The mammalian nonsense-mediated mRNA decay pathway: To decay or not to decay! Which players make the decision?

FEBS Letters

Volumn 583, Issue 3, 2009, Pages 499-505

  Silva, Ana Luísa ^a   Romão, Luísa ^a  

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

Author keywords

NMD factor; Nonsense mediated mRNA decay; Poly(A) binding protein; Premature translation termination codon; RNA protein interaction

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOPROTEIN; POLYADENYLIC ACID BINDING PROTEIN; PROTEIN SMG1; PROTEIN SMG5; PROTEIN SMG6; PROTEIN SMG7; PROTEIN UPF1; TRIOSEPHOSPHATE ISOMERASE; UNCLASSIFIED DRUG;

ENZYME ACTIVITY; ENZYME REGULATION; EXON; GENE TARGETING; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RNA BINDING; RNA SPLICING; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; SHORT SURVEY; STOP CODON;

ANIMALS; CODON, NONSENSE; HUMANS; MAMMALS; RNA SPLICING; RNA STABILITY; RNA, MESSENGER; TRANS-ACTIVATORS;

MAMMALIA;

EID: 58649117962     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2008.12.058     Document Type: Short Survey

References (67)

1. Moore M.J. From birth to death: the complex lives of eukaryotic mRNAs. Science 309 (2005) 1514-1518
2. Fasken M.B., and Corbett A.H. Process or perish: quality control in mRNA biogenesis. Nat. Struct. Mol. Biol. 12 (2005) 482-488
3. Holbrook J.A., Neu-Yilik G., Hentze A.E., and Kulozik M.W. Nonsense-mediated decay approaches the clinic. Nat. Genet. 36 (2004) 801-808
4. Chang Y.F., Imam J.S., and Wilkinson M.F. The nonsense-mediated decay RNA surveillance pathway. Annu. Rev. Biochem. 76 (2007) 51-74
5. Maquat L.E. Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nat. Rev. Mol. Cell. Biol. 5 (2004) 89-99
6. Mendell J.T., Sharifi N.A., Meyers J.L., Martinez-Murillo F., and Dietz H.C. Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat. Genet. 36 (2004) 1073-1078
7. Rehwinkel J., Raes J., and Izaurralde E. Nonsense-mediated mRNA decay: target genes and functional diversification of effectors. Trend Biochem. Sci. 31 (2006) 639-646
8. Rehwinkel J., Letunic I., Raes J., Bork P., and Izaurralde E. Nonsense-mediated mRNA decay factors act in concert to regulate common mRNA targets. RNA 11 (2005) 1530-1544
9. He F., Li X., Spatrick P., Casillo R., Dong S., and Jacobson A. Genome-wide analysis of mRNAs regulated by the nonsense-mediated and 5′ to 3′ mRNA decay pathways in yeast. Mol. Cell. 12 (2003) 1439-1452
10. Wittmann J., Hol E.M., and Jack H.M. HUPF2 silencing identifies physiologic substrates of mammalian nonsense-mediated mRNA decay. Mol. Cell. Biol. 26 (2006) 1272-1287
11. Conti E., and Izaurralde E. Nonsense-mediated mRNA decay: molecular insights and mechanistic variations across species. Curr. Opin. Cell. Biol. 17 (2005) 316-325
12. Nagy E., and Maquat L.E. A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trend Biochem. Sci. 23 (1998) 198-199
13. Zhang J., Sun X., Qian Y., LaDuca J.P., and Maquat L.E. At least one intron is required for the nonsense-mediated decay of triosephosphate isomerase mRNA: a possible link between nuclear splicing and cytoplasmic translation. Mol. Cell. Biol. 18 (1998) 5272-5283
14. Zhang J., Sun X., Qian Y., and 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 4 (1998) 801-815
