Functional activity of RLIM/Rnf12 is regulated by phosphorylation-dependent nucleocytoplasmic shuttling

Molecular Biology of the Cell

Volumn 24, Issue 19, 2013, Pages 3085-3096

  Jiao, Baowei ^a,c   Taniguchi Ishigaki, Naoko ^a   Güngör, Cenap ^a,b   Peters, Marvin A ^b,d   Chen, Ya Wen ^a,e   Riethdorf, Sabine ^b   Drung, Alexander ^a   Ahronian, Leanne G ^a   Shin, Jongdae ^a   Pagnis, Rachna ^a   Pantel, Klaus ^b   Tachibana, Taro ^a,f   Lewis, Brian C ^a   Johnsen, Steven A ^b   Bach, Ingolf ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c KUNMING INSTITUTE OF ZOOLOGY   (China)

^d ROCHE INNOVATION CENTER MUNICH   (Germany)

^e NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^f Osaka Prefecture University   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; RLIM PROTEIN; SERINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST EPITHELIUM; CELL DIFFERENTIATION; CELL FUNCTION; CELL MEMBRANE; CELL MIGRATION; CELL NUCLEUS; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; EMBRYO DEVELOPMENT; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HETEROKARYON; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; INTRACELLULAR SPACE; KERATINOCYTE; LUNG ALVEOLUS CELL; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEOCYTOPLASMIC SHUTTLING; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; CELL SURVIVAL; EMBRYONIC DEVELOPMENT; EPIGENESIS, GENETIC; FEMALE; HELA CELLS; HUMANS; LIM DOMAIN PROTEINS; MAMMARY GLANDS, ANIMAL; MICE; PHOSPHORYLATION; PREGNANCY; SEX DETERMINATION PROCESSES; UBIQUITIN-PROTEIN LIGASES;

EID: 84884753179     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-05-0239     Document Type: Article

References (41)

