A novel phosphorylation-independent interaction between SMG6 and UPF1 is essential for human NMD

Nucleic Acids Research

Volumn 42, Issue 14, 2014, Pages 9217-9235

  Nicholson, Pamela ^a   Josi, Christoph ^a   Kurosawa, Hitomi ^b   Yamashita, Akio ^b   Mühlemann, Oliver ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ENDONUCLEASE; MESSENGER RNA; PROTEIN SMG6; PROTEIN UPF1; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NONSENSE MEDIATED MRNA DECAY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA DEGRADATION;

BINDING SITES; HELA CELLS; HUMANS; MUTATION; NONSENSE MEDIATED MRNA DECAY; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TELOMERASE; TRANS-ACTIVATORS;

EID: 84906239869     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku645     Document Type: Article

References (68)

1. Mendell, J.T., Sharifi, N.A., Meyers, J.L., Martinez-Murillo, F. and Dietz, H.C. (2004) Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat. Genet., 36, 1073-1078.
2. He, F., Li, X., Spatrick, P., Casillo, R., Dong, S. and Jacobson, A. (2003) Genome-wide analysis of mRNAs regulated by the nonsense-mediated and 5′ to 3′ mRNA decay pathways in yeast. Mol. Cell, 12, 1439-1452.
3. Rehwinkel, J., Letunic, I., Raes, J., Bork, P. and Izaurralde, E. (2005) Nonsense-mediated mRNA decay factors act in concert to regulate common mRNA targets. RNA, 11, 1530-1544.
4. Frischmeyer, P.A. and Dietz, H.C. (1999) Nonsense-mediated mRNA decay in health and disease. Hum. Mol. Genet., 8, 1893-1900.
5. Keeling, K.M. and Bedwell, D.M. (2011) Suppression of nonsense mutations as a therapeutic approach to treat genetic diseases. Wiley Interdiscip. Rev. RNA, 2, 837-852.
6. Bhattacharya, A., Czaplinski, K., Trifillis, P., He, F., Jacobson, A. and Peltz, S.W. (2000) Characterization of the biochemical properties of the human Upf1 gene product that is involved in nonsense-mediated mRNA decay. RNA, 6, 1226-1235.
7. Czaplinski, K., Ruiz-Echevarria, M.J., Paushkin, S.V., Han, X., Weng, Y., Perlick, H.A., Dietz, H.C., Ter Avanesyan, M.D. and Peltz, S.W. (1998) The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev., 12, 1665-1677.
8. Eberle, A.B., Stalder, L., Mathys, H., Orozco, R.Z. and Muhlemann, O. (2008) Posttranscriptional gene regulation by spatial rearrangement of the 3′ untranslated region. PLoS Biol., 6, e92.
9. Ivanov, P.V., Gehring, N.H., Kunz, J.B., Hentze, M.W. and Kulozik, A.E. (2008) Interactions between UPF1, eRFs, PABP and the exon junction complex suggest an integrated model for mammalian NMD pathways. EMBO J., 27, 736-747.
10. Silva, A.L., Ribeiro, P., Inacio, A., Liebhaber, S.A. and Romao, L. (2008) Proximity of the poly(A)-binding protein to a premature termination codon inhibits mammalian nonsense-mediated mRNA decay. RNA, 14, 563-576.
11. Singh, G., Rebbapragada, I. and Lykke-Andersen, J. (2008) A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol., 6, e111.
12. Yamashita, A. (2013) Role of SMG-1-mediated Upf1 phosphorylation in mammalian nonsense-mediated mRNA decay. Genes Cells, 18, 161-175.
13. Kashima, I., Yamashita, A., Izumi, N., Kataoka, N., Morishita, R., Hoshino, S., Ohno, M., Dreyfuss, G. and Ohno, S. (2006) 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., 20, 355-367.
14. Yamashita, A., Izumi, N., Kashima, I., Ohnishi, T., Saari, B., Katsuhata, Y., Muramatsu, R., Morita, T., Iwamatsu, A., Hachiya, T. et al. (2009) 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.
15. Izumi, N., Yamashita, A., Iwamatsu, A., Kurata, R., Nakamura, H., Saari, B., Hirano, H., Anderson, P. and Ohno, S. (2010) AAA+ proteins RUVBL1 and RUVBL2 coordinate PIKK activity and function in nonsense-mediated mRNA decay. Sci. Signal., 3, 1-13.