15. Neu-Yilik G., Gehring N.H., Thermann R., Frede U., Hentze M.W., and Kulozik A.E. Splicing and 3′ end formation in the definition of nonsense-mediated decay-competent human beta-globin mRNPs. EMBO J. 20 (2001) 532-540
16. Thermann R., Neu-Yilik G., Deters A., Frede U., Wehr K., Hagemeier C., Hentze M.W., and Kulozik A.E. Binary specification of nonsense codons by splicing and cytoplasmic translation. EMBO J. 17 (1998) 3484-3494
17. Maquat L.E., and Li X. Mammalian heat shock p70 and histone H4 transcripts, which derive from naturally intronless genes, are immune to nonsense-mediated decay. RNA 7 (2001) 445-456
18. Brocke K.S., Neu-Yilik G., Gehring N.H., Hentze M.W., and Kulozik A.E. The human intronless melanocortin 4-receptor gene is NMD insensitive. Hum. Mol. Genet. 11 (2002) 331-335
19. Le Hir H., Izaurralde E., Maquat L.E., and Moore M.J. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon-junctions. EMBO J. 19 (2000) 6860-6869
20. Le Hir H., Gatfield D., Izaurralde E., and Moore M.J. The exon-exon-junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO J. 20 (2001) 4987-4997
21. Tange T.O., Nott A., and Moore M.J. The ever-increasing complexities of the exon-junction complex. Curr. Opin. Cell. Biol. 16 (2004) 279-284
22. Kim V.N., Kataoka N., and Dreyfuss G. Role of the nonsense-mediated decay factor hUpf3 in the splicing-dependent exon-exon-junction complex. Science 293 (2001) 1832-1836
23. Lykke-Andersen J., Shu M.D., and Steitz J.A. Communication of the position of exon-exon-junctions to the mRNA surveillance machinery by the protein RNPS1. Science 293 (2001) 1836-1839
24. Gehring N.H., Neu-Yilik G., Schell T., Hentze M.W., and Kulozik A.E. Y14 and hUpf3b form an NMD-activating complex. Mol. Cell. 11 (2003) 939-949
25. Bono F., Ebert J., Unterholzner L., Guttler T., Izaurralde E., and Conti E. Molecular insights into the interaction of PYM with the Mago-Y14 core of the exon-junction complex. EMBO Rep. 53 (2004) 04-10
26. Palacios I.M., Gatfield D., St Johnston D., and Izaurralde E. An eIF4AIII-containing complex required for mRNA localization and nonsense-mediated mRNA decay. Nature 427 (2004) 753-757
27. Rajavel K.S., and Neufeld E.F. Nonsense-mediated decay of human HEXA mRNA. Mol. Cell. Biol. 21 (2001) 5512-5519
28. Buhler M., Steiner S., Mohn F., Paillusson A., and Muhlemann O. EJC-independent degradation of nonsense immunoglobulin-mu mRNA depends on 3′-UTR length. Nat. Struct. Mol. Biol. 13 (2006) 462-464
29. Eberle A.B., Stalder L., Mathys H., Orozco R.Z., and Mühlemann O. Posttranscriptional gene regulation by spatial rearrangement of the 3′ untranslated region. PLoS Biol. 6 (2008) e92
30. Singh G., Rebbapragada I., and Lykke-Andersen J. A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol. 6 (2008) e111
31. Lykke-Andersen J., Shu M.D., and Steitz J.A. Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination-codon. Cell 103 (2000) 1121-1131
32. Mendell J.T., Medghalchi S.M., Lake R.G., Noensie E.N., and Dietz H.C. Novel Upf2p orthologs suggest a functional link between translation initiation and nonsense surveillance complexes. Mol. Cell. Biol. 20 (2000) 8944-8957
