Identification of two functional nuclear localization signals mediating nuclear import of liver receptor homologue-1

Cellular and Molecular Life Sciences

Volumn 68, Issue 7, 2011, Pages 1241-1253

  Yang, Feng Ming ^a   Lin, Yu Chi ^a   Hu, Meng Chun ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

Importin; Liver receptor homologue 1 (LRH 1); Nuclear import; Nuclear localization signal; Nuclear receptor; Zinc finger

Indexed keywords

KARYOPHERIN ALPHA; KARYOPHERIN BETA; LIVER RECEPTOR HOMOLOG 1;

ARTICLE; CELL NUCLEUS; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA BINDING MOTIF; GENE MUTATION; GENETIC TRANSCRIPTION; MUTAGENESIS; NUCLEAR LOCALIZATION SIGNAL; PROTEIN DNA BINDING; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN TARGETING; PROTEIN TRANSPORT; TRANSPORT KINETICS;

ACTIVE TRANSPORT, CELL NUCLEUS; ALPHA KARYOPHERINS; AMINO ACID SEQUENCE; ANIMALS; BETA KARYOPHERINS; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; COS CELLS; MICE; MOLECULAR SEQUENCE DATA; NUCLEAR LOCALIZATION SIGNALS; PROTEIN CONFORMATION; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT;

EID: 79953727848     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-010-0521-5     Document Type: Article

References (45)

