The dharma of nonsense-mediated mRNA decay in mammalian cells

Molecules and Cells

Volumn 37, Issue 1, 2014, Pages 1-8

  Popp, Maximilian Wei Lin ^a,b   Maquat, Lynne E ^a,b  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

mRNA quality control; Nonsense mediated mRNA decay; Premature termination codon; RNA metabolism; RNP remodeling

Indexed keywords

CYTOPLASM PROTEIN; MESSENGER RIBONUCLEOPROTEIN; MESSENGER RNA; MESSENGER RNA PRECURSOR; NUCLEAR PROTEIN; RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG; STOP CODON;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ANIMAL CELL; BIOGENESIS; CODON USAGE; CYTOPLASM; EXON SKIPPING; GENE REPRESSION; MAMMAL CELL; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; NUCLEAR EXPORT SIGNAL; NUCLEAR PORE COMPLEX; REGULATORY RNA SEQUENCE; RNA ANALYSIS; RNA CAPPING; RNA SPLICING; RNA TRANSLATION; SHORT SURVEY; TRANSLATION INITIATION; ANIMAL; BIOSYNTHESIS; GENETICS; HUMAN; METABOLISM; PROTEIN TRANSPORT; STOP CODON;

ANIMALS; CODON, TERMINATOR; HUMANS; NONSENSE MEDIATED MRNA DECAY; PROTEIN TRANSPORT; RIBONUCLEOPROTEINS; RNA, MESSENGER;

EID: 84901437738     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.14348/molcells.2014.2193     Document Type: Short Survey

References (88)