33. Serin G., Gersappe A., Black J.D., Aronoff R., and Maquat L.E. Identification and characterization of human orthologues to Saccharomyces cerevisiae Upf2 protein and Upf3 protein (Caenorhabditis elegans SMG-4). Mol. Cell. Biol. 21 (2001) 209-223
34. Pal M., Ishigaki Y., Nagy E., and 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 7 (2001) 5-15
35. Yamashita A., Ohnishi T., Kashima I., Taya Y., and 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 (2001) 2215-2228
36. Ohnishi T., Yamashita A., Kashima I., Schell T., Anders K.R., Grimson A., Hachiya T., Hentze M.W., Anderson P., and Ohno S. Phosphorylation of hUPF1 induces formation of mRNA surveillance complexes containing hSMG-5 and hSMG-7. Mol. Cell. 12 (2003) 1187-1200
37. Kadlec J., Izaurralde E., and Cusack S. The structural basis for the interaction between nonsense-mediated mRNA decay factors UPF2 and UPF3. Nat. Struct. Mol. Biol. 11 (2004) 330-337
38. Sun X., Perlick H.A., Dietz H.C., and Maquat L.E. A mutated human homologue to yeast Upf1 protein has a dominant-negative effect on the decay of nonsense-containing mRNAs in mammalian cells. Proc. Natl. Acad. Sci. USA 95 (1998) 10009-10014
39. Mendell J.T., Rhys C.M., and Dietz H.C. Separable roles for rent1/hUpf1 in altered splicing and decay of nonsense transcripts. Science 298 (2002) 419-422
40. Kim Y.K., Furic L., Desgroseillers L., and Maquat L.E. Mammalian Staufen1 recruits Upf1 to specific mRNA 3'UTRs so as to elicit mRNA decay. Cell 120 (2005) 195-208
41. Kunz J.B., Neu-Yilik G., Hentze M.W., Kulozik A.E., and Gehring N.H. Functions of hUpf3a and hUpf3b in nonsense-mediated mRNA decay and translation. RNA 12 (2006) 1015-1022
42. Gehring N.H., Kunz J.B., Neu-Yilik G., Breit S., Viegas M.H., Hentze M.W., and Kulozik A.E. Exon-junction complex components specify distinct routes of nonsense-mediated mRNA decay with differential cofactor requirements. Mol. Cell. 20 (2005) 65-75
43. Chan W.K., Huang L., Gudikote J.P., Chang Y.F., Imam J.S., MacLean II J.A., and Wilkinson M.F. An alternative branch of the nonsense-mediated decay pathway. EMBO J. 26 (2007) 1820-1830
44. Tarpey P.S., Raymond F.L., Nguyen L.S., et al. Mutations in UPF3B, a member of the nonsense-mediated mRNA decay complex, cause syndromic and nonsyndromic mental retardation. Nat. Genet. 39 (2007) 1127-1133
45. Chiu S.Y., Serin G., Ohara O., and Maquat L.E. Characterization of human Smg5/7a: a protein with similarities to Caenorhabditis elegans SMG5 and SMG7 that functions in the dephosphorylation of Upf1. RNA 9 (2003) 77-87
46. Fukuhara N., Ebert J., Unterholzner L., Lindner D., Izaurralde E., and Conti E. SMG7 is a 14-3-3-like adaptor in the nonsense-mediated mRNA decay pathway. Mol. Cell. 17 (2005) 537-547
47. Unterholzner L., and Izaurralde E. SMG7 acts as a molecular link between mRNA surveillance and mRNA decay. Mol. Cell. 16 (2004) 587-596
48. Durand S., Cougot N., Mahuteau-Betzer F., Nguyen C.H., Grierson D.S., Bertrand E., Tazi J., and Lejeune F. Inhibition of nonsense-mediated mRNA decay (NMD) by a new chemical molecule reveals the dynamic of NMD factors in P-bodies. J. Cell. Biol. 78 (2007) 1145-1160
49. Glavan F., Behm-Ansmant I., Izaurralde E., and Conti E. Structures of the PIN domains of SMG6 and SMG5 reveal a nuclease within the mRNA surveillance complex. EMBO J. 25 (2006) 5117-5125