1. D Boerboom N Pilon R Behdjani DW Silversides J Sirois 2000 Expression and regulation of transcripts encoding two members of the NR5A nuclear receptor subfamily of orphan nuclear receptors, steroidogenic factor-1 and NR5A2, in equine ovarian cells during the ovulatory process Endocrinology 141 4647 4656 11108279 10.1210/en.141.12.4647 1:CAS:528:DC%2BD3cXosVSqtr4%3D (Pubitemid 32055144)
2. E Fayard J Auwerx K Schoonjans 2004 LRH-1: an orphan nuclear receptor involved in development, metabolism and steroidogenesis Trends Cell Biol 14 250 260 15130581 10.1016/j.tcb.2004.03.008 1:CAS:528:DC%2BD2cXjvVemu74%3D (Pubitemid 38591329)
3. JF Pare D Malenfant C Courtemanche M Jacob-Wagner S Roy D Allard L Belanger 2004 The fetoprotein transcription factor (FTF) gene is essential to embryogenesis and cholesterol homeostasis and is regulated by a DR4 element J Biol Chem 279 21206 21216 15014077 10.1074/jbc.M401523200 1:CAS:528: DC%2BD2cXjvV2ntLg%3D (Pubitemid 38656525)
4. X Luo Y Ikeda KL Parker 1994 A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation Cell 77 481 490 8187173 10.1016/0092-8674(94)90211-9 1:CAS:528:DyaK2cXksFCnu7c%3D (Pubitemid 24153989)
5. KI Morohashi T Omura 1996 Ad4BP/SF-1, a transcription factor essential for the transcription of steroidogenic cytochrome P450 genes and for the establishment of the reproductive function FASEB J 10 1569 1577 9002548 1:CAS:528:DyaK2sXmslKjtg%3D%3D (Pubitemid 27043773)
6. K Shinoda H Lei H Yoshii M Nomura M Nagano H Shiba H Sasaki Y Osawa Y Ninomiya O Niwa 1995 Developmental defects of the ventromedial hypothalamic nucleus and pituitary gonadotroph in the Ftz-F1 disrupted mice Dev Dyn 204 22 29 8563022 1:CAS:528:DyaK2MXovFCjtL8%3D
7. L Galarneau JF Pare D Allard D Hamel L Levesque JD Tugwood S Green L Belanger 1996 The alpha1-fetoprotein locus is activated by a nuclear receptor of the Drosophila FTZ-F1 family Mol Cell Biol 16 3853 3865 8668203 1:CAS:528:DyaK28XjvVWnu7k%3D (Pubitemid 26199905)
8. Y Luo CP Liang AR Tall 2001 The orphan nuclear receptor LRH-1 potentiates the sterol-mediated induction of the human CETP gene by liver X receptor J Biol Chem 276 24767 24773 11331284 10.1074/jbc.M100912200 1:CAS:528: DC%2BD3MXlt1agtrg%3D
9. M Nitta S Ku C Brown AY Okamoto B Shan 1999 CPF: an orphan nuclear receptor that regulates liver-specific expression of the human cholesterol 7alpha-hydroxylase gene Proc Natl Acad Sci U S A 96 6660 6665 10359768 10.1073/pnas.96.12.6660 1:CAS:528:DyaK1MXks1Wksrs%3D (Pubitemid 29274939)
10. CD Clyne CJ Speed J Zhou ER Simpson 2002 Liver receptor homologue-1 (LRH-1) regulates expression of aromatase in preadipocytes J Biol Chem 277 20591 20597 11927588 10.1074/jbc.M201117200 1:CAS:528:DC%2BD38XkslWgur4%3D (Pubitemid 34967360)
11. OA Botrugno E Fayard JS Annicotte C Haby T Brennan O Wendling T Tanaka T Kodama W Thomas J Auwerx K Schoonjans 2004 Synergy between LRH-1 and beta-catenin induces G1 cyclin-mediated cell proliferation Mol Cell 15 499 509 15327767 10.1016/j.molcel.2004.07.009 1:CAS:528:DC%2BD2cXns1ynurs%3D (Pubitemid 39141778)
12. H Ueda GC Sun T Murata S Hirose 1992 A novel DNA-binding motif abuts the zinc finger domain of insect nuclear hormone receptor FTZ-F1 and mouse embryonal long terminal repeat-binding protein Mol Cell Biol 12 5667 5672 1448096 1:CAS:528:DyaK3sXjtlyitw%3D%3D
13. EP Sablin IN Krylova RJ Fletterick HA Ingraham 2003 Structural basis for ligand-independent activation of the orphan nuclear receptor LRH-1 Mol Cell 11 1575 1585 12820970 10.1016/S1097-2765(03)00236-3 1:CAS:528:DC%2BD3sXltlSku7g%3D (Pubitemid 36776543)
14. FM Yang CT Pan HM Tsai TW Chiu ML Wu MC Hu 2009 Liver receptor homolog-1 localization in the nuclear body is regulated by sumoylation and cAMP signaling in rat granulosa cells FEBS J 276 425 436 19125815 10.1111/j.1742-4658.2008. 06785.x 1:CAS:528:DC%2BD1MXptV2lsA%3D%3D
