The role of Trim25 in development, disease and RNA metabolism

Biochemical Society Transactions

Volumn 44, Issue 4, 2016, Pages 1045-1050

  Heikel, Gregory ^a   Choudhury, Nila Roy ^a   Michlewski, Gracjan ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

E3 ubiquitin ligase; Novel RNA binding proteins; RNA metabolism; Trim25

Indexed keywords

ESTROGEN; RNA; RNA BINDING PROTEIN; TRIM25 PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; TRANSCRIPTION FACTOR; TRIM25 PROTEIN, HUMAN; TRIM25 PROTEIN, MOUSE; TRIPARTITE MOTIF PROTEIN; UBIQUITIN PROTEIN LIGASE;

ARTICLE; DEVELOPMENT; DISEASES; HUMAN; INNATE IMMUNITY; MALIGNANT NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RNA METABOLISM; UTERUS; ANIMAL; BIOLOGICAL MODEL; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOUSE;

ANIMALS; DISEASE; DNA-BINDING PROTEINS; FEMALE; HUMANS; MICE; MODELS, GENETIC; RNA; TRANSCRIPTION FACTORS; TRIPARTITE MOTIF PROTEINS; UBIQUITIN-PROTEIN LIGASES; UTERUS;

EID: 85009809694     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20160077     Document Type: Article

References (51)

