Resistance of mRNAs with AUG-proximal nonsense mutations to nonsense-mediated decay reflects variables of mRNA structure and translational activity

Nucleic Acids Research

Volumn 43, Issue 13, 2015, Pages 6528-6544

  Pereira, Francisco J C ^a   Teixeira, Alexandre ^a,b   Kong, Jian ^c   Barbosa, Cristina ^a,d   Silva, Ana Luísa ^a   Marques Ramos, Ana ^a   Liebhaber, Stephen A ^c   Romão, Luísa ^a,d  

^a NATIONAL INSTITUTE OF HEALTH DR RICARDO JORGE   (Portugal)

^b NOVA MEDICAL SCHOOL   (Portugal)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF LISBON   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOGLOBIN ALPHA CHAIN; HEMOGLOBIN BETA CHAIN; MESSENGER RNA; START CODON; STOP CODON;

ANIMAL CELL; ARTICLE; AUG PROXIMITY; CONTROLLED STUDY; GENETIC RESISTANCE; HUMAN; MOUSE; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; NONSENSE MUTATION; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; RIBOSOME; RNA SEQUENCE; RNA STRUCTURE; RNA TRANSLATION; STOP CODON; TRANSLATION INITIATION; ANIMAL; CHEMISTRY; GENETICS; PROTEIN SYNTHESIS; START CODON; TUMOR CELL LINE;

ALPHA-GLOBINS; ANIMALS; BETA-GLOBINS; CELL LINE, TUMOR; CODON, INITIATOR; CODON, NONSENSE; HUMANS; MICE; NONSENSE MEDIATED MRNA DECAY; OPEN READING FRAMES; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; PROTEIN BIOSYNTHESIS; RNA, MESSENGER;

EID: 84939611842     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv588     Document Type: Article

References (66)

