Functional and molecular insights into KSRP function in mRNA decay

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1829, Issue 6-7, 2013, Pages 689-694

  Briata, Paola ^a   Chen, Ching Yi ^b   Ramos, Andres ^c   Gherzi, Roberto ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Extracellular signal; KH domain; MicroRNA maturation; MRNA decay

Indexed keywords

INTERLEUKIN 6; INTERLEUKIN 8; KH TYPE SPLICING REGULATORY PROTEIN; NUCLEIC ACID BINDING PROTEIN; PROTEIN C FOS; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; CELL DIFFERENTIATION; DOWN REGULATION; EXOSOME; GENE DELETION; GENETIC TRANSCRIPTION; HALF LIFE TIME; HUMAN; MICRORNA DECAY; NONHUMAN; NUCLEIC ACID STRUCTURE, METABOLISM AND FUNCTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW; RNA DEGRADATION; RNA SPLICING; SIGNAL TRANSDUCTION;

BINDING SITES; CELL LINE; GENE EXPRESSION REGULATION; HUMANS; MICRORNAS; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS; TRANS-ACTIVATORS;

EID: 84877811576     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2012.11.003     Document Type: Review

References (58)

1. Gherzi R., Chen C.-Y., Trabucchi M., Ramos A., Briata P. The role of KSRP in mRNA decay and microRNA precursor maturation. Wiley Interdiscip. Rev. RNA 2010, 1:230-239.
2. Gherzi R., Trabucchi M., Ponassi M., Ruggiero T., Corte G., Moroni C., Chen C.Y., Khabar K.S., Andersen J.S., Briata P. The RNA-binding protein KSRP promotes decay of beta-catenin mRNA and is inactivated by PI3K-AKT signaling. PLoS Biol. 2006, 5:e5.
3. Zhang X., Wan G., Berger F.G., He X., Lu X. The ATM kinase induces microRNA biogenesis in the DNA damage response. Mol. Cell 2011, 41:371-383.
4. Briata P., Forcales S.V., Ponassi M., Corte G., Chen C.Y., Karin M., Puri P.L., Gherzi R. p38-Dependent phosphorylation of the mRNA decay-promoting factor KSRP controls the stability of select myogenic transcripts. Mol. Cell 2005, 20:891-903.
5. Davis-Smyth T., Duncan R.C., Zheng T., Michelotti G., Levens D. The far upstream element-binding proteins comprise an ancient family of single-strand DNA-binding transactivators. J. Biol. Chem. 1996, 271:31679-31687.
6. Min H., Turck C.W., Nikolic J.M., Black D.L. A new regulatory protein, KSRP, mediates exon inclusion through an intronic splicing enhancer. Genes Dev. 1997, 11:1023-1036.
7. Lellek H., Kirsten R., Diehl I., Apostel F., Buck F., Greeve J. Purification and molecular cloning of a novel essential component of the apolipoprotein B mRNA editing enzyme-complex. J. Biol. Chem. 2000, 275:19848-19856.
8. Hao S., Baltimore D. The stability of mRNA influences the temporal order of the induction of genes encoding inflammatory molecules. Nat. Immunol. 2009, 10:281-288.
9. Gingerich T.J., Feige J.J., LaMarre J. AU-rich elements and the control of gene expression through regulated mRNA stability. Anim. Health Res. Rev. 2004, 5:49-63.
10. Wu X., Brewer G. The regulation of mRNA stability in mammalian cells: 2.0. Gene 2012, 500:10-21.
11. Beisang D., Bohjanen P.R. Perspectives on the ARE as it turns 25years old. Wiley Interdiscip. Rev. RNA 2012, 3:719-731.
12. Chen C.Y., Gherzi R., Ong S.E., Chan E.L., Raijmakers R., Pruijn G.J., Stoecklin G., Moroni C., Mann M., Karin M. AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 2001, 107:451-464.
13. Gherzi R., Lee K.Y., Briata P., Wegmuller D., Moroni C., Karin M., Chen C.Y. A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Mol. Cell 2004, 14:571-583.
14. Chou C.F., Mulky A., Maitra S., Lin W.J., Gherzi R., Kappes J., Chen C.-Y. Tethering KSRP, a decay-promoting AU-rich element-binding protein, to mRNAs elicits mRNA decay. Mol. Cell. Biol. 2006, 26:3695-3706.
15. Winzen R., Thakur B.K., Dittrich-Breiholz O., Shah M., Redich N., Dhamija S., Kracht M., Holtmann H. Functional analysis of KSRP interaction with the AU-rich element of interleukin-8 and identification of inflammatory mRNA targets. Mol. Cell. Biol. 2007, 27:8388-8400.
16. Briata P., Ilengo C., Corte G., Moroni C., Rosenfeld M.G., Chen C.Y., Gherzi R. The Wnt/beta-catenin->Pitx2 pathway controls the turnover of Pitx2 and other unstable mRNAs. Mol. Cell 2003, 12:1201-1211.