15. AV Sorokin ER Kim LP Ovchinnikov 2007 Nucleocytoplasmic transport of proteins Biochemistry (Mosc) 72 1439 1457 10.1134/S0006297907130032 1:CAS:528:DC%2BD1cXitFWkt7Y%3D
16. D Kalderon WD Richardson AF Markham AE Smith 1984 Sequence requirements for nuclear location of simian virus 40 large-T antigen Nature 311 33 38 6088992 10.1038/311033a0 1:CAS:528:DyaL2cXlvVGjtrc%3D (Pubitemid 14065276)
17. J Robbins SM Dilworth RA Laskey C Dingwall 1991 Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence Cell 64 615 623 1991323 10.1016/0092-8674(91)90245-T 1:CAS:528:DyaK3MXhtFOhs7s%3D (Pubitemid 121002977)
18. A Lange RE Mills CJ Lange M Stewart SE Devine AH Corbett 2007 Classical nuclear localization signals: definition, function, and interaction with importin alpha J Biol Chem 282 5101 5105 17170104 10.1074/jbc.R600026200 1:CAS:528:DC%2BD2sXhvVajs7k%3D (Pubitemid 47093710)
19. D Palmeri MH Malim 1999 Importin beta can mediate the nuclear import of an arginine-rich nuclear localization signal in the absence of importin alpha Mol Cell Biol 19 1218 1225 9891056 1:CAS:528:DyaK1MXhtVKhtrY%3D (Pubitemid 29046864)
20. AS Philips JC Kwok BH Chong 2007 Analysis of the signals and mechanisms mediating nuclear trafficking of GATA-4. Loss of DNA binding is associated with localization in intranuclear speckles J Biol Chem 282 24915 24927 17548362 10.1074/jbc.M701789200 1:CAS:528:DC%2BD2sXpt1Slt78%3D (Pubitemid 47347503)
21. EC LaCasse YA Lefebvre 1995 Nuclear localization signals overlap DNA- or RNA-binding domains in nucleic acid-binding proteins Nucleic Acids Res 23 1647 1656 7540284 10.1093/nar/23.10.1647 1:CAS:528:DyaK2MXmsVOksrk%3D
22. D Picard KR Yamamoto 1987 Two signals mediate hormone-dependent nuclear localization of the glucocorticoid receptor EMBO J 6 3333 3340 3123217 1:CAS:528:DyaL2sXmt12nt7c%3D
23. JG Savory B Hsu IR Laquian W Giffin T Reich RJ Hache YA Lefebvre 1999 Discrimination between NL1- and NL2-mediated nuclear localization of the glucocorticoid receptor Mol Cell Biol 19 1025 1037 9891038 1:CAS:528: DyaK1MXhtVKhs74%3D (Pubitemid 29046846)
24. H Poukka U Karvonen N Yoshikawa H Tanaka JJ Palvimo OA Janne 2000 The RING finger protein SNURF modulates nuclear trafficking of the androgen receptor J Cell Sci 113 Pt 17 2991 3001 10934038 1:CAS:528:DC%2BD3cXmvFSnurs%3D
25. ZX Zhou M Sar JA Simental MV Lane EM Wilson 1994 A ligand-dependent bipartite nuclear targeting signal in the human androgen receptor. Requirement for the DNA-binding domain and modulation by NH2-terminal and carboxyl-terminal sequences J Biol Chem 269 13115 13123 8175737 1:STN:280:DyaK2c3jtVCjtA%3D%3D
26. T Ylikomi MT Bocquel M Berry H Gronemeyer P Chambon 1992 Cooperation of proto-signals for nuclear accumulation of estrogen and progesterone receptors EMBO J 11 3681 3694 1327748 1:CAS:528:DyaK38Xmt1Kms7w%3D
27. ND Freedman KR Yamamoto 2004 Importin 7 and importin alpha/importin beta are nuclear import receptors for the glucocorticoid receptor Mol Biol Cell 15 2276 2286 15004228 10.1091/mbc.E03-11-0839 1:CAS:528:DC%2BD2cXjvFKjtLw%3D (Pubitemid 38580645)
28. N Kaku K Matsuda A Tsujimura M Kawata 2008 Characterization of nuclear import of the domain-specific androgen receptor in association with the importin alpha/beta and Ran-guanosine 5′-triphosphate systems Endocrinology 149 3960 3969 18420738 10.1210/en.2008-0137 1:CAS:528:DC%2BD1cXptlamtro%3D
29. CL Fisher GK Pei 1997 Modification of a PCR-based site-directed mutagenesis method Biotechniques 23 570 574 9343663 1:CAS:528:DyaK2sXmslWnsb8%3D (Pubitemid 27450899)
30. R Higuchi B Krummel RK Saiki 1988 A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions Nucleic Acids Res 16 7351 7367 3045756 10.1093/nar/16.15.7351 1:CAS:528:DyaL1cXls1Cqu74%3D
31. N Imamoto T Shimamoto T Takao T Tachibana S Kose M Matsubae T Sekimoto Y Shimonishi Y Yoneda 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 7641681 1:CAS:528:DyaK2MXnsFGqtrc%3D