1. Versteeg, G.A., Benke, S., Garcia-Sastre, A. and Rajsbaum, R. (2014) InTRIMsic immunity: positive and negative regulation of immune signaling by tripartite motif proteins. Cytokine Growth Factor Rev. 25, 563-576 CrossRef PubMed.
2. Kwon, S.C., Yi, H., Eichelbaum, K., Fohr, S., Fischer, B., You, K.T., Castello, A., Krijgsveld, J., Hentze, M.W. and Kim, V.N. (2013) The RNA-binding protein repertoire of embryonic stem cells. Nat. Struct. Mol. Biol. 20, 1122-1130 CrossRef PubMed.
3. Castello, A., Fischer, B., Eichelbaum, K., Horos, R., Beckmann, B.M., Strein, C., Davey, N.E., Humphreys, D.T., Preiss, T., Steinmetz, L.M. et al. (2012) Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 149, 1393-1406 CrossRef PubMed.
4. Beckmann, B.M., Horos, R., Fischer, B., Castello, A., Eichelbaum, K., Alleaume, A.M., Schwarzl, T., Curk, T., Foehr, S., Huber, W. et al. (2015) The RNA-binding proteomes from yeast to man harbour conserved enigmRBPs. Nat. Commun. 6, 10127 CrossRef PubMed.
5. Cano, F., Miranda-Saavedra, D. and Lehner, P.J. (2010) RNA-binding E3 ubiquitin ligases: novel players in nucleic acid regulation. Biochem. Soc. Trans. 38, 1621-1626 CrossRef PubMed.
6. Komander, D. and Rape, M. (2012) The ubiquitin code. Annu. Rev. Biochem. 81, 203-229 CrossRef PubMed.
7. Choudhury, N.R., Nowak, J.S., Zuo, J., Rappsilber, J., Spoel, S.H. and Michlewski, G. (2014) Trim25 is an RNA-specific activator of Lin28a/TuT4-mediated uridylation. Cell Rep. 9, 1265-1272 CrossRef PubMed.
8. Inoue, S., Orimo, A., Hosoi, T., Kondo, S., Toyoshima, H., Kondo, T., Ikegami, A., Ouchi, Y., Orimo, H. and Muramatsu, M. (1993) Genomic binding-site cloning reveals an estrogen-responsive gene that encodes a RING finger protein. Proc. Natl. Acad. Sci. U.S.A. 90, 11117-11121 CrossRef PubMed.
9. Orimo, A., Inoue, S., Ikeda, K., Noji, S. and Muramatsu, M. (1995) Molecular cloning, structure, and expression of mouse estrogen-responsive finger protein Efp. Co-localization with estrogen receptor mRNA in target organs. J. Biol. Chem. 270, 24406-24413 CrossRef PubMed.
10. Orimo, A., Inoue, S., Minowa, O., Tominaga, N., Tomioka, Y., Sato, M., Kuno, J., Hiroi, H., Shimizu, Y., Suzuki, M. et al. (1999) Underdeveloped uterus and reduced estrogen responsiveness in mice with disruption of the estrogen-responsive finger protein gene, which is a direct target of estrogen receptor alpha. Proc. Natl. Acad. Sci. U.S.A. 96, 12027-12032 CrossRef PubMed.
11. Nakajima, A., Maruyama, S., Bohgaki, M., Miyajima, N., Tsukiyama, T., Sakuragi, N. and Hatakeyama, S. (2007) Ligand-dependent transcription of estrogen receptor alpha is mediated by the ubiquitin ligase EFP. Biochem. Biophys. Res. Commun. 357, 245-251 CrossRef PubMed.
12. Dong, X.Y., Fu, X., Fan, S., Guo, P., Su, D. and Dong, J.T. (2012) Oestrogen causes ATBF1 protein degradation through the oestrogen-responsive E3 ubiquitin ligase EFP. Biochem. J. 444, 581-590 CrossRef PubMed.
13. Zhao, K.W., Sikriwal, D., Dong, X., Guo, P., Sun, X. and Dong, J.T. (2011) Oestrogen causes degradation of KLF5 by inducing the E3 ubiquitin ligase EFP in ER-positive breast cancer cells. Biochem J. 437, 323-333 CrossRef PubMed.
14. Ikeda, K., Orimo, A., Higashi, Y., Muramatsu, M. and Inoue, S. (2000) Efp as a primary estrogen-responsive gene in human breast cancer. FEBS Lett. 472, 9-13 CrossRef PubMed.
15. Urano, T., Saito, T., Tsukui, T., Fujita, M., Hosoi, T., Muramatsu, M., Ouchi, Y. and Inoue, S. (2002) Efp targets 14-3-3 sigma for proteolysis and promotes breast tumour growth. Nature 417, 871-875 CrossRef PubMed.
16. Thomson, S.D., Ali, S., Pickles, L., Taylor, J., Pace, P.E., Lymboura, M., Shousha, S. and Coombes, R.C. (2001) Analysis of estrogen-responsive finger protein expression in benign and malignant human breast. Int. J. Cancer 91, 152-158 CrossRef PubMed.