50. Huntzinger, E., Kashima, I., Fauser, M., Saulière, J. and Izaurralde, E. (2008). SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA 14, 2609-2617.
51. Kashima I., Yamashita A., Izumi N., Kataoka N., Morishita R., Hoshino S., Ohno M., Dreyfuss G., and 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. 20 (2006) 355-367
52. Isken O., Kim Y.K., Hosoda N., Mayeur G.L., Hershey J.W., and Maquat L.E. Upf1 phosphorylation triggers translational repression during nonsense-mediated mRNA decay. Cell 133 (2008) 314-327
53. Ivanov P.V., Gehring N.H., Kunz J.B., Hentze M.W., and Kulozik A.E. Interactions between UPF1, eRFs, PABP and the exon-junction complex suggest an integrated model for mammalian NMD pathways. EMBO J. 27 (2008) 736-747
54. Culbertson M.R., and Leeds P.F. Looking at mRNA decay pathways through the window of molecular evolution. Curr. Opin. Genet. Dev. 13 (2003) 207-214
55. Longman D., Plasterk R.H., Johnstone I.L., and Caceres J.F. Mechanistic insights and identification of two novel factors in the Caenorhabditis elegans NMD pathway. Genes Dev. 21 (2007) 1075-1085
56. Gatfield D., Unterholzner L., Ciccarelli F.D., Bork P., and Izaurralde E. Nonsense-mediated mRNA decay in Drosophila: at the intersection of the yeast and mammalian pathways. EMBO J. 22 (2003) 3960-3967
57. Kertesz S., Kerenyi Z., Merai Z., Bartos I., Palfy T., Barta E., and Silhavy D. Both introns and long 3′-UTRs operate as cis-acting elements to trigger nonsense-mediated decay in plants. Nucl. Acid Res. 34 (2006) 6147-6157
58. Gonzalez C.I., Ruiz-Echevarria M.J., Vasudevan S., Henry M.F., and Peltz S.W. The yeast hnRNP-like protein Hrp1/Nab4 marks a transcript for nonsense-mediated mRNA decay. Mol. Cell. 5 (2000) 489-499
59. Amrani N., Ganesan R., Kervestin S., Mangus D.A., Ghosh S., and Jacobson A. A faux 3'-UTR promotes aberrant termination and triggers nonsense-mediated mRNA decay. Nature 432 (2004) 112-118
60. Muhlrad D., and Parker R. Aberrant mRNAs with extended 3′-UTRs are substrates for rapid degradation by mRNA surveillance. RNA 5 (1999) 1299-1307
61. Behm-Ansmant I., Gatfield D., Rehwinkel J., Hilgers V., and Izaurralde E. A conserved role for cytoplasmic poly(A)-binding protein 1 (PABPC1) in nonsense-mediated mRNA decay. EMBO J. 26 (2007) 1591-1601
62. Silva A.L., Ribeiro P., Inácio A., Liebhaber S.A., and Romão L. Proximity of the poly(A)-binding protein to a premature termination-codon inhibits mammalian nonsense-mediated mRNA decay. RNA 14 (2008) 563-576
63. Mangus D.A., Evans M.C., and Jacobson A. Poly(A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol. 4 (2003) 223
64. Meaux S., van Hoof A., and Baker K.E. Nonsense-mediated mRNA decay in yeast does not require PAB1 or a poly(A) tail. Mol. Cell. 29 (2008) 134-140
65. Lejeune F., Li X., and Maquat L.E. Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol. Cell. 12 (2003) 675-687
66. Körner C.G., and Wahle E. Poly(A) tail shortening by a mammalian poly(A)-specific 3′-exoribonuclease. J. Biol. Chem. 272 (1997) 10448-10456
67. Körner C.G., Wormington M., Muckenthaler M., Schneider S., Dehlin E., and Wahle E. The deadenylating nuclease (DAN) is involved in poly(A) tail removal during the meiotic maturation of Xenopus oocytes. EMBO J. 17 (1998) 5427-5437