32. S Kose N Imamoto T Tachibana T Shimamoto Y Yoneda 1997 Ran-unassisted nuclear migration of a 97-kD component of nuclear pore-targeting complex J Cell Biol 139 841 849 9362503 10.1083/jcb.139.4.841 1:CAS:528:DyaK2sXnsV2ntrg%3D (Pubitemid 27508555)
33. HT Hsieh CH Wang ML Wu FM Yang YC Tai MC Hu 2009 PIASy inhibits LRH-1-dependent CYP11A1 expression by competing for SRC-1 binding Biochem J 419 201 209 19067654 10.1042/BJ20081402 1:CAS:528:DC%2BD1MXjtVShu7c%3D
34. MC Hu NC Hsu CI Pai CK Wang B Chung 2001 Functions of the upstream and proximal steroidogenic factor 1 (SF-1)-binding sites in the CYP11A1 promoter in basal transcription and hormonal response Mol Endocrinol 15 812 818 11328860 10.1210/me.15.5.812 1:CAS:528:DC%2BD3MXjt1Omu7o%3D (Pubitemid 32411318)
35. X Wei VG Henke C Strubing EB Brown DE Clapham 2003 Real-time imaging of nuclear permeation by EGFP in single intact cells Biophys J 84 1317 1327 12547812 10.1016/S0006-3495(03)74947-9 1:CAS:528:DC%2BD3sXovV2jtw%3D%3D (Pubitemid 36133453)
36. F Cardarelli M Serresi R Bizzarri M Giacca F Beltram 2007 In vivo study of HIV-1 Tat arginine-rich motif unveils its transport properties Mol Ther 15 1313 1322 17505482 10.1038/sj.mt.6300172 1:CAS:528:DC%2BD2sXhtVejtLrP (Pubitemid 46965328)
37. U Stochaj R Rassadi J Chiu 2000 Stress-mediated inhibition of the classical nuclear protein import pathway and nuclear accumulation of the small GTPase Gsp1p FASEB J 14 2130 2132 11024003 1:CAS:528:DC%2BD3MXht1KgsbY%3D
38. C Matheny ML Day J Milbrandt 1994 The nuclear localization signal of NGFI-A is located within the zinc finger DNA binding domain J Biol Chem 269 8176 8181 8132543 1:CAS:528:DyaK2cXjtFOqtLk%3D (Pubitemid 24200229)
39. DA Jans CY Xiao MH Lam 2000 Nuclear targeting signal recognition: a key control point in nuclear transport? Bioessays 22 532 544 10842307 10.1002/(SICI)1521-1878(200006)22:6<532::AID-BIES6>3.0.CO;2-O 1:CAS:528:DC%2BD3MXmslSiurg%3D (Pubitemid 30387974)
40. LA Li EF Chiang JC Chen NC Hsu YJ Chen BC Chung 1999 Function of steroidogenic factor 1 domains in nuclear localization, transactivation, and interaction with transcription factor TFIIB and c-Jun Mol Endocrinol 13 1588 1598 10478848 10.1210/me.13.9.1588 1:CAS:528:DyaK1MXmtVamtLg%3D (Pubitemid 30650598)
41. S Chopin-Delannoy S Thenot F Delaunay E Buisine A Begue M Duterque-Coquillaud V Laudet 2003 A specific and unusual nuclear localization signal in the DNA binding domain of the Rev-erb orphan receptors J Mol Endocrinol 30 197 211 12683943 10.1677/jme.0.0300197 1:CAS:528: DC%2BD3sXjs1eisrw%3D (Pubitemid 36592513)
42. IN Krylova EP Sablin J Moore RX Xu GM Waitt JA MacKay D Juzumiene JM Bynum K Madauss V Montana L Lebedeva M Suzawa JD Williams SP Williams RK Guy JW Thornton RJ Fletterick TM Willson HA Ingraham 2005 Structural analyses reveal phosphatidyl inositols as ligands for the NR5 orphan receptors SF-1 and LRH-1 Cell 120 343 355 15707893 10.1016/j.cell.2005.01.024 1:CAS:528: DC%2BD2MXhs1Krt74%3D (Pubitemid 40222429)
43. J Zhu Z Qiu C Wiese Y Ishii J Friedrichsen G Rajashekara GA Splitter 2005 Nuclear and mitochondrial localization signals overlap within bovine herpesvirus 1 tegument protein VP22 J Biol Chem 280 16038 16044 15705574 10.1074/jbc.M500054200 1:CAS:528:DC%2BD2MXjtleit74%3D (Pubitemid 40616728)
44. P Gu B Goodwin AC Chung X Xu DA Wheeler RR Price C Galardi L Peng AM Latour BH Koller J Gossen SA Kliewer AJ Cooney 2005 Orphan nuclear receptor LRH-1 is required to maintain Oct4 expression at the epiblast stage of embryonic development Mol Cell Biol 25 3492 3505 15831456 10.1128/MCB.25.9.3492-3505.2005 1:CAS:528:DC%2BD2MXjvFSmsbc%3D (Pubitemid 40575723)
45. JC Heng B Feng J Han J Jiang P Kraus JH Ng YL Orlov M Huss L Yang T Lufkin T Lufkin B Lim HH Ng 2010 The nuclear receptor Nr5a2 can replace Oct4 in the reprogramming of murine somatic cells to pluripotent cells Cell Stem Cell 6 167 174 20096661 10.1016/j.stem.2009.12.009 1:CAS:528:DC%2BC3cXlt1Knu7g%3D