17. Suzuki, T., Urano, T., Tsukui, T., Horie-Inoue, K., Moriya, T., Ishida, T., Muramatsu, M., Ouchi, Y., Sasano, H. and Inoue, S. (2005) Estrogen-responsive finger protein as a new potential biomarker for breast cancer. Clin. Cancer Res. 11, 6148-6154 CrossRef PubMed.
18. Qin, Y., Cui, H. and Zhang, H. (2015) Overexpression of TRIM25 in lung cancer regulates tumor cell progression. Technol. Cancer Res. Treat, doi:10.1177/1533034615595903.
19. Sakuma, M., Akahira, J., Suzuki, T., Inoue, S., Ito, K., Moriya, T., Sasano, H., Okamura, K. and Yaegashi, N. (2005) Expression of estrogen-responsive finger protein (Efp) is associated with advanced disease in human epithelial ovarian cancer. Gynecol. Oncol. 99, 664-670 CrossRef PubMed.
20. Dai, H., Zhang, P., Zhao, S., Zhang, J. and Wang, B. (2009) Regulation of the vascular endothelial growth factor and growth by estrogen and antiestrogens through Efp in Ishikawa endometrial carcinoma cells. Oncol. Rep. 21, 395-401 PubMed.
21. Zhu, Z., Wang, Y., Zhang, C., Yu, S., Zhu, Q., Hou, K. and Yan, B. (2016) TRIM25 blockade by RNA interference inhibited migration and invasion of gastric cancer cells through TGF-beta signaling. Sci. Rep. 6, 19070 CrossRef PubMed.
22. p53/Mdm2 circuit. Oncogene 34, 5729-5738 CrossRef PubMed.
23. Ozato, K., Shin, D.M., Chang, T.H. and Morse 3rd, H.C. (2008) TRIM family proteins and their emerging roles in innate immunity. Nat. Rev. Immunol. 8, 849-860 CrossRef PubMed.
24. Versteeg, G.A., Rajsbaum, R., Sanchez-Aparicio, M.T., Maestre, A.M., Valdiviezo, J., Shi, M., Inn, K.S., Fernandez-Sesma, A., Jung, J. and Garcia-Sastre, A. (2013) The E3-ligase TRIM family of proteins regulates signaling pathways triggered by innate immune pattern-recognition receptors. Immunity 38, 384-398 CrossRef PubMed.
25. Yoneyama, M., Kikuchi, M., Natsukawa, T., Shinobu, N., Imaizumi, T., Miyagishi, M., Taira, K., Akira, S. and Fujita, T. (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5, 730-737 CrossRef PubMed.
26. Loo, Y.M. and Gale, Jr M. (2011) Immune signaling by RIG-I-like receptors. Immunity 34, 680-692 CrossRef PubMed.
27. Gack, M.U., Shin, Y.C., Joo, C.H., Urano, T., Liang, C., Sun, L., Takeuchi, O., Akira, S., Chen, Z., Inoue, S. and Jung, J.U. (2007) TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446, 916-920 CrossRef PubMed.
28. Gack, M.U., Kirchhofer, A., Shin, Y.C., Inn, K.S., Liang, C., Cui, S., Myong, S., Ha, T., Hopfner, K.P. and Jung, J.U. (2008) Roles of RIG-I N-terminal tandem CARD and splice variant in TRIM25-mediated antiviral signal transduction. Proc. Natl. Acad. Sci. U.S.A. 105, 16743-16748 CrossRef PubMed.
29. Zeng, W., Sun, L., Jiang, X., Chen, X., Hou, F., Adhikari, A., Xu, M. and Chen, Z.J. (2010) Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 141, 315-330 CrossRef PubMed.
30. Gack, M.U., Albrecht, R.A., Urano, T., Inn, K.S., Huang, I.C., Carnero, E., Farzan, M., Inoue, S., Jung, J.U. and Garcia-Sastre, A. (2009) Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe 5, 439-449 CrossRef PubMed.
31. Donelan, N.R., Basler, C.F. and Garcia-Sastre, A. (2003) A recombinant influenza A virus expressing an RNA-binding-defective NS1 protein induces high levels of beta interferon and is attenuated in mice. J. Virol. 77, 13257-13266 CrossRef PubMed.
32. Inn, K.S., Gack, M.U., Tokunaga, F., Shi, M., Wong, L.Y., Iwai, K. and Jung, J.U. (2011) Linear ubiquitin assembly complex negatively regulates RIG-I-and TRIM25-mediated type I interferon induction. Mol. Cell 41, 354-365 CrossRef PubMed.
33. Cook, K.B., Kazan, H., Zuberi, K., Morris, Q. and Hughes, T.R. (2011) RBPDB: A database of RNA-binding specificities. Nucleic Acids Res. 39, D301-D308 CrossRef PubMed.
