Identification of elements in human long 3′ UTRs that inhibit nonsense-mediated decay

RNA

Volumn 21, Issue 5, 2015, Pages 887-897

  Toma, Kalodiah G ^a   Rebbapragada, Indrani ^b   Durand, Sébastien ^a,b   Lykke Andersen, Jens ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Long 3 UTR; NMD inhibition; Nonsense mediated decay; UPF1

Indexed keywords

MEMBRANE PROTEIN; MESSENGER RNA; TRANSLOCATION ASSOCIATED MEMBRANE PROTEIN 1; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; CARRIER PROTEIN; CRIPT PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TRAM1 PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN; UPF1 PROTEIN, HUMAN;

3' UNTRANSLATED REGION; ARTICLE; CODON; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; NONSENSE MEDIATED MRNA DECAY; POLYSOME; PRIORITY JOURNAL; RNA DEGRADATION; GENETICS; HELA CELL LINE; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; REGULATORY SEQUENCE;

3' UNTRANSLATED REGIONS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BASE SEQUENCE; HELA CELLS; HUMANS; MEMBRANE GLYCOPROTEINS; MEMBRANE TRANSPORT PROTEINS; NONSENSE MEDIATED MRNA DECAY; POLYRIBOSOMES; REGULATORY ELEMENTS, TRANSCRIPTIONAL; TRANS-ACTIVATORS;

EID: 84928042455     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.048637.114     Document Type: Article

References (51)