1. Le Hir,H., Izaurralde,E., Maquat,L.E. and Moore,M.J. (2000) The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J., 19, 6860-6869.
2. Le Hir,H., Gatfield,D., Izaurralde,E. and Moore,M.J. (2001) The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO J., 20, 4987-4997.
3. Alexandrov,A., Colognori,D., Shu,M.D. and Steitz,J.A. (2012) Human spliceosomal protein CWC22 plays a role in coupling splicing to exon junction complex deposition and nonsense-mediated decay. Proc. Natl. Acad. Sci. U.S.A., 109, 21313-21318.
4. 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.
5. 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.
6. Popp,M.W. and Maquat,L.E. (2014) The dharma of nonsense-mediated mRNA decay in mammalian cells. Mol. Cells, 37, 1-8.
7. Kashima,I., Yamashita,A., Izumim,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.
8. Hwang,J., Sato,H., Tang,Y., Matsuda,D. and Maquat,L.E. (2010) UPF1 association with the cap-binding protein, CBP80, promotes nonsense-mediated mRNA decay at two distinct steps. Mol. Cell, 39, 396-409.
9. 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.
10. 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.
11. Cho,H., Kim,K.M. and Kim,Y.K. (2009) Human proline-rich nuclear receptor coregulatory protein 2 mediates an interaction between mRNA surveillance machinery and decapping complex. Mol. Cell, 33, 75-86.
12. 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 Acids Res., 42, 9447-9460.
13. Nicholson,P., Josi,C., Kurosawa,H., Yamashita,A. and Mühlemann,O. (2014) A novel phosphorylation-independent interaction between SMG6 and UPF1 is essential for human NMD. Nucleic Acids Res., 42, 9217-9235.
14. Eberle,A.B., Lykke-Andersen,S., Mühlemann,O. and Jensen,T.H. (2009) SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat. Struct. Mol. Biol., 16, 49-55.
15. 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.
16. Schmidt,S.A., Foley,P.L., Jeong,D.H., Rymarquis,L.A., Doyle,F., Tenenbaum,S.A., Belasco,J.G. and Green,P.J. (2014) Identification of SMG6 cleavage sites and a preferred RNA cleavage motif by global analysis of endogenous NMD targets in human cells. Nucleic Acids Res., 43, 309-323.
17. 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.
18. Lejeune,F., Li,X. and Maquat,L.E. (2003) Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol. Cell, 12, 675-687.
19. Unterholzner,L. and Izaurralde,E. (2004) SMG7 acts as a molecular link between mRNA surveillance and mRNA decay. Mol. Cell, 16, 587-596.
20. Amrani,N., Ganesan,R., Kervestin,S., Mangus,D.A., Ghosh,S. and Jacobson,A. (2004) A faux 3′-UTR promotes aberrant termination and triggers nonsense-mediated mRNA decay. Nature, 432, 112-118.
21. Silva,A.L., Ribeiro,P., Inácio,A., Liebhaber,S.A. and Romão,L. (2008) Proximity of the poly(A)-binding protein to a premature termination codon inhibits mammalian nonsense-mediated mRNA decay. RNA, 14, 563-576.
22. 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.
23. Eberle,A.B., Mathys,H., Stalder,L., Orozco,R.Z. and Mühlemann,O. (2008) Posttranscriptional gene regulation by spatial rearrangement of the 3′ untranslated region. PLoS Biol., 6, e92.
24. 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.
25. Silva,A.L and Romão,L. (2009) The mammalian nonsense-mediated mRNA decay pathway: to decay or not to decay! Which players make the decision? FEBS Lett., 583, 499-505.
26. Uchida,N., Hoshino,S., Imataka,H., Sonenberg,N. and Katada,T. (2002) A novel role of the mammalian GSPT/eRF3 associating with poly(A)-binding protein in Cap/Poly(A)-dependent translation. J. Biol. Chem., 277, 50286-50292.
27. Hogg,J.R. and Goff,S.P. (2010) Upf1 senses 3′ UTR length to potentiate mRNA decay. Cell, 143, 379-389.
28. Zünd,D., Gruber,A.R., Zavolan,M. and Mühlemann,O. (2013) Translation-dependent displacement of UPF1 from coding sequences causes its enrichment in 3? UTRs. Nat. Struct. & Mol. Biol., 20, 936-943.
29. Kurosaki,T., Li,W., Hoque,M., Popp,M.W., Ermolenko,D.N., Tian,B. and Maquat,L.E. (2014) A post-translational regulatory switch on UPF1 controls targeted mRNA degradation. Genes Dev., 28, 1900-1916.
30. Mendell,J.T., Sharifi,N.A., Meyers,J.L., Martinez-Murillo,F and Dietz,HC. (2004) Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat. Genet., 36, 1073-1078.
31. 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. and Wilkinson,M.F. (2011) Identification of a microRNA that activates gene expression by repressing nonsense-mediated RNA decay. Mol. Cell, 42, 500-510.
32. 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.
33. Hurt,J.A., Robertson,A.D. and Burge,C.B. (2013) Global analyses of UPF1 binding and function reveal expanded scope of nonsense-mediated mRNA decay. Genome Res., 23, 1636-1650.
34. Peixeiro,I., Inácio,A., Barbosa,C., Silva,A.L., Liebhaber,S.A. and Romão,L. (2012). Interaction of PABPC1 with the translation initiation complex is critical to the NMD resistance of AUG-proximal nonsense mutations. Nucleic Acids Res., 40, 1160-1173.
35. Roque,S., Cerciat,M., Gaugué,I., Mora,L., Floch,A.G., Zamaroczy,M., Heurgué-Hamard,V. and Kervestin,S. (2015) Interaction between the poly(A)-binding protein Pab1 and the eukaryotic release factor eRF3 regulates translation termination but not mRNA decay in Saccharomyces cerevisiae. RNA, 21, 124-134.
36. Fatscher,T., Boehm,V., Weiche,B. and Gehring,N.H. (2014) The interaction of cytoplasmic poly(A)-binding protein with eukaryotic initiation factor 4G suppresses nonsense-mediated mRNA decay. RNA, 20, 1579-1592.