1. Bach I (2000). The LIM domain: regulation by association. Mech Dev 91, 5-17.
2. Bach I, Carriere C, Ostendorff HP, Andersen B, Rosenfeld MG (1997). A family of LIM domain-associated cofactors confer transcriptional synergism between LIM and Otx homeodomain proteins. Genes Dev 11, 1370-1380.
3. Bach I, Ostendorff HP (2003). Orchestrating nuclear functions: ubiquitin sets the rhythm. Trends Biochem Sci 28, 189-195.
4. Bach I, Rodriguez-Esteban C, Carriere C, Bhushan A, Krones A, Rose DW, Glass CK, Andersen B, Izpisua Belmonte JC, Rosenfeld MG (1999). RLIM inhibits functional activity of LIM homeodomain transcription factors via recruitment of the histone deacetylase complex. Nat Genet 22, 394-399.
5. Barakat TS, Gunhanlar N, Pardo CG, Achame EM, Ghazvini M, Boers R, Kenter A, Rentmeester E, Grootegoed JA, Gribnau J (2011). RNF12 activates Xist and is essential for X chromosome inactivation. PLoS Genet 7, e1002001.
6. Campeau E, Ruhl VE, Rodier F, Smith CL, Rahmberg BL, Fuss JO, Campisi J, Yaswen P, Cooper PK, Kaufman PD (2009). A versatile viral system for expression and depletion of proteins in mammalian cells. PLoS One 4, e6529.
7. Chen YW, Klimstra DS, Mongeau ME, Tatem JL, Boyartchuk V, Lewis BC (2007). Loss of p53 and Ink4a/Arf cooperate in a cell autonomous fashion to induce metastasis of hepatocellular carcinoma cells. Cancer Res 67, 7589-7596.
8. Gontan C, Achame EM, Demmers J, Barakat TS, Rentmeester E, van IJcken W, Grootegoed JA, Gribnau J (2012). RNF12 initiates X-chromosome inactivation by targeting REX1 for degradation. Nature 485, 386-390.
9. Graveley BR (2000). Sorting out the complexity of SR protein functions. RNA 6, 1197-1211.
10. Gungor C, Taniguchi-Ishigaki N, Ma H, Drung A, Tursun B, Ostendorff HP, Bossenz M, Becker CG, Becker T, Bach I (2007). Proteasomal selection of multiprotein complexes recruited by LIM homeodomain transcription factors. Proc Natl Acad Sci USA 104, 15000-15005.
11. Her YR, Chung IK (2009). Ubiquitin ligase RLIM modulates telomere length homeostasis through a proteolysis of TRF1. J Biol Chem 284, 8557-8566.
12. Hervy M, Hoffman L, Beckerle MC (2006). From the membrane to the nucleus and back again: bifunctional focal adhesion proteins. Curr Opin Cell Biol 18, 524-532.
13. Huang Y, Yang Y, Gao R, Yang X, Yan X, Wang C, Jiang S, Yu L (2011). RLIM interacts with Smurf2 and promotes TGF-beta induced U2OS cell migration. Biochem Biophys Res Commun 414, 181-185.
14. Hunter T (2007). The age of crosstalk: phosphorylation, ubiquitination, and beyond. Mol Cell 28, 730-738.
15. Jiao B et al. (2012). Paternal RLIM/Rnf12 is a survival factor for milk-producing alveolar cells. Cell 149, 630-641.
16. Johnsen SA et al. (2009). Regulation of estrogen-dependent transcription by the LIM cofactors CLIM and RLIM in breast cancer. Cancer Res 69, 128-136.
17. Jonkers I, Barakat TS, Achame EM, Monkhorst K, Kenter A, Rentmeester E, Grosveld F, Gribnau J (2009). RNF12 is an X-encoded dose-dependent activator of X chromosome inactivation. Cell 139, 999-1011.
18. Kadrmas JL, Beckerle MC (2004). The LIM domain: from the cytoskeleton to the nucleus. Nat Rev Mol Cell Biol 5, 920-931.
19. Katahira J, Strasser K, Podtelejnikov A, Mann M, Jung JU, Hurt E (1999). The Mex67p-mediated nuclear mRNA export pathway is conserved from yeast to human. EMBO J 18, 2593-2609.
20. Kramer OH et al. (2003). The histone deacetylase inhibitor valproic acid selectively induces proteasomal degradation of HDAC2. EMBO J 22, 3411-3420.
21. Kudo N, Matsumori N, Taoka H, Fujiwara D, Schreiner EP, Wolff B, Yoshida M, Horinouchi S (1999). Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc Natl Acad Sci USA 96, 9112-9117.
22. Langdon SP (2004). Isolation and culture of ovarian cancer cell lines. Methods Mol Med 88, 133-139.
23. Lykke-Andersen J, Shu MD, Steitz JA (2001). Communication of the position of exon-exon junctions to the mRNA surveillance machinery by the protein RNPS1. Science 293, 1836-1839.
24. Olsen JV et al. (2010). Quantitative phosphoproteomics reveals wide-spread full phosphorylation site occupancy during mitosis. Sci Signal 12, ra3.
25. Ostendorff HP, Bossenz M, Mincheva A, Copeland NG, Gilbert DJ, Jenkins NA, Lichter P, Bach I (2000). Functional characterization of the gene encoding RLIM, the corepressor of LIM homeodomain factors. Genomics 69, 120-130.
26. Ostendorff HP, Peirano RI, Peters MA, Schlüter A, Bossenz M, Scheffner M, Bach I (2002). Ubiquitination-dependent cofactor exchange on LIM homeodomain transcription factors. Nature 416, 99-103.
27. Ostendorff HP, Tursun B, Cornils K, Schluter A, Drung A, Gungor C, Bach I (2006). Dynamic expression of LIM cofactors in the developing mouse neural tube. Dev Dyn 235, 786-791.
28. Pederson T (2008). As functional nuclear actin comes into view, is it globular, filamentous, or both? J Cell Biol 180, 1061-1064.
29. Pickart CM (2001). Mechanisms underlying ubiquitination. Annu Rev Biochem 70, 503-533.
30. Pollard VW, Malim MH (1998). The HIV-1 Rev protein. Annu Rev Microbiol 52, 491-532.
31. Sanford JR, Ellis JD, Cazalla D, Caceres JF (2005). Reversible phosphorylation differentially affects nuclear and cytoplasmic functions of splicing factor 2/alternative splicing factor. Proc Natl Acad Sci USA 102, 15042-15047.
32. Shin J et al. (2010). Maternal Rnf12/RLIM is required for imprinted X-chromosome inactivation in mice. Nature 467, 977-981.
33. Tursun B et al. (2005). The ubiquitin ligase Rnf6 regulates local LIM kinase 1 levels in axonal growth cones. Genes Dev 19, 2307-2319.
34. Visa N, Percipalle P (2010). Nuclear functions of actin. Cold Spring Harb Perspect Biol 2, a000620.
35. Visvader JE, Venter D, Hahm K, Santamaria M, Sum EY, O'Reilly L, White D, Williams R, Armes J, Lindeman GJ (2001). The LIM domain gene LMO4 inhibits differentiation of mammary epithelial cells in vitro and is overexpressed in breast cancer. Proc Natl Acad Sci USA 98, 14452-14457.
36. Vucic D, Dixit VM, Wertz IE (2011). Ubiquitylation in apoptosis: a post-translational modification at the edge of life and death. Nat Rev Mol Cell Biol 12, 439-452.
37. Wagner KU, Wall RJ, St Onge L, Gruss P, Wynshaw-Boris A, Garrett L, Li M, Furth PA, Hennighausen L (1997). Cre-mediated gene deletion in the mammary gland. Nucleic Acids Res 25, 4323-4330.
38. Wang N, Kudryavtseva E, Ch'en IL, McCormick J, Sugihara TM, Ruiz R, Andersen B (2004). Expression of an engrailed-LMO4 fusion protein in mammary epithelial cells inhibits mammary gland development in mice. Oncogene 23, 1507-1513.
39. Windle JJ, Weiner RI, Mellon PL (1990). Cell lines of the pituitary gonadotrope lineage derived by targeted oncogenesis in transgenic mice. Mol Endocrinol 4, 597-603.
40. Xu K et al. (2009). Regulation of androgen receptor transcriptional activity and specificity by RNF6-induced ubiquitination. Cancer Cell 15, 270-282.
41. Zhang L et al. (2012). RNF12 controls embryonic stem cell fate and mor-phogenesis in zebrafish embryos by targeting Smad7 for degradation. Mol Cell 46, 650-661