17. Ruggiero T., Trabucchi M., Ponassi M., Corte G., Chen C.Y., al-Haj L., Khabar K.S., Briata P., Gherzi R. Identification of a set of KSRP target transcripts upregulated by PI3K-AKT signaling. BMC Mol. Biol. 2007, 8:28.
18. Ben-Dov I.Z., Briata P., Gherzi R., Naveh-Many T. The mRNA decay promoting factor K-homology splicing regulator protein post-transcriptionally determines parathyroid hormone mRNA levels. FASEB J. 2008, 22:3458-3468.
19. Linker K., Pautz A., Fechir M., Hubrich T., Greeve J., Kleinert H. Involvement of KSRP in the post-transcriptional regulation of human iNOS expression-complex interplay of KSRP with TTP and HuR. Nucleic Acids Res. 2005, 33:4813-4827.
20. Dhamija S., Kuehne N., Winzen R., Doerrie A., Dittrich-Breiholz O., Thakur B.K., Kracht M., Holtmann H. Interleukin-1 activates synthesis of interleukin-6 by interfering with a KH-type splicing regulatory protein (KSRP)-dependent translational silencing mechanism. J. Biol. Chem. 2011, 286:33279-33288.
21. Krol J., Loedige I., Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 2010, 11:597-610.
22. Jing Q., Huang S., Guth S., Zarubin T., Motoyama A., Chen J., Di Padova F., Lin S.C., Gram H., Han J. Involvement of microRNA in AU-rich element-mediated mRNA instability. Cell 2005, 120:623-634.
23. Srikantan S., Tominaga K., Gorospe M. Functional interplay between RNA-binding protein HuR and microRNAs. Curr. Protein Pept. Sci. 2012, 13:372-379.
24. Trabucchi M., Briata P., Garcia-Mayoral M.F., Haase A.D., Filipowicz W., Ramos A., Gherzi R., Rosenfeld M.G. The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature 2009, 459:1010-1014.
25. Liu Y., Liu Q. ATM signals miRNA biogenesis through KSRP. Mol. Cell 2011, 41:367-368.
26. Michlewski G., Cáceres J.F. Antagonistic role of hnRNP A1 and KSRP in the regulation of let-7a biogenesis. Nat. Struct. Mol. Biol. 2010, 17:1011-1018.
27. Ruggiero T., Trabucchi M., De Santa F., Zupo S., Harfe B.D., McManus M.T., Rosenfeld M.G., Briata P., Gherzi R. LPS induces KH-type splicing regulatory protein-dependent processing of microRNA-155 precursors in macrophages. FASEB J. 2009, 23:2898-2908.
28. Briata P., Lin W.J., Giovarelli M., Pasero M., Chou C.F., Trabucchi M., Rosenfeld M.G., Chen C.Y., Gherzi R. PI3K/AKT signaling determines a dynamic switch between distinct KSRP functions favoring skeletal myogenesis. Cell Death Differ. 2012, 19:478-487.
29. Trabucchi M., Briata P., Filipowicz W., Rosenfeld M.G., Ramos A., Gherzi R. How to control miRNA maturation?. RNA Biol. 2009, 6:536-540.
30. Rüegger S., Großhans H. MicroRNA turnover: when, how, and why. Trends Biochem. Sci. 2012, 37:436-446.
31. Repetto E., Briata P., Kuziner N., Harfe B.D., McManus M.T., Gherzi R., Rosenfeld M.G., Trabucchi M. Let-7b/c enhance the stability of a tissue-specific mRNA during Mammalian organogenesis as part of a feedback loop involving KSRP. PLoS Genet. 2012, 8:e1002823.
32. Zhou R., Gong A.Y., Eischeid A.N., Chen X.M. miR-27b targets KSRP to coordinate TLR4-mediated epithelial defense against Cryptosporidium parvum infection. PLoS Pathog. 2012, 8:e1002702.
33. Stumpo D.J., Lai W.S., Blackshear P.J. Inflammation: cytokines and RNA-based regulation. Wiley Interdiscip. Rev. RNA 2010, 1:60-80.
34. Sandler H., Stoecklin G. Control of mRNA decay by phosphorylation of tristetraprolin. Biochem. Soc. Trans. 2008, 36:491-496.
35. Maitra S., Chou C.F., Luber C.A., Lee K.Y., Mann M., Chen C.-Y. The AU-rich element mRNA decay-promoting activity of BRF1 is regulated by mitogen-activated protein kinase-activated protein kinase 2. RNA 2008, 14:950-959.
36. Danckwardt S., Gantzert A.S., Macher-Goeppinger S., Probst H.C., Gentzel M., Wilm M., Gröne H.J., Schirmacher P., Hentze M.W., Kulozik A.E. p38 MAPK controls prothrombin expression by regulated RNA 3' end processing. Mol. Cell 2011, 41:298-310.
37. Vasudevan K.M., Garraway L.A. AKT signaling in physiology and disease. Curr. Top. Microbiol. Immunol. 2010, 347:105-133.
