The RNA helicase DHX34 functions as a scaffold for SMG1-mediated UPF1 phosphorylation

Nature Communications

Volumn 7, Issue , 2016, Pages

  Melero, Roberto ^a,d   Hug, Nele ^b   Lopez Perrote, Andres ^a   Yamashita, Akio ^c   Caceres, Javier F ^b   Llorca, Oscar ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c YOKOHAMA CITY UNIVERSITY   (Japan)

^d CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DHX34 PROTEIN; MESSENGER RNA; RNA HELICASE; SCAFFOLD PROTEIN; SMALL INTERFERING RNA; SMG1 KINASE; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; UPF1 PROTEIN; DHX34 PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BINDING; SMG1 PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN; UPF1 PROTEIN, HUMAN;

CHEMICAL REACTION; ELECTRON MICROSCOPY; ENZYME ACTIVITY; GENE EXPRESSION; MOLECULAR ANALYSIS; PROTEIN; RNA;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DELETION MUTANT; IMMUNOPRECIPITATION; IN VITRO STUDY; NONSENSE MEDIATED MRNA DECAY; PROTEIN CONFORMATION; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; ELECTRON MICROSCOPY; HEK293 CELL LINE; HELA CELL LINE; HUMAN; METABOLISM; PHOSPHORYLATION;

HEK293 CELLS; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; IN VITRO TECHNIQUES; MICROSCOPY, ELECTRON; NONSENSE MEDIATED MRNA DECAY; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN BINDING; RNA HELICASES; TRANS-ACTIVATORS;

EID: 84956915190     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10585     Document Type: Article

References (51)