16. Loh, B., Jonas, S. and Izaurralde, E. (2013) The SMG5-SMG7 heterodimer directly recruits the CCR4-NOT deadenylase complex to mRNAs containing nonsense codons via interaction with POP2. Genes Dev., 27, 2125-2138.
17. Cho, H., Han, S., Choe, J., Park, S.G., Choi, S.S. and Kim, Y.K. (2013) SMG5-PNRC2 is functionally dominant compared with SMG5-SMG7 in mammalian nonsense-mediated mRNA decay. Nucleic Acids Res., 41, 1319-1328.
18. Okada-Katsuhata, Y., Yamashita, A., Kutsuzawa, K., Izumi, N., Hirahara, F. and Ohno, S. (2012) N- and C-terminal Upf1 phosphorylations create binding platforms for SMG-6 and SMG-5:SMG-7 during NMD. Nucleic Acids Res., 40, 1251-1266.
19. Fukuhara, N., Ebert, J., Unterholzner, L., Lindner, D., Izaurralde, E. and Conti, E. (2005) SMG7 Is a 14-3-3-like adaptor in the nonsense-mediated mRNA decay pathway. Mol. Cell, 17, 537-547.
20. Kashima, I., Jonas, S., Jayachandran, U., Buchwald, G., Conti, E., Lupas, A.N. and Izaurralde, E. (2010) SMG6 interacts with the exon junction complex via two conserved EJC-binding motifs (EBMs) required for nonsense-mediated mRNA decay. Genes Dev., 24, 2440-2450.
21. Glavan, F., Behm-Ansmant, I., Izaurralde, E. and Conti, E. (2006) Structures of the PIN domains of SMG6 and SMG5 reveal a nuclease within the mRNA surveillance complex. EMBO J., 25, 5117-5125.
22. Takeshita, D., Zenno, S., Lee, W.C., Saigo, K. and Tanokura, M. (2006) Crystallization and preliminary X-ray analysis of the PIN domain of human EST1A. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun., 62, 656-658.
23. Takeshita, D., Zenno, S., Lee, W.C., Saigo, K. and Tanokura, M. (2007) Crystal structure of the PIN domain of human telomerase-associated protein EST1A. Proteins, 68, 980-989.
24. Eberle, A.B., Lykke-Andersen, S., Muhlemann, O. and Jensen, T.H. (2009) SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat. Struct. Mol. Biol., 16, 49-55.
25. Huntzinger, E., Kashima, I., Fauser, M., Sauliere, J. and Izaurralde, E. (2008) SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA, 14, 2609-2617.
26. Nicholson, P. and Mühlemann, O. (2010) Cutting the nonsense: the degradation of PTC-containing mRNAs. Biochem. Soc. Trans., 38, 1615-1620.
27. Metze, S., Herzog, V.A., Ruepp, M.-D. and Mühlemann, O. (2013) Comparison of EJC-enhanced and EJC-independent NMD in human cells reveals two partially redundant degradation pathways. RNA, 19, 1432-1448.
28. Yepiskoposyan, H., Aeschimann, F., Nilsson, D., Okoniewski, M. and Mühlemann, O. (2011) Autoregulation of the nonsense-mediated mRNA decay pathway in human cells. RNA, 17, 2108-2118.
29. Nicholson, P., Joncourt, R. and Mühlemann, O. (2012) Analysis of nonsense-mediated mRNA decay in mammalian cells. Curr. Protoc. Cell Biol., Unit 27.4, 1-61.
30. Chakrabarti, S., Jayachandran, U., Bonneau, F., Fiorini, F., Basquin, C., Domcke, S., Le Hir, H. and Conti, E. (2011) Molecular mechanisms for the RNA-dependent ATPase activity of Upf1 and its regulation by Upf2. Mol. Cell, 41, 693-703.
31. Vidal, M., Brachmann, R.K., Fattaey, A., Harlow, E. and Boeke, J.D. (1996) Reverse two-hybrid and one-hybrid systems to detect dissociation of protein-protein and DNA-protein interactions. Proc. Natl Acad. Sci. U.S.A., 93, 10315-10320.
32. Gietz, D., St Jean, A., Woods, R.A. and Schiestl, R.H. (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res., 20, 1425.
33. Duttweiler, H.M. (1996) A highly sensitive and non-lethal beta-galactosidase plate assay for yeast. Trends Genet., 12, 340-341.
34. Arias-Palomo, E., Yamashita, A., Fernández, I.S., Núñez-Ramírez, R., Bamba, Y., Izumi, N., Ohno, S. and Llorca, O. (2011) The nonsense-mediated mRNA decay SMG-1 kinase is regulated by large-scale conformational changes controlled by SMG-8. Genes Dev., 25, 153-164.
