CK2-mediated TEL2 phosphorylation augments nonsense-mediated mRNA decay (NMD) by increase of SMG1 stability

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1829, Issue 10, 2013, Pages 1047-1055

  Ahn, Seyoung ^a   Kim, Jinyoung ^a   Hwang, Jungwook ^a  

^a Hanyang University   (South Korea)

Author keywords

CK2; MRNP remodeling; NMD; SMG1; TEL2 phosphorylation; UPF1

Indexed keywords

1 JOIN HETERODIMERIC EUKARYOTIC TRANSLATION RELEASE FACTOR; CASEIN KINASE II; CYCLOHEXIMIDE; INITIATION FACTOR; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN SERINE THREONINE KINASE; SMALL INTERFERING RNA; SUPPRESSOR WITH MORPHOLOGICAL EFFECT ON GENITALIA; UNCLASSIFIED DRUG; UP FRAMESHIFT FACTOR 1;

ARTICLE; CASEIN KINASE II MEDIATED TELOMERE MAINTENANCE 2 PHOSPHORYLATION; COMPLEX FORMATION; DOWN REGULATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; NONSENSE MEDIATED MRNA DECAY; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN STABILITY; TELOMERE; TRANSLATION REGULATION; UPREGULATION; WESTERN BLOTTING;

CK2; MRNP REMODELING; NMD; SMG1; TEL2 PHOSPHORYLATION; UPF1;

BLOTTING, WESTERN; CASEIN KINASE II; CODON, NONSENSE; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; NONSENSE MEDIATED MRNA DECAY; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-ETS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA STABILITY; RNA, MESSENGER; RNA, SMALL INTERFERING; TRANS-ACTIVATORS;

EID: 84880970788     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2013.06.002     Document Type: Article

References (39)