1. Huang, L., Wilkinson, M. F. Regulation of nonsense-mediated mRNA decay. Wiley Interdiscip. Rev. RNA 3, 807-828 (2012).
2. Kervestin, S., Jacobson, A. NMD: a multifaceted response to premature translational termination. Nat. Rev. Mol. Cell Biol. 13, 700-712 (2012).
3. Schweingruber, C., Rufener, S. C., Zund, D., Yamashita, A., Muhlemann, O. Nonsense-mediated mRNA decay-mechanisms of substrate mRNA recognition and degradation in mammalian cells. Biochim. Biophys. Acta 1829, 612-623 (2013).
4. Weischenfeldt, J. et al. Mammalian tissues defective in nonsense-mediated mRNA decay display highly aberrant splicing patterns. Genome Biol. 13, R35 (2012).
5. Li, T. et al. Smg6/Est1 licenses embryonic stem cell differentiation via nonsense-mediated mRNA decay. EMBO J. 34, 1630-1647 (2015).
6. Lou, C. H., Shum, E. Y., Wilkinson, M. F. RNA degradation drives stem cell differentiation. EMBO J. 34, 1606-1608 (2015).
7. Popp, M. W., Maquat, L. E. Organizing principles of mammalian nonsensemediated mRNA decay. Annu. Rev. Genet. 47, 139-165 (2013).
8. Chakrabarti, S. et al. Molecular mechanisms for the RNA-dependent ATPase activity of Upf1 and its regulation by Upf2. Mol. Cell 41, 693-703 (2011).
9. Clerici, M. et al. Unusual bipartite mode of interaction between the nonsensemediated decay factors, UPF1 and UPF2. EMBO J. 28, 2293-2306 (2009).
10. Chamieh, H., Ballut, L., Bonneau, F., Le Hir, H. NMD factors UPF2 and UPF3 bridge UPF1 to the exon junction complex and stimulate its RNA helicase activity. Nat. Struct. Mol. Biol. 15, 85-93 (2008).
11. Fiorini, F., Boudvillain, M., Le Hir, H. Tight intramolecular regulation of the human Upf1 helicase by its N-and C-terminal domains. Nucleic Acids Res. 41, 2404-2415 (2013).
12. Franks, T. M., Singh, G., Lykke-Andersen, J. Upf1 ATPase-dependent mRNP disassembly is required for completion of nonsense-mediated mRNA decay. Cell 143, 938-950 (2010).
13. Lasalde, C. et al. Identification and functional analysis of novel phosphorylation sites in the RNA surveillance protein Upf1. Nucleic Acids Res. 42, 1916-1929 (2014).
14. Yamashita, A. Role of SMG-1-mediated Upf1 phosphorylation in mammalian nonsense-mediated mRNA decay. Genes Cells 18, 161-175 (2013).
15. Kurosaki, T. et al. A post-translational regulatory switch on UPF1 controls targeted mRNA degradation. Genes Dev. 28, 1900-1916 (2014).
16. Yamashita, A., Kashima, I., Ohno, S. The role of SMG-1 in nonsensemediated mRNA decay. Biochim. Biophys. Acta 1754, 305-315 (2005).
17. Yamashita, A., Ohnishi, T., Kashima, I., Taya, Y., Ohno, S. Human SMG-1, a novel phosphatidylinositol 3-kinase-related protein kinase, associates with components of the mRNA surveillance complex and is involved in the regulation of nonsense-mediated mRNA decay. Genes Dev. 15, 2215-2228 (2001).
18. Yang, H. et al. mTOR kinase structure, mechanism and regulation. Nature 497, 217-223 (2013).
19. Sibanda, B. L., Chirgadze, D. Y., Blundell, T. L. Crystal structure of DNA-PKcs reveals a large open-ring cradle comprised of HEAT repeats. Nature 463, 118-121 (2010).
20. Deniaud, A. et al. A network of SMG-8, SMG-9 and SMG-1 C-terminal insertion domain regulates UPF1 substrate recruitment and phosphorylation. Nucleic Acids Res. 43, 7600-7611 (2015).
21. Melero, R. et al. Structures of SMG1-UPFs complexes: SMG1 contributes to regulate UPF2-dependent activation of UPF1 in NMD. Structure 22, 1105-1119 (2014).
22. Arias-Palomo, E. et al. The nonsense-mediated mRNA decay SMG-1 kinase is regulated by large-scale conformational changes controlled by SMG-8. Genes Dev. 25, 153-164 (2011).
23. Yamashita, A. et al. 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. 23, 1091-1105 (2009).
24. Fernandez, I. S. et al. Characterization of SMG-9, an essential component of the nonsense-mediated mRNA decay SMG1C complex. Nucleic Acids Res. 39, 347-358 (2011).
25. Chan, W. K. et al. An alternative branch of the nonsense-mediated decay pathway. EMBO J. 26, 1820-1830 (2007).
26. Gehring, N. H. et al. Exon-junction complex components specify distinct routes of nonsense-mediated mRNA decay with differential cofactor requirements. Mol. Cell 20, 65-75 (2005).
27. Ivanov, P. V., Gehring, N. H., Kunz, J. B., Hentze, M. W., Kulozik, A. E. Interactions between UPF1, eRFs, PABP and the exon junction complex suggest an integrated model for mammalian NMD pathways. EMBO J. 27, 736-747 (2008).
28. Metze, S., Herzog, V. A., Ruepp, M. D., Muhlemann, O. Comparison of EJC-enhanced and EJC-independent NMD in human cells reveals two partially redundant degradation pathways. RNA 19, 1432-1448 (2013).
29. Casadio, A. et al. Identification and characterization of novel factors that act in the nonsense-mediated mRNA decay pathway in nematodes, flies and mammals. EMBO Rep. 16, 71-78 (2015).
30. Cho, H., Kim, K. M., Kim, Y. K. Human proline-rich nuclear receptor coregulatory protein 2 mediates an interaction between mRNA surveillance machinery and decapping complex. Mol. Cell 33, 75-86 (2009).
31. Longman, D., Plasterk, R. H., Johnstone, I. L., Caceres, J. F. Mechanistic insights and identification of two novel factors in the C. elegans NMD pathway. Genes Dev. 21, 1075-1085 (2007).
32. Izumi, N., Yamashita, A., Ohno, S. Integrated regulation of PIKK-mediated stress responses by AAA\+ proteins RUVBL1 and RUVBL2. Nucleus 3, 29-43 (2012).
33. Matias, P. M. et al. The AAA\+ proteins Pontin and Reptin enter adult age: from understanding their basic biology to the identification of selective inhibitors. Front. Mol. Biosci. 2, 17 (2015).
34. Longman, D. et al. DHX34 and NBAS form part of an autoregulatory NMD circuit that regulates endogenous RNA targets in human cells, zebrafish and Caenorhabditis elegans. Nucleic Acids Res. 41, 8319-8331 (2013).
35. Abdelhaleem, M., Maltais, L., Wain, H. The human DDX and DHX gene families of putative RNA helicases. Genomics 81, 618-622 (2003).
36. Ozgur, S. et al. The conformational plasticity of eukaryotic RNA-dependent ATPases. FEBS J. 282, 850-863 (2015).
37. Robert-Paganin, J., Rety, S., Leulliot, N. Regulation of DEAH/RHA helicases by G-patch proteins. BioMed Res. Int. 2015, 931857 (2015).
38. Hug, N., Caceres, J. F. The RNA helicase DHX34 activates NMD by promoting a transition from the surveillance to the decay-inducing complex. Cell Rep. 8, 1845-1856 (2014).
39. Kelley, L. A., Sternberg, M. J. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371 (2009).
40. He, Y., Andersen, G. R., Nielsen, K. H. Structural basis for the function of DEAH helicases. EMBO Rep. 11, 180-186 (2010).
41. Walbott, H. et al. Prp43p contains a processive helicase structural architecture with a specific regulatory domain. EMBO J. 29, 2194-2204 (2010).
42. Kashima, I. et al. Binding of a novel SMG-1-Upf1-eRF1-eRF3 complex (SURF) to the exon junction complex triggers Upf1 phosphorylation and nonsensemediated mRNA decay. Genes Dev. 20, 355-367 (2006).
43. Wang, J., Gudikote, J. P., Olivas, O. R., Wilkinson, M. F. Boundaryindependent polar nonsense-mediated decay. EMBO Rep. 3, 274-279 (2002).
44. Anastasaki, C., Longman, D., Capper, A., Patton, E. E., Caceres, J. F. Dhx34 and Nbas function in the NMD pathway and are required for embryonic development in zebrafish. Nucleic Acids Res. 39, 3686-3694 (2011).
45. Hara, K. et al. Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 110, 177-189 (2002).
46. Yonezawa, K., Tokunaga, C., Oshiro, N., Yoshino, K. Raptor, a binding partner of target of rapamycin. Biochem. Biophys. Res. Commun. 313, 437-441 (2004).
47. Thermann, R. et al. Binary specification of nonsense codons by splicing and cytoplasmic translation. EMBO J. 17, 3484-3494 (1998).
48. Heymann, J. B., Belnap, D. M. Bsoft: image processing and molecular modeling for electron microscopy. J. Struct. Biol. 157, 3-18 (2007).
49. Sorzano, C. O. et al. XMIPP: a new generation of an open-source image processing package for electron microscopy. J. Struct. Biol. 148, 194-204 (2004).
50. Tang, G. et al. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007).
51. Goddard, T. D., Huang, C. C., Ferrin, T. E. Visualizing density maps with UCSF Chimera. J. Struct. Biol. 157, 281-287 (2007).