35. Zillner, K., Jerabek-Willemsen, M., Duhr, S., Braun, D., Längst, G. and Baaske, P. Part V protein analysis II: functionalcharacterization. (2012) In: Kaufmann, M and Klinger, C. Microscale Thermophoresis as a Sensitive Methodto Quantify Protein: Nucleic Acid Interactions in Solution. Springer, New York, NY, 815, 241-252.
36. Seidel, S.A.I., Dijkman, P.M., Lea, W.A., van den Bogaart, G., Jerabek-Willemsen, M., Lazic, A., Joseph, J.S., Srinivasan, P., Baaske, P., Simeonov, A. et al. (2013) Microscale thermophoresis quantifies biomolecular interactions under previously challenging conditions. Methods, 59, 301-315.
37. Jerabek-Willemsen, M., Wienken, C.J., Braun, D., Baaske, P. and Duhr, S. (2011) Molecular interaction studies using microscale thermophoresis. Assay Drug Dev. Technol., 9, 342-353.
38. Wienken, C.J., Baaske, P., Duhr, S. and Braun, D. (2011) Thermophoretic melting curves quantify the conformation and stability of RNA and DNA. Nucleic Acids Res., 39, e52.
39. Page, M.F., Carr, B., Anders, K.R., Grimson, A. and Anderson, P. (1999) SMG-2 is a phosphorylated protein required for mRNA surveillance in Caenorhabditis elegans and related to Upf1p of yeast. Mol. Cell. Biol., 19, 5943-5951.
40. Ohnishi, T., Yamashita, A., Kashima, I., Schell, T., Anders, K.R., Grimson, A., Hachiya, T., Hentze, M.W., Anderson, P. and Ohno, S. (2003) Phosphorylation of hUPF1 induces formation of mRNA surveillance complexes containing hSMG-5 and hSMG-7. Mol. Cell, 12, 1187-1200.
41. Yamashita, A., Ohnishi, T., Kashima, I., Taya, Y. and Ohno, S. (2001) 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.
42. Morita, T., Yamashita, A., Kashima, I., Ogata, K., Ishiura, S. and Ohno, S. (2007) Distant N- and C-terminal domains are required for intrinsic kinase activity of SMG-1, a critical component of nonsense-mediated mRNA decay. J. Biol. Chem., 282, 7799-7808.
43. Fields, S. and Song, O. (1989) A novel genetic system to detect protein-protein interactions. Nature, 340, 245-246.
44. Stansfield, I., Jones, K.M., Kushnirov, V.V., Dagkesamanskaya, A.R., Poznyakovski, A.I., Paushkin, S.V., Nierras, C.R., Cox, B.S., Ter-Avanesyan, M.D. and Tuite, M.F. (1995) The products of the SUP45 (eRF1) and SUP35 genes interact to mediate translation termination in Saccharomyces cerevisiae. EMBO J., 14, 4365-4373.
45. Zhouravleva, G., Frolova, L., Le Goff, X., Le Guellec, R., Inge-Vechtomov, S., Kisselev, L. and Philippe, M. (1995) Termination of translation in eukaryotes is governed by two interacting polypeptide chain release factors, eRF1 and eRF3. EMBO J., 14, 4065-4072.
46. Cheng, Z., Muhlrad, D., Lim, M.K., Parker, R. and Song, H. (2007) Structural and functional insights into the human Upf1 helicase core. EMBO J., 26, 253-264.
47. Applequist, S.E., Selg, M., Raman, C. and Jack, H.M. (1997) Cloning and characterization of HUPF1, a human homolog of the Saccharomyces cerevisiae nonsense mRNA-reducing UPF1 protein. Nucleic Acids Res., 25, 814-821.
48. Chakrabarti, S., Bonneau, F., Schüssler, S., Eppinger, E. and Conti, E. (2014) Phospho-dependent and phospho-independent interactions of the helicase UPF1 with the NMD factors SMG5-SMG7 and SMG6. Nucleic Acid Res., doi:10.1093/nar/gku562.
49. Hornbeck, P.V., Kornhauser, J.M., Tkachev, S., Zhang, B., Skrzypek, E., Murray, B., Latham, V. and Sullivan, M. (2011) PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res., 40, D261-D270.
