three related glucose repressors and genes they regulate in Saccharomyces cerevisiae. Genetics 1998, 150(4):1377-1391. 1460414, 9832517.
19. Ostling J, Carlberg M, Ronne H. Functional domains in the Mig1 repressor. Mol Cell Biol 1996, 16(3):753-761. 231055, 8622676.
20. Ahuatzi D, Herrero P, de la Cera T, Moreno F. The glucose-regulated nuclear localization of hexokinase 2 in Saccharomyces cerevisiae is Mig1-dependent. J Biol Chem 2004, 279(14):14440-14446. 10.1074/jbc.M313431200, 14715653.
21. Ahuatzi D, Riera A, Pelaez R, Herrero P, Moreno F. Hxk2 regulates the phosphorylation state of Mig1 and therefore its nucleocytoplasmic distribution. J Biol Chem 2007, 282(7):4485-4493.
22. Moreno F, Ahuatzi D, Riera A, Palomino CA, Herrero P. Glucose sensing through the Hxk2-dependent signalling pathway. Biochem Soc Trans 2005, 33(Pt 1):265-268.
23. Treitel MA, Kuchin S, Carlson M. Snf1 protein kinase regulates phosphorylation of the Mig1 repressor in Saccharomyces cerevisiae. Mol Cell Biol 1998, 18(11):6273-6280. 109214, 9774644.
24. Pelaez R, Herrero P, Moreno F. Nuclear export of the yeast hexokinase 2 protein requires the Xpo1 (Crm1)-dependent pathway. J Biol Chem 2009, 284(31):20548-20555. 10.1074/jbc.M109.013730, 2742819, 19525230.
25. Fernandez-Cid A, Riera A, Herrero P, Moreno F. Glucose levels regulate the nucleo-mitochondrial distribution of Mig2. Mitochondrion 2012, 12(3):370-380. 10.1016/j.mito.2012.02.001, 22353369.
26. Wallis JW, Chrebet G, Brodsky G, Rolfe M, Rothstein R. A hyper-recombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase. Cell 1989, 58(2):409-419. 10.1016/0092-8674(89)90855-6, 2546682.
27. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, Boeke JD. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 1998, 14(2):115-132. 10.1002/(SICI)1097-0061(19980130)14:2<115::AID-YEA204>3.0.CO;2-2, 9483801.
28. Longtine MS, 3rd McKenzie A, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998, 14(10):953-961. 10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U, 9717241.
29. Ma H, Botstein D. Effects of null mutations in the hexokinase genes of Saccharomyces cerevisiae on catabolite repression. Mol Cell Biol 1986, 6(11):4046-4052. 367170, 3540605.
30. Belinchon MM, Gancedo JM. Different signalling pathways mediate glucose induction of SUC2, HXT1 and pyruvate decarboxylase in yeast. FEMS Yeast Res 2007, 7(1):40-47. 10.1111/j.1567-1364.2006.00136.x, 17311583.
31. Nehlin JO, Ronne H. Yeast MIG1 repressor is related to the mammalian early growth response and Wilms' tumour finger proteins. EMBO J 1990, 9(9):2891-2898. 552004, 2167835.
32. Mercado JJ, Vincent O, Gancedo JM. Regions in the promoter of the yeast FBP1 gene implicated in catabolite repression may bind the product of the regulatory gene MIG1. FEBS Lett 1991, 291(1):97-100. 10.1016/0014-5793(91)81112-L, 1657641.
33. Taberner FJ, Quilis I, Igual JC. Spatial regulation of the start repressor Whi5. Cell Cycle 2009, 8(18):3010-3018.
34. Michaelis C, Ciosk R, Nasmyth K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 1997, 91(1):35-45. 10.1016/S0092-8674(01)80007-6, 9335333.
35. Kadowaki H, Kadowaki T, Wondisford FE, Taylor SI. Use of polymerase chain reaction catalyzed by Taq DNA polymerase for site-specific mutagenesis. Gene 1989, 76(1):161-166. 10.1016/0378-1119(89)90018-8, 2744478.
36. Pelaez R, Fernandez-Garcia P, Herrero P, Moreno F. Nuclear import of the yeast hexokinase 2 protein requires alpha/beta-importin-dependent pathway. J Biol Chem 2012, 287(5):3518-3529. 10.1074/jbc.M111.317230, 22157003.
37. Kunzler M, Gerstberger T, Stutz F, Bischoff FR, Hurt E. Yeast Ran-binding protein 1 (Yrb1) shuttles between the nucleus and cytoplasm and is exported from the nucleus via a CRM1 (XPO1)-dependent pathway. Mol Cell Biol 2000, 20(12):4295-4308. 10.1128/MCB.20.12.4295-4308.2000, 85797, 10825193.
38. Leslie DM, Timney B, Rout MP, Aitchison JD. Studying nuclear protein import in yeast. Methods 2006, 39(4):291-308. 10.1016/j.ymeth.2006.07.013, 16979507.
39. Gascon S, Lampen JO. Purification of the internal invertase of yeast. J Biol Chem 1968, 243(7):1567-1572.
40. DeVit MJ, Johnston M. The nuclear exportin Msn5 is required for nuclear export of the Mig1 glucose repressor of Saccharomyces cerevisiae. Curr Biol 1999, 9(21):1231-1241. 10.1016/S0960-9822(99)80503-X, 10556086.
41. Yoshida K, Blobel G. The karyopherin Kap142p/Msn5p mediates nuclear import and nuclear export of different cargo proteins. J Cell Biol 2001, 152(4):729-740. 10.1083/jcb.152.4.729, 2195777, 11266464.
42. Kosugi S, Hasebe M, Matsumura N, Takashima H, Miyamoto-Sato E, Tomita M, Yanagawa H. Six classes of nuclear localization signals specific to different binding grooves of importin alpha. J Biol Chem 2009, 284(1):478-485.
43. Quan X, Yu J, Bussey H, Stochaj U. The localization of nuclear exporters of the importin-beta family is regulated by Snf1 kinase, nutrient supply and stress. Biochim Biophys Acta 2007, 1773(7):1052-1061. 10.1016/j.bbamcr.2007.04.014, 17544521.
44. De Vit MJ, Waddle JA, Johnston M. Regulated nuclear translocation of the Mig1 glucose repressor. Mol Biol Cell 1997, 8(8):1603-1618. 276179, 9285828.
45. Fornerod M, Ohno M, Yoshida M, Mattaj IW. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 1997, 90(6):1051-1060. 10.1016/S0092-8674(00)80371-2, 9323133.
46. Tiganis T, Flint AJ, Adam SA, Tonks NK. Association of the T-cell protein tyrosine phosphatase with nuclear import factor p97. J Biol Chem 1997, 272(34):21548-21557. 10.1074/jbc.272.34.21548, 9261175.
47. 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 1997, 274(5):693-707. 10.1006/jmbi.1997.1420, 9405152.
48. Fries T, Betz C, Sohn K, Caesar S, Schlenstedt G, Bailer SM. A novel conserved nuclear localization signal is recognized by a group of yeast importins. J Biol Chem 2007, 282(27):19292-19301. 10.1074/jbc.M700217200, 17485461.
49. Belanger KD, Griffith AL, Baker HL, Hansen JN, Kovacs LA, Seconi JS, Strine AC. The karyopherin Kap95 and the C-termini of Rfa1, Rfa2, and Rfa3 are necessary for efficient nuclear import of functional RPA complex proteins in Saccharomyces cerevisiae. DNA Cell Biol 2011, 30(9):641-651. 10.1089/dna.2010.1071, 3168979, 21332387.