38. Díaz-Moreno I., Hollingworth D., Frenkiel T.A., Kelly G., Martin S., Howell S., García-Mayoral M.F., Gherzi R., Briata P., Ramos A. Phosphorylation-mediated unfolding of a KH domain regulates KSRP localization via 14-3-3 binding. Nat. Struct. Mol. Biol. 2009, 16:238-246.
39. Bikkavilli R.K., Malbon C.C. Dishevelled-KSRP complex regulates Wnt signaling through post-transcriptional stabilization of beta-catenin mRNA. J. Cell Sci. 2010 Apr 15, 123(Pt 8):1352-1362.
40. Tullai J.W., Graham J.R., Cooper G.M. A GSK-3-mediated transcriptional network maintains repression of immediate early genes in quiescent cells. Cell Cycle 2011, 10:3072-3077.
41. Graham J.R., Hendershott M.C., Terragni J., Cooper G.M. mRNA degradation plays a significant role in the program of gene expression regulated by phosphatidylinositol 3-kinase signaling. Mol. Cell. Biol. 2010, 30:5295-5305.
42. Tajbakhsh S. Skeletal muscle stem cells in developmental versus regenerative myogenesis. J. Intern. Med. 2009, 266:372-389.
43. Lin W.J., Zheng X., Lin C.C., Tsao J., Zhu X., Cody J.J., Coleman J.M., Gherzi R., Luo M., Townes T.M., Parker J.N., Chen C.Y. Posttranscriptional control of type I interferon genes by KSRP in the innate immune response against viral infection. Mol. Cell. Biol. 2011, 31:3196-3207.
44. Li X., Lin W.J., Chen C.Y., Si Y., Zhang X., Lu L., Suswam E., Zheng L., King P.H. KSRP: a checkpoint for inflammatory cytokine production in astrocytes. Glia 2012, 60:1773-1784.
45. Liu N., Williams A.H., Maxeiner J.M., Bezprozvannaya S., Shelton J.M., Richardson J.A., Bassel-Duby R., Olson E.N. microRNA-206 promotes skeletal muscle regeneration and delays progression of Duchenne muscular dystrophy in mice. J. Clin. Invest. 2012, 122:2054-2065.
46. Nevins A.K., Thurmond D.C. Caveolin-1 functions as a novel Cdc42 guanine nucleotide dissociation inhibitor in pancreatic beta-cells. J. Biol. Chem. 2006, 281:18961-18972.
47. Valverde R., Edwards L., Regan L. Structure and function of KH domains. FEBS J. 2008, 275:2712-2726.
48. Lewis H.A., Musunuru K., Jensen K.B., Edo C., Chen H., Darnell R.B., Burley S.K. Sequence-specific RNA binding by a Nova KH domain: implications for paraneoplastic disease and the fragile X syndrome. Cell 2000, 100:323-332.
49. Braddock D.T., Louis J.M., Baber J.L., Levens D., Clore G.M. Structure and dynamics of KH domains from FBP bound to single-stranded DNA. Nature 2002, 415:1051-1056.
50. Garcia-Mayoral M.F., Hollingworth D., Masino L., Diaz-Moreno I., Kelly G., Gherzi R., Chou C.F., Chen C.-Y., Ramos A. The structure of the C-terminal domains of KSRP reveals a new element important to mRNA degradation. Structure 2007, 15:485-498.
51. Beuth B., Garcia-Mayoral M.F., Taylor I.A., Ramos A. Scaffold independent analysis of RNA-protein interactions: the Nova-1 KH3-RNA complex. J. Am. Chem. Soc. 2007, 129:10205-10210.
52. García-Mayoral M.F., Díaz-Moreno I., Hollingworth D., Ramos A. The sequence selectivity of KSRP explains its flexibility in the recognition of the RNA targets. Nucleic Acids Res. 2008, 36:5290-5296.
53. Hollingworth D., Candel A.M., Nicastro G., Martin S.R., Briata P., Gherzi R., Ramos A. KH domains with impaired nucleic acid binding as a tool for functional analysis. Nucleic Acid Res. 2012, 40:6873-6886.
54. G. Nicastro, M.F. García-Mayoral, D. Hollingworth, G. Kelly, S.R. Martin, P. Briata, R. Gherzi, A. Ramos, Non-canonical Guanine recognition mediates KSRP regulation of Let-7 biogenesis, Nat. Struct. Mol. Biol. in press.
55. Lunde B.M., Moore C., Varani G. RNA-binding proteins: modular design for efficient function. Nat. Rev. Mol. Cell Biol. 2007, 8:479-490.
56. Markovtsov V., Nikolic J.M., Goldman J.A., Turck C.W., Chou M.Y., Black D.L. Cooperative assembly of an hnRNP complex induced by a tissue-specific homolog of polypyrimidine tract binding protein. Mol. Cell. Biol. 2000, 20:7463-7479.
57. Cukier C.D., Hollingworth D., Kelly G., Martin S.R., Díaz-Moreno I., Ramos A. Molecular basis of FIR-mediated c-myc transcriptional control. Nat. Struct. Mol. Biol. 2010, 17:1058-1064.
58. Russo A., Catillo M., Esposito D., Briata P., Pietropaolo C., Russo G. Autoregulatory circuit of human rpL3 expression requires hnRNP H1, NPM and KHSRP. Nucleic Acids Res. 2011, 39:7576-7585.