1. 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. USA 109, 21313-21318.
2. 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. (Pubitemid 39490837)
3. Amrani, N., Ghosh, S., Mangus, D.A., and Jacobson, A. (2008). Translation factors promote the formation of two states of the closed-loop mRNP. Nature 453, 1276-1280. (Pubitemid 351913593)
4. Anczukow, O., Ware, M.D., Buisson, M., Zetoune, A.B., Stoppa-Lyonnet, D., Sinilnikova, O.M., and Mazoyer, S. (2008). Does the nonsense-mediated mRNA decay mechanism prevent the synthesis of truncated BRCA1, CHK2, and p53 proteins? Hum. Mutat. 29, 65-73.
5. Anders, K.R., Grimson, A., and Anderson, P. (2003). SMG-5, required for C. elegans nonsense-mediated mRNA decay, associates with SMG-2 and protein phosphatase 2A. EMBO J. 22, 641-650. (Pubitemid 36193608)
6. Ballut, L., Marchadier, B., Baguet, A., Tomasetto, C., Séraphin, B., and Le Hir, H. (2005). The exon junction core complex is locked onto RNA by inhibition of eIF4AIII ATPase activity. Nat. Struct. Mol. Biol. 12, 861-869. (Pubitemid 41486709)
7. Bazzini, A.A., Lee, M.T., and Giraldez, A.J. (2012). Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish. Science 336, 233-237.
8. Bhuvanagiri, M., Schlitter, A.M., Hentze, M.W., and Kulozik, A.E. (2010). NMD: RNA biology meets human genetic medicine. Biochem J. 430, 365-377.
9. Braunschweig, U., Gueroussov, S., Plocik, A.M., Graveley, B.R., and Blencowe, B.J. (2013). Dynamic integration of splicing within gene regulatory pathways. Cell 152, 1252-1269.
10. Burns, L.T., and Wente, S.R. (2012). Trafficking to uncharted territory of the nuclear envelope. Curr. Opin. Cell Biol. 24, 341-349.
11. 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.
12. 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. (Pubitemid 36206304)
13. 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.
14. Choe, J., Oh, N., Park, S., Lee, Y.K., Song, O.K., Locker, N., Chi, S.G., and Kim, Y.K. (2012). Translation initiation on mRNAs bound by nuclear cap-binding protein complex CBP80/20 requires interaction between CBP80/20-dependent translation initiation factor and eukaryotic translation initiation factor 3g. J. Biol. Chem. 287, 18500-18509.
15. Cole, C.N., and Scarcelli, J.J. (2006). Transport of messenger RNA from the nucleus to the cytoplasm. Curr. Opin. Cell Biol. 18, 299-306.
16. 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. (Pubitemid 28299517)
17. Dias, S.M., Wilson, K.F., Rojas, K.S., Ambrosio, A.L., and Cerione, R.A. (2009). The molecular basis for the regulation of the cap-binding complex by the importins. Nat. Struct. Mol. Biol. 16, 930-937.
18. Dias, S.M., Cerione, R.A., and Wilson, K.F. (2010). Unloading RNAs in the cytoplasm: an "importin" task. Nucleus 1, 139-143.
19. Djuranovic, S., Nahvi, A., and Green, R. (2012). miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 336, 237-240.
20. Dostie, J., and Dreyfuss, G. (2002). Translation is required to remove Y14 from mRNAs in the cytoplasm. Curr. Biol. 12, 1060-1067. (Pubitemid 34766927)
21. Durand, S., and Lykke-Andersen, J. (2013). Nonsense-mediated mRNA decay occurs during eIF4F-dependent translation in human cells. Nat. Struct. Mol. Biol. 20, 702-709.
22. Eberle, A.B., Stalder, L., Mathys, H., Orozco, R.Z., and Mühlemann, O. (2008). Posttranscriptional gene regulation by spatial rearrangement of the 3′ untranslated region. PLoS Biol. 6, e92.
23. 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.
24. Franks, T.M., Singh, G., and Lykke-Andersen, J. (2010). Upf1 ATPase-dependent mRNP disassembly is required for completion of nonsense-mediated mRNA decay. Cell 143, 938-950.
25. Frischmeyer, P.A., and Dietz, H.C. (1999). Nonsense-mediated mRNA decay in health and disease. Hum. Mol. Genet. 8, 1893-1900. (Pubitemid 29458667)
26. 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. (Pubitemid 40269118)
27. Gardner, L.B. (2010). Nonsense-mediated RNA decay regulation by cellular stress: implications for tumorigenesis. Mol. Cancer Res. 8, 295-308.
28. Gehring, N.H., Lamprinaki, S., Hentze, M.W., and Kulozik, A.E. (2009a). The hierarchy of exon-junction complex assembly by the spliceosome explains key features of mammalian nonsense-mediated mRNA decay. PLoS Biol. 7, e1000120.
29. Gehring, N.H., Lamprinaki, S., Kulozik, A.E., and Hentze, M.W. (2009b). Disassembly of exon junction complexes by PYM. Cell 137, 536-548.
30. Hentze, M.W., and Izaurralde, E. (2013). Making sense of nonsense. Nat. Struct. Mol. Biol. 20, 651-653.
31. Hogg, J.R., and Goff, S.P. (2010). Upf1 senses 3′UTR length to potentiate mRNA decay. Cell 143, 379-389.