34. Baltz, A.G., Munschauer, M., Schwanhausser, B., Vasile, A., Murakawa, Y., Schueler, M., Youngs, N., Penfold-Brown, D., Drew, K., Milek, M. et al. (2012) The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol. Cell 46, 674-690 CrossRef PubMed.
35. Moss, E.G., Lee, R.C. and Ambros, V. (1997) The cold shock domain protein LIN-28 controls developmental timing in C. elegans and is regulated by the lin-4 RNA. Cell 88, 637-646 CrossRef PubMed.
36. Moss, E.G. and Tang, L. (2003) Conservation of the heterochronic regulator Lin-28, its developmental expression and microRNA complementary sites. Dev. Biol. 258, 432-442 CrossRef PubMed.
37. Seggerson, K., Tang, L. and Moss, E.G. (2002) Two genetic circuits repress the Caenorhabditis elegans heterochronic gene lin-28 after translation initiation. Dev. Biol. 243, 215-225 CrossRef PubMed.
38. Darr, H. and Benvenisty, N. (2009) Genetic analysis of the role of the reprogramming gene LIN-28 in human embryonic stem cells. Stem Cells 27, 352-362 CrossRef PubMed.
39. Van Wynsberghe, P.M., Kai, Z.S., Massirer, K.B., Burton, V.H., Yeo, G.W. and Pasquinelli, A.E. (2011) LIN-28 co-transcriptionally binds primary let-7 to regulate miRNA maturation in Caenorhabditis elegans. Nat. Struct. Mol. Biol. 18, 302-308 CrossRef PubMed.
40. Nowak, J.S., Choudhury, N.R., de Lima Alves, F., Rappsilber, J. and Michlewski, G. (2014) Lin28a regulates neuronal differentiation and controls miR-9 production. Nat. Commun. 5, 3687 PubMed.
41. Michlewski, G., Guil, S., Semple, C.A. and Caceres, J.F. (2008) Posttranscriptional regulation of miRNAs harboring conserved terminal loops. Mol. Cell 32, 383-393 CrossRef PubMed.
42. Newman, M.A., Thomson, J.M. and Hammond, S.M. (2008) Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing. RNA 14, 1539-1549 CrossRef PubMed.
43. Rybak, A., Fuchs, H., Smirnova, L., Brandt, C., Pohl, E.E., Nitsch, R. and Wulczyn, F.G. (2008) A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat. Cell Biol. 10, 987-993 CrossRef PubMed.
44. Wulczyn, F.G., Smirnova, L., Rybak, A., Brandt, C., Kwidzinski, E., Ninnemann, O., Strehle, M., Seiler, A., Schumacher, S. and Nitsch, R. (2007) Post-transcriptional regulation of the let-7 microRNA during neural cell specification. FASEB J 21, 415-426 CrossRef PubMed.
45. Hagan, J.P., Piskounova, E. and Gregory, R.I. (2009) Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nat. Struct. Mol. Biol. 16, 1021-1025 CrossRef PubMed.
46. Heo, I., Joo, C., Kim, Y.K., Ha, M., Yoon, M.J., Cho, J., Yeom, K.H., Han, J. and Kim, V.N. (2009) TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 138, 696-708 CrossRef PubMed.
47. Chang, H.M., Triboulet, R., Thornton, J.E. and Gregory, R.I. (2013) A role for the Perlman syndrome exonuclease Dis3l2 in the Lin28-let-7 pathway. Nature 497, 244-248 CrossRef PubMed.
48. Ustianenko, D., Hrossova, D., Potesil, D., Chalupnikova, K., Hrazdilova, K., Pachernik, J., Cetkovska, K., Uldrijan, S., Zdrahal, Z. and Vanacova, S. (2013) Mammalian DIS3L2 exoribonuclease targets the uridylated precursors of let-7 miRNAs. RNA 19, 1632-1638 CrossRef PubMed.
49. Wilbert, M.L., Huelga, S.C., Kapeli, K., Stark, T.J., Liang, T.Y., Chen, S.X., Yan, B.Y., Nathanson, J.L., Hutt, K.R., Lovci, M.T. et al. (2012) LIN28 binds messenger RNAs at GGAGA motifs and regulates splicing factor abundance. Mol. Cell 48, 195-206 CrossRef PubMed.
50. Yoon, J.H., Abdelmohsen, K., Kim, J., Yang, X., Martindale, J.L., Tominaga-Yamanaka, K., White, E.J., Orjalo, A.V., Rinn, J.L., Kreft, S.G. et al. (2013) Scaffold function of long non-coding RNA HOTAIR in protein ubiquitination. Nat. Commun. 4, 2939 CrossRef PubMed.
51. Ghosh, P. and Sowdhamini, R. (2016) Genome-wide survey of putative RNA-binding proteins encoded in the human proteome. Mol. Biosyst. 12, 532-540 CrossRef PubMed.