1. Hwang J., Maquat L.E. Nonsense-mediated mRNA decay (NMD) in animal embryogenesis: to die or not to die, that is the question. Curr. Opin. Genet. Dev. 2011, 21:422-430.
2. Mendell J.T., Sharifi N.A., Meyers J.L., Martinez-Murillo F., Dietz H.C. Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat. Genet. 2004, 36:1073-1078.
3. Schoenberg D.R., Maquat L.E. Regulation of cytoplasmic mRNA decay. Nat. Rev. Genet. 2012, 13:246-259.
4. Shoemaker C.J., Green R. Translation drives mRNA quality control. Nat. Struct. Mol. Biol. 2012, 19:594-601.
5. Hwang J., Kim Y.K. When a ribosome encounters a premature termination codon. BMB Rep. 2013, 46:9-16.
6. Lewis B.P., Green R.E., Brenner S.E. Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:189-192.
7. Khajavi M., Inoue K., Lupski J.R. Nonsense-mediated mRNA decay modulates clinical outcome of genetic disease. Eur. J. Hum. Genet. 2006, 14:1074-1081.
8. Gardner L.B. Nonsense-mediated RNA decay regulation by cellular stress: implications for tumorigenesis. Mol. Cancer Res. 2010, 8:295-308.
9. Kashima I., Yamashita A., Izumi N., Kataoka N., Morishita R., Hoshino S., Ohno M., Dreyfuss G., Ohno S. Binding of a novel SMG-1-Upf1-eRF1-eRF3 complex (SURF) to the exon junction complex triggers Upf1 phosphorylation and nonsense-mediated mRNA decay. Genes Dev. 2006, 20:355-367.
10. Singh G., Rebbapragada I., Lykke-Andersen J. A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol. 2008, 6:e111.
11. Izumi N., Yamashita A., Ohno S. Integrated regulation of PIKK-mediated stress responses by AAA+ proteins RUVBL1 and RUVBL2. Nucleus 2012, 3:29-43.
12. Kashima I., Jonas S., Jayachandran U., Buchwald G., Conti E., Lupas A.N., Izaurralde E. SMG6 interacts with the exon junction complex via two conserved EJC-binding motifs (EBMs) required for nonsense-mediated mRNA decay. Genes Dev. 2010, 24:2440-2450.
13. Okada-Katsuhata Y., Yamashita A., Kutsuzawa K., Izumi N., Hirahara F., Ohno S. N- and C-terminal Upf1 phosphorylations create binding platforms for SMG-6 and SMG-5:SMG-7 during NMD. Nucleic Acids Res. 2012, 40:1251-1266.
14. Collis S.J., Barber L.J., Clark A.J., Martin J.S., Ward J.D., Boulton S.J. HCLK2 is essential for the mammalian S-phase checkpoint and impacts on Chk1 stability. Nat. Cell Biol. 2007, 9:391-401.
15. Jiang N., Benard C.Y., Kebir H., Shoubridge E.A., Hekimi S. Human CLK2 links cell cycle progression, apoptosis, and telomere length regulation. J. Biol. Chem. 2003, 278:21678-21684.
16. Shikata M., Ishikawa F., Kanoh J. Tel2 is required for activation of the Mrc1-mediated replication checkpoint. J. Biol. Chem. 2007, 282:5346-5355.
17. Trcek T., Sato H., Singer R.H., Maquat L.E. Temporal and spatial characterization of nonsense-mediated mRNA decay. Genes Dev. 2013.
18. Horejsi Z., Takai H., Adelman C.A., Collis S.J., Flynn H., Maslen S., Skehel J.M., de Lange T., Boulton S.J. CK2 phospho-dependent binding of R2TP complex to TEL2 is essential for mTOR and SMG1 stability. Mol. Cell 2010, 39:839-850.
19. Takai H., Wang R.C., Takai K.K., Yang H., de Lange T. Tel2 regulates the stability of PI3K-related protein kinases. Cell 2007, 131:1248-1259.
20. Izumi N., Yamashita A., Hirano H., Ohno S. Heat shock protein 90 regulates phosphatidylinositol 3-kinase-related protein kinase family proteins together with the RUVBL1/2 and Tel2-containing co-factor complex. Cancer Sci. 2012, 103:50-57.
21. Izumi N., Yamashita A., Iwamatsu A., Kurata R., Nakamura H., Saari B., Hirano H., Anderson P., Ohno S. AAA+ proteins RUVBL1 and RUVBL2 coordinate PIKK activity and function in nonsense-mediated mRNA decay. Sci. Signal. 2010, 3:ra27.
22. Zhang J., Sun X., Qian Y., Maquat L.E. Intron function in the nonsense-mediated decay of beta-globin mRNA: indications that pre-mRNA splicing in the nucleus can influence mRNA translation in the cytoplasm. RNA 1998, 4:801-815.
23. Moriarty P.M., Reddy C.C., Maquat L.E. Selenium deficiency reduces the abundance of mRNA for Se-dependent glutathione peroxidase 1 by a UGA-dependent mechanism likely to be nonsense codon-mediated decay of cytoplasmic mRNA. Mol. Cell Biol. 1998, 18:2932-2939.
24. Belgrader P., Maquat L.E. Nonsense but not missense mutations can decrease the abundance of nuclear mRNA for the mouse major urinary protein, while both types of mutations can facilitate exon skipping. Mol. Cell Biol. 1994, 14:6326-6336.
25. Park E., Gleghorn M.L., Maquat L.E. Staufen2 functions in Staufen1-mediated mRNA decay by binding to itself and its paralog and promoting UPF1 helicase but not ATPase activity. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:405-412.
26. Hwang J., Sato H., Tang Y., Matsuda D., Maquat L.E. UPF1 association with the cap-binding protein, CBP80, promotes nonsense-mediated mRNA decay at two distinct steps. Mol. Cell 2010, 39:396-409.
27. Franks T.M., Singh G., Lykke-Andersen J. Upf1 ATPase-dependent mRNP disassembly is required for completion of nonsense-mediated mRNA decay. Cell 2010, 143:938-950.
28. Tapia J.C., Torres V.A., Rodriguez D.A., Leyton L., Quest A.F. Casein kinase 2 (CK2) increases survivin expression via enhanced beta-catenin-T cell factor/lymphoid enhancer binding factor-dependent transcription. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:15079-15084.
29. Cho H., Kim K.M., Han S., Choe J., Park S.G., Choi S.S., Kim Y.K. Staufen1-mediated mRNA decay functions in adipogenesis. Mol. Cell 2012, 46:495-506.
30. Bruno I.G., Karam R., Huang L., Bhardwaj A., Lou C.H., Shum E.Y., Song H.W., Corbett M.A., Gifford W.D., Gecz J., Pfaff S.L., Wilkinson M.F. Identification of a microRNA that activates gene expression by repressing nonsense-mediated RNA decay. Mol. Cell 2011, 42:500-510.
31. Hosoda N., Kim Y.K., Lejeune F., Maquat L.E. CBP80 promotes interaction of Upf1 with Upf2 during nonsense-mediated mRNA decay in mammalian cells. Nat. Struct. Mol. Biol. 2005, 12:893-901.
32. Hogg J.R., Goff S.P. Upf1 senses 3'UTR length to potentiate mRNA decay. Cell 2010, 143:379-389.
33. Pal M., Ishigaki Y., Nagy E., Maquat L.E. Evidence that phosphorylation of human Upfl protein varies with intracellular location and is mediated by a wortmannin-sensitive and rapamycin-sensitive PI 3-kinase-related kinase signaling pathway. RNA 2001, 7:5-15.
34. Tinguely A., Chemin G., Peron S., Sirac C., Reynaud S., Cogne M., Delpy L. Cross talk between immunoglobulin heavy-chain transcription and RNA surveillance during B cell development. Mol. Cell Biol. 2012, 32:107-117.
35. Rebbapragada I., Lykke-Andersen J. Execution of nonsense-mediated mRNA decay: what defines a substrate?. Curr. Opin. Cell Biol. 2009, 21:394-402.
36. Kurosaki T., Maquat L.E. Rules that govern UPF1 binding to mRNA 3' UTRs. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:3357-3362.
37. Maquat L.E., Hwang J., Sato H., Tang Y. CBP80-promoted mRNP rearrangements during the pioneer round of translation, nonsense-mediated mRNA decay, and thereafter. Cold Spring Harb. Symp. Quant. Biol. 2010, 75:127-134.
38. Nicholson P., Muhlemann O. Cutting the nonsense: the degradation of PTC-containing mRNAs. Biochem. Soc. Trans. 2010, 38:1615-1620.
39. Yamashita A., Izumi N., Kashima I., Ohnishi T., Saari B., Katsuhata Y., Muramatsu R., Morita T., Iwamatsu A., Hachiya T., Kurata R., Hirano H., Anderson P., Ohno S. SMG-8 and SMG-9, two novel subunits of the SMG-1 complex, regulate remodeling of the mRNA surveillance complex during nonsense-mediated mRNA decay. Genes Dev. 2009, 23:1091-1105.