32. Holbrook, J.A., Neu-Yilik, G., Hentze, M.W., and Kulozik, A.E. (2006). NMD and Human Disease. In nonsense-mediated mRNA decay, L.E. Maquat, ed. (TX, USA: Landes Bioscience), pp. 111-119.
33. Hoskins, A.A., and Moore, M.J. (2012). The spliceosome: a flexible, reversible macromolecular machine. Trends Biochem. Sci. 37, 179-188.
34. Hosoda, N., Kim, Y.K., Lejeune, F., and Maquat, L.E. (2005). CBP80 promotes interaction of Upf1 with Upf2 during nonsense-mediated mRNA decay in mammalian cells. Nat. Struct. Mol. Biol. 12, 893-901. (Pubitemid 41486713)
35. Hosoda, N., Lejeune, F., and Maquat, L.E. (2006). Evidence that poly(A) binding protein C1 binds nuclear pre-mRNA poly(A) tails. Mol. Cell. Biol. 26, 3085-3097.
36. Huang, L., Lou, C.H., Chan, W., Shum, E.Y., Shao, A., Stone, E., Karam, R., Song, H.W., and Wilkinson, M.F. (2011). RNA homeostasis governed by cell type-specific and branched feedback loops acting on NMD. Mol. Cell 43, 950-961.
37. 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.
38. Hwang, J., and Kim, Y.K. (2013). When a ribosome encounters a premature termination codon. BMB Rep. 46, 9-16.
39. 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.
40. Ishigaki, Y., Li, X., Serin, G., and Maquat, L.E. (2001). Evidence for a pioneer round of mRNA translation: mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20. Cell 106, 607-617. (Pubitemid 32879322)
41. Isken, O., and Maquat, L.E. (2007). Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev. 21, 1833-1856. (Pubitemid 47204924)
42. Isken, O., Kim, Y.K., Hosoda, N., Mayeur, G.L., Hershey, J.W., and Maquat, L.E. (2008). Upf1 phosphorylation triggers translational repression during nonsense-mediated mRNA decay. Cell 133, 314-327. (Pubitemid 351508299)
43. 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. (Pubitemid 351506680)
44. 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. (Pubitemid 43200289)
45. Kervestin, S., and Jacobson, A. (2012). NMD: a multifaceted response to premature translational termination. Nat. Rev. Mol. Cell. Biol. 13, 700-712.
46. Kervestin, S., Li, C., Buckingham, R., and Jacobson, A. (2012). Testing the faux-UTR model for NMD: analysis of Upf1p and Pab1p competition for binding to eRF3/Sup35p. Biochimie 94, 1560-1571.
47. Kornblihtt, A.R., Schor, I.E., Allo, M., Dujardin, G., Petrillo, E., and Munoz, M.J. (2013). Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nat. Rev. Mol. Cell Biol. 14, 153-165.
48. Kugler, W., Enssle, J., Hentze, M.W., and Kulozik, A.E. (1995). Nuclear degradation of nonsense mutated beta-globin mRNA: a post-transcriptional mechanism to protect heterozygotes from severe clinical manifestations of beta-thalassemia? Nucleic Acids Res. 23, 413-418.
49. Kuhn, U., Gundel, M., Knoth, A., Kerwitz, Y., Rudel, S., and Wahle, E. (2009). Poly(A) tail length is controlled by the nuclear poly(A)-binding protein regulating the interaction between poly(A) polymerase and the cleavage and polyadenylation specificity factor. J. Biol. Chem. 284, 22803-22814.
50. Kuroha, K., Tatematsu, T., and Inada, T. (2009). Upf1 stimulates degradation of the product derived from aberrant messenger RNA containing a specific nonsense mutation by the proteasome. EMBO Rep. 10, 1265-1271.
51. Kurosaki, T., and Maquat, L.E. (2013). Rules that govern UPF1 binding to mRNA 3′ UTRs. Proc. Natl. Acad. Sci. USA 110, 3357-3362.
52. Le Hir, H., Izaurralde, E., Maquat, L.E., and Moore, M.J. (2000a). The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 19, 6860-6869. (Pubitemid 32011679)
53. Le Hir, H., Moore, M.J., and Maquat, L.E. (2000b). Pre-mRNA splicing alters mRNP composition: evidence for stable association of proteins at exon-exon junctions. Genes Dev. 14, 1098-1108. (Pubitemid 30324423)
54. 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. (Pubitemid 37222488)
55. Lejeune, F., Ranganathan, A.C., and Maquat, L.E. (2004). eIF4G is required for the pioneer round of translation in mammalian cells. Nat. Struct. Mol. Biol. 11, 992-1000. (Pubitemid 39315304)
56. Maquat, L.E., Hwang, J., Sato, H., and Tang, Y. (2010a). CBP80-promoted mRNP rearrangements during the pioneer round of translation, nonsense-mediated mRNA decay, and thereafter. Cold Spring Harb. Symp. Quant. Biol. 75, 127-134.
57. Maquat, L.E., Tarn, W.Y., and Isken, O. (2010b). The pioneer round of translation: features and functions. Cell 142, 368-374.
58. McCracken, S., Fong, N., Rosonina, E., Yankulov, K., Brothers, G., Siderovski, D., Hessel, A., Foster, S., Shuman, S., and Bentley, D.L. (1997). 5′-Capping enzymes are targeted to pre-mRNA by binding to the phosphorylated carboxy-terminal domain of RNA polymerase II. Genes Dev. 11, 3306-3318. (Pubitemid 28023955)