50. Lasalde, C., Rivera, A.V., León, A.J., González-Feliciano, J.A., Estrella, L.A., Rodríguez-Cruz, E.N., Correa, M.E., Cajigas, I.J., Bracho, D.P., Vega, I.E. et al. (2013) Identification and functional analysis of novel phosphorylation sites in the RNA surveillance protein Upf1. Nucleic Acids Res., 42, 1916-1929.
51. Clerici, M., Mourao, A., Gutsche, I., Gehring, N.H., Hentze, M.W., Kulozik, A., Kadlec, J., Sattler, M. and Cusack, S. (2009) Unusual bipartite mode of interaction between the nonsense-mediated decay factors, UPF1 and UPF2. EMBO J., 28, 2293-2306.
52. Chamieh, H., Ballut, L., Bonneau, F. and Le Hir, H. (2008) 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.
53. Fiorini, F., Boudvillain, M. and Le Hir, H. (2013) Tight intramolecular regulation of the human Upf1 helicase by its N- and C-terminal domains. Nucleic Acids Res., 41, 2404-2415.
54. Redon, S., Reichenbach, P. and Lingner, J. (2007) Protein RNA and protein protein interactions mediate association of human EST1A/SMG6 with telomerase. Nucleic Acids Res., 35, 7011-7022.
55. Buhler, M., Paillusson, A. and Muhlemann, O. (2004) Efficient downregulation of immunoglobulin mu mRNA with premature translation-termination codons requires the 5′-half of the VDJ exon. Nucleic Acids Res., 32, 3304-3315.
56. Thermann, R., Neu-Yilik, G., Deters, A., Frede, U., Wehr, K., Hagemeier, C., Hentze, M.W. and Kulozik, A.E. (1998) Binary specification of nonsense codons by splicing and cytoplasmic translation. EMBO J., 17, 3484-3494.
57. Unterholzner, L. and Izaurralde, E. (2004) SMG7 acts as a molecular link between mRNA surveillance and mRNA decay. Mol. Cell, 16, 587-596.
58. Schoenberg, D.R. (2011) Mechanisms of endonuclease-mediated mRNA decay. Wiley Interdiscip. Rev. RNA, 2, 582-600.
59. Gatfield, D., Unterholzner, L., Ciccarelli, F.D., Bork, P. and Izaurralde, E. (2003) Nonsense-mediated mRNA decay in Drosophila: at the intersection of the yeast and mammalian pathways. EMBO J., 22, 3960-3970.
60. Singh, G., Kucukural, A., Cenik, C., Leszyk, J.D., Shaffer, S.A., Weng, Z. and Moore, M.J. (2012) The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus. Cell, 151, 750-764.
61. Sauliere, J., Murigneux, V., Wang, Z., Marquenet, E., Barbosa, I., Le Tonqueze, O., Audic, Y., Paillard, L., Roest Crollius, H. and Le Hir, H. (2012) CLIP-seq of eIF4AIII reveals transcriptome-wide mapping of the human exon junction complex. Nat. Struct. Mol. Biol., 19, 1124-1131.
62. Chiu, S.Y., Serin, G., Ohara, O. and Maquat, L.E. (2003) Characterization of human Smg5/7a: a protein with similarities to Caenorhabditis elegans SMG5 and SMG7 that functions in the dephosphorylation of Upf1. RNA, 9, 77-87.
63. Wang, W., Cajigas, I.J., Peltz, S.W., Wilkinson, M.F. and Gonzalez, C.I. (2006) Role for Upf2p phosphorylation in Saccharomyces cerevisiae nonsense-mediated mRNA decay. Mol. Cell. Biol., 26, 3390-3400.
64. Kalmar, L., Acs, V., Silhavy, D. and Tompa, P. (2012) Long-range interactions in nonsense-mediated mRNA decay are mediated by intrinsically disordered protein regions. J. Mol. Biol., 424, 125-131.
65. Kadlec, J., Guilligay, D., Ravelli, R.B. and Cusack, S. (2006) Crystal structure of the UPF2-interacting domain of nonsense-mediated mRNA decay factor UPF1. RNA, 12, 1817-1824.
66. Fernández, I.S., Yamashita, A., Arias-Palomo, E., Bamba, Y., Bartolomé, R.A., Canales, M.A., Teixidó, J., Ohno, S. and Llorca, O. (2011) Characterization of SMG-9, an essential component of the nonsense-mediated mRNA decay SMG1C complex. Nucleic Acids Res., 39, 347-358.
67. Azzalin, C.M. and Lingner, J. (2006) The double life of UPF1 in RNA and DNA stability pathways. Cell Cycle, 5, 1496-1498.
68. Chawla, R. and Azzalin, C.M. (2008) The telomeric transcriptome and SMG proteins at the crossroads. Cytogenet. Genome Res., 122, 194-201.