37. Joncourt,R., Eberle,A.B., Rufener,S.C. and Mühlemann,O. (2014) Eukaryotic initiation factor 4G suppresses nonsense-mediated mRNA decay by two genetically separable mechanisms. PLoS One, 9, e104391.
38. Brogna,S. and Wen,J. (2009) Nonsense-mediated mRNA decay (NMD) mechanisms. Nat. Struct. & Mol. Biol., 16, 107-113.
39. Ghosh,S., Ganesan,R., Amrani,N. and Jacobson,A. (2010) Translational competence of ribosomes released from a premature termination codon is modulated by NMD factors. RNA, 16, 1832-1847.
40. Romão,L., Inácio,A., Santos,S., Ávila,M., Faustino,P., Pacheco,P. and Lavinha,J. (2000) Nonsense mutations in the human beta-globin gene lead to unexpected levels of cytoplasmic mRNA accumulation. Blood, 96, 2895-2901.
41. Inácio,A., Silva,A.L., Pinto,J., Ji,X., Morgado,A., Almeida,F., Faustino,P., Lavinha,J., Liebhaber,S.A. and Romão,L. (2004) Nonsense mutations in close proximity to the initiation codon fail to trigger full nonsense-mediated mRNA decay. J. Biol. Chem., 279, 32170-32180.
42. Kong,J., Ji,X. and Liebhaber,S.A. (2003) The KH-domain protein alpha-CP has a direct role in mRNA stabilization independent of its cognate binding site. Mol. Cell. Biol., 23, 1125-1134.
43. Kozak,M. (2001) Constraints on re-initiation of translation in mammals. Nucleic Acids Res., 29, 5226-5232.
44. Pereira,F.J.C., Silva,M.C., Picanço,I., Seixas,M.T., Ferrão,A., Faustino,P. and Romão,L. (2006) Human alpha2-globin nonsense-mediated mRNA decay induced by a novel alpha-thalassaemia frameshift mutation at codon 22. Br. J. Haematol., 133, 98-102.
45. Pfaffl,M.W. (2001) A new mathematical model for relative quantification in realtime RT-PCR. Nucleic Acids Res., 29, e45.
46. Silva,A.L., Pereira,F.J., Morgado,A., Kong,J., Martins,R., Faustino,P., Liebhaber,S.A. and Romão,L. (2006) The canonical UPF1-dependent nonsense-mediated mRNA decay is inhibited in transcripts carrying a short open reading frame independent of sequence context. RNA, 12, 2160-2170.
47. 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.
48. Zhang,J., Sun,X., Qian,Y. and Maquat,L.E. (1998) Intron function in the nonsense-mediated decay of β-globin mRNA: Indications that pre-mRNA splicing in the nucleus can influence mRNA translation in the cytoplasm. RNA, 4, 801-815.
49. Zhang,J. and Maquat,L.E. (1997) Evidence that translation re-initiation abrogates nonsense-mediated mRNA decay in mammalian cells. EMBO J., 16, 826-833.
50. Pöyry,T.A.A., Kaminski,A. and Jackson,R.J. (2004) What determines whether mammalian ribosomes resume scanning after translation of a short upstream open reading frame? Genes Dev., 18, 62-75.
51. Neu-Yilik,G., Amthor,B., Gehring,N.H., Bahri,S., Paidassi,H., Hentze,M.W. and Kulozik,A.E. (2011) Mechanism of escape from nonsense-mediated mRNA decay of human beta-globin transcripts with nonsense mutations in the first exon. RNA, 17, 843-854.
52. Shakin,H. and Liebhaber,S.A. (1986) Translational profiles of alpha 1-, alpha 2-, and beta-globin messenger ribonucleic acids in human reticulocytes. J. Clin. Invest., 78, 1125-1129.
53. Wen,J.D., Lancaster,L., Hodges,C., Zeri,A.C., Yoshimura,S.H., Noller,H.F., Bustamante,C. and Tinoco,I. (2008) Following translation by single ribosomes one codon at a time. Nature, 452, 598-603.
54. Somogyi,P., Jenner,A.J., Brierley,I. and Inglis,S.C. (1993) Ribosomal pausing during translation of an RNA pseudoknot. Mol. Cell. Biol., 13, 6931-6940.
55. Pestova,T.V. and Kolupaeva,V.G. (2002) The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev., 16, 2906-2922.
56. Meaux,S., vanHoof,A. and Baker,K.E. (2008) Nonsense-mediated mRNA decay in yeast does not require PAB1 or a poly(A) tail. Mol. Cell, 29, 134-140.
57. Wen,J. and Brogna,S. (2010) Splicing-dependent NMD does not require the EJC in Schizosaccharomyces pombe. EMBO J., 29, 1537-1551.
58. Chaisue,C., Kitcharoen,S., Wilairat,P., Jetsrisuparb,A., Fucharoen,G. and Fucharoen,S. (2007) Alpha/beta-globin mRNA ratio determination by multiplex quantitative real-time reverse transcription-polymerase chain reaction as an indicator of globin gene function. Clin. Biochem., 40, 1373-1377.
59. Fischel-Ghodsian,N., Nicholls,R.D. and Higgs,D.R. (1987) Long range genome structure around the human alpha-globin complex analysed by PFGE. Nucleic Acids Res., 15, 6197-6207.
60. Cooper,G.M., Brudno,M., Stone,E.A., Dubchak,I., Batzoglou,S. and Sidow,A. (2004) Characterization of evolutionary rates and constraints in three mammalian genomes. Genome Res., 14, 539-548.
61. Jiang,C. and Zhao,Z. (2006) Mutational spectrum in the recent human genome inferred by single nucleotide polymorphisms. Genomics 88, 527-534.
62. Tuan,D. and Forget,B.G. (1980) Physicochemical measurement of the base composition of mRNA-related sequences of the human alpha and beta globin genes. Mol. Biol. Rep., 6, 179-183.
63. Jackson,R.J. (2005) Alternative mechanisms of initiating translation of mammalian mRNAs. Biochem. Soc. Trans., 33, 1231-1241.
64. Szamecz,B., Rutkai,E., Cuchalová,L., Munzarová,V., Herrmannová,A., Nielsen,N.H., Burela,L., Hinnebusch,A.G. and Valášek,L. (2008) eIF3a cooperates with sequences 5′ of uORF1 to promote resumption of scanning by post-termination ribosomes for re-initiation on GCN4 mRNA. Genes Dev., 22, 2414-2425.
65. Kahvejian,A., Roy,G. and Sonenberg,N. (2001) The mRNA closed-loop model: the function of PABP and PABP-interacting proteins in mRNA translation. Cold Spring Harbor Symp. Quant. Biol., 66, 293-300.
66. Wagner,S., Herrmannová,A., Malík,R., Peclinovská,L. and Valášek,L.S. (2014) Functional and biochemical characterization of human eukaryotic translation initiation factor 3 in living cells. Mol. Cell. Biol., 34, 3041-3052.