59. McGlincy, N.J., and Smith, C.W. (2008). Alternative splicing resulting in nonsense-mediated mRNA decay: what is the meaning of nonsense? Trends Biochem. Sci. 33, 385-393.
60. Meaux, S., van Hoof, 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.
61. Meijer, H.A., Kong, Y.W., Lu, W.T., Wilczynska, A., Spriggs, R.V., Robinson, S.W., Godfrey, J.D., Willis, A.E., and Bushell, M. (2013). Translational repression and eIF4A2 activity are critical for microRNA-mediated gene regulation. Science 340, 82-85.
62. 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. (Pubitemid 41184468)
63. Millevoi, S., and Vagner, S. (2010). Molecular mechanisms of eukaryotic pre-mRNA 3′ end processing regulation. Nucleic Acids Res. 38, 2757-2774.
64. Mühlemann, O., and Lykke-Andersen, J. (2010). How and where are nonsense mRNAs degraded in mammalian cells? RNA Biol. 7, 28-32.
65. Nagy, E., and Maquat, L.E. (1998). A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends. Biochem. Sci. 23, 198-199. (Pubitemid 28302613)
66. 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.
67. Ni, J.Z., Grate, L., Donohue, J.P., Preston, C., Nobida, N., O'Brien, G., Shiue, L., Clark, T.A., Blume, J.E., and Ares, M., Jr. (2007). Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay. Genes Dev. 21, 708-718. (Pubitemid 46440292)
68. 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. (Pubitemid 37487927)
69. 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.
70. Peixeiro, I., Inácio, Â., Barbosa, C., Silva, A.L., Liebhaber, S.A., and Româo, 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.
71. Rebbapragada, I., and Lykke-Andersen, J. (2009). Execution of nonsense-mediated mRNA decay: what defines a substrate? Curr. Opin. Cell Biol. 21, 394-402.
72. Rufener, S.C., and Mühlemann, O. (2013). eIF4E-bound mRNPs are substrates for nonsense-mediated mRNA decay in mammalian cells. Nat. Struct. Mol. Biol. 20, 710-717.
73. Saltzman, A.L., Kim, Y.K., Pan, Q., Fagnani, M.M., Maquat, L.E., and Blencowe, B.J. (2008). Regulation of multiple core spliceosomal proteins by alternative splicing-coupled nonsense-mediated mRNA decay. Mol. Cell. Biol. 28, 4320-4330. (Pubitemid 351904954)
74. Sato, H., and Maquat, L.E. (2009). Remodeling of the pioneer translation initiation complex involves translation and the karyopherin importin beta. Genes Dev. 23, 2537-2550.
75. Serin, G., Gersappe, A., Black, J.D., Aronoff, R., and Maquat, L.E. (2001). Identification and characterization of human orthologues to Saccharomyces cerevisiae Upf2 protein and Upf3 protein (Caenorhabditis elegans SMG-4). Mol. Cell. Biol. 21, 209-223.
76. Shatkin, A.J., and Manley, J.L. (2000). The ends of the affair: capping and polyadenylation. Nat. Struct. Biol. 7, 838-842.
77. Shigeoka, T., Kato, S., Kawaichi, M., and Ishida, Y. (2012). Evidence that the Upf1-related molecular motor scans the 3′-UTR to ensure mRNA integrity. Nucleic Acids Res. 40, 6887-6897.
78. 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.
79. 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.
80. Takahashi, S., Araki, Y., Ohya, Y., Sakuno, T., Hoshino, S., Kontani, K., Nishina, H., and Katada, T. (2008). Upf1 potentially serves as a RING-related E3 ubiquitin ligase via its association with Upf3 in yeast. RNA 14, 1950-1958.
81. Topisirovic, I., Svitkin, Y.V., Sonenberg, N., and Shatkin, A.J. (2011). Cap and cap-binding proteins in the control of gene expression. Wiley Interdiscip. Rev. RNA 2, 277-298.
82. Tran, E.J., and Wente, S.R. (2006). Dynamic nuclear pore complexes: life on the edge. Cell 125, 1041-1053. (Pubitemid 43866205)
83. Trcek, T., Sato, H., Singer, R.H., and Maquat, L.E. (2013). Temporal and spatial characterization of nonsense-mediated mRNA decay. Genes Dev. 27, 541-551.
84. Unterholzner, L., and Izaurralde, E. (2004). SMG7 acts as a molecular link between mRNA surveillance and mRNA decay. Mol. Cell 16, 587-596. (Pubitemid 39531881)
85. Wang, D., Zavadil, J., Martin, L., Parisi, F., Friedman, E., Levy, D., Harding, H., Ron, D., and Gardner, L.B. (2011). Inhibition of nonsense-mediated RNA decay by the tumor microenvironment promotes tumorigenesis. Mol. Cell. Biol. 31, 3670-3680.
86. 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.
87. 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.
88. Zhang, J., and Maquat, L.E. (1997). Evidence that translation reinitiation abrogates nonsense-mediated mRNA decay in mammalian cells. EMBO J. 16, 826-833. (Pubitemid 27089529)