1. Amrani N, Ganesan R, Kervestin S, Mangus DA, Ghosh S, Jacobson A. 2004. A faux 3′-UTR promotes aberrant termination and triggers nonsense-mediated mRNA decay. Nature 432: 112-118.
2. Balistreri G, Horvath P, Schweingruber C, Zünd D, McInerney G, Merits A, Muhlemann O, Azzalin C, Helenius A. 2014. The host nonsense-mediated mRNA decay pathway restricts mammalian RNA virus replication. Cell Host Microbe 16: 403-411.
3. Bollig F, Winzen R, Gaestel M, Kostka S, Resch K, Holtmann H. 2003. Affinity purification of ARE-binding proteins identifies polyA-binding protein 1 as a potential substrate in MK2-induced mRNA stabilization. Biochem Biophys Res Commun 301: 665-670.
4. Bruno IG, Karam R, Huang L, Bhardwaj A, Lou CH, Shum EY, Song HW, Corbett MA, Gifford WD, Gecz J, et al. 2011. Identification of a microRNA that activates gene expression by repressing nonsense-mediated RNA decay. Mol Cell 42: 500-510.
5. Buhler M, Steiner S, Mohn F, Paillusson A, Mühlemann O. 2006. EJC-independent degradation of nonsense immunoglobulin-μ mRNA depends on 3′ UTR length. Nat Struct Mol Biol 13: 462-464.
6. Chang YF, Imam JS, Wilkinson MF. 2007. The nonsense-mediated decay RNA surveillance pathway. Annu Rev Biochem 76: 51-74.
7. Chen CY, Chen ST, Juan HF, Huang HC. 2012. Lengthening of 3′ UTR increases with morphological complexity in animal evolution. Bioinformatics 28: 3178-3181.
8. Doma MK, Parker R. 2007. RNA quality control in eukaryotes. Cell 131: 660-668.
9. Eberle AB, Stalder L, Mathys H, Orozco RZ, Mühlemann O. 2008. Posttranscriptional gene regulation by spatial rearrangement of the 3′ untranslated region. PLoS Biol 6: e92.
10. Fatscher T, Boehm V, Weiche B, Gehring NH. 2014. The interaction of cytoplasmic poly(A)-binding protein with eukaryotic initiation factor 4G suppresses nonsense-mediated mRNA decay. RNA 20: 1579-1592.
11. Frischmeyer PA, Dietz HC. 1999. Nonsense-mediated mRNA decay in health and disease. Hum Mol Genet 8: 1893-1900.
12. Frischmeyer-Guerrerio PA, Montgomery RA, Warren DS, Cooke SK, Lutz J, Sonnenday CJ, Guerrerio AL, Dietz HC. 2011. Perturbation of thymocyte development in nonsense-mediated decay (NMD)-deficient mice. Proc Natl Acad Sci 108: 10638-10643.
13. Gehring NH, Neu-Yilik G, Schell T, HentzeMW, Kulozik AE. 2003. Y14 and hUpf3b form an NMD-activating complex. Mol Cell 11: 939-949.
14. Gehring NH, Kunz JB, Neu-Yilik G, Breit S, Viegas MH, Hentze MW, Kulozik AE. 2005. Exon-junction complex components specify distinct routes of nonsense-mediated mRNA decay with differential cofactor requirements. Mol Cell 20: 65-75.
15. Gong C, Kim YK, Woeller CF, Tang Y, Maquat LE. 2009. SMD and NMD are competitive pathways that contribute to myogenesis: effects on PAX3 and myogenin mRNAs. Genes Dev 23: 54-66.
16. Hogg JR, Goff SP. 2010. Upf1 senses 3′UTR length to potentiate mRNA decay. Cell 143: 379-389.
17. Huang L, Lou CH, Chan W, Shum EY, Shao A, Stone E, Karam R, Song HW, Wilkinson MF. 2011. RNA homeostasis governed by cell type-specific and branched feedback loops acting on NMD. Mol Cell 43: 950-961.
18. Hurt JA, Robertson AD, Burge CB. 2013. Global analyses of UPF1 binding and function reveal expanded scope of nonsense-mediated mRNA decay. Genome Res 23: 1636-1650.
19. Ivanov PV, Gehring NH, Kunz JB, Hentze MW, Kulozik AE. 2008. Interactions between UPF1, eRFs, PABP and the exon junction complex suggest an integrated model for mammalian NMD pathways. EMBO J 27: 736-747.
20. Johannes G, Sarnow P. 1998. Cap-independent polysomal association of natural mRNAs encoding c-myc, BiP, and eIF4G conferred by internal ribosome entry sites. RNA 4: 1500-1513.
21. Kashima I, Jonas S, Jayachandran U, Buchwald G, Conti E, Lupas AN, 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.
22. Kim VN, Kataoka N, Dreyfuss G. 2001. Role of the nonsense-mediated decay factor hUpf3 in the splicing-dependent exon-exon junction complex. Science 293: 1832-1836.
23. Kuzmiak HA, Maquat LE. 2006. Applying nonsense-mediated mRNA decay research to the clinic: progress and challenges. Trends Mol Med 12: 306-316.
24. Le Hir H, Izaurralde E, Maquat LE, Moore MJ. 2000a. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J 19: 6860-6869.
25. Le Hir H, Moore MJ, Maquat LE. 2000b. Pre-mRNA splicing alters mRNP composition: evidence for stable association of proteins at exon-exon junctions. Genes Dev 14: 1098-1108.
26. Le Hir H, Gatfield D, Izaurralde E, Moore MJ. 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.
27. Lou CH, Shao A, Shum EY, Espinoza JL, Huang L, Karam R, Wilkinson MF. 2014. Posttranscriptional control of the stem cell and neurogenic programs by the nonsense-mediated RNA decay pathway. Cell Rep 6: 748-764.
28. Lykke-Andersen J, Shu MD, Steitz JA. 2000. Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell 103: 1121-1131.
29. Lykke-Andersen J, Shu MD, Steitz JA. 2001. Communication of the position of exon-exon junctions to the mRNA surveillance machinery by the protein RNPS1. Science 293: 1836-1839.
30. Maquat LE. 2005. Nonsense-mediated mRNA decay in mammals. J Cell Sci 118: 1773-1776.
31. Mendell JT, Sharifi NA, Meyers JL, Martinez-Murillo F, Dietz HC. 2004. Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat Genet 36: 1073-1078.
32. Nicholson P, Yepiskoposyan H, Metze S, Zamudio Orozco R, Kleinschmidt N, Muhlemann O. 2010. Nonsense-mediated mRNA decay in human cells: mechanistic insights, functions beyond quality control and the double-life of NMD factors. Cell Mol Life Sci 67: 677-700.
33. Peixeiro I, Inácio Â, Barbosa C, Silva AL, Liebhaber SA, 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.
34. Pesole G, Liuni S, Grillo G, Licciulli F, Larizza A, Makalowski W, Saccone C. 2000. UTRdb and UTRsite: specialized databases of sequences and functional elements of 5′ and 3′ untranslated regions of eukaryotic mRNAs. Nucleic Acids Res 28: 193-196.
35. Popp MW, Maquat LE. 2013. Organizing principles of mammalian nonsense-mediated mRNA decay. Annu Rev Genet 47: 139-165.
36. Rebbapragada I, Lykke-Andersen J. 2009. Execution of nonsense-mediated mRNA decay: What defines a substrate? Curr Opin Cell Biol 21: 394-402.
37. Ruiz-Echevarria MJ, Peltz SW. 2000. The RNA binding protein Pub1 modulates the stability of transcripts containing upstream open reading frames. Cell 101: 741-751.
38. Ruiz-Echevarria MJ, González CI, Peltz SW. 1998. Identifying the right stop: determining how the surveillance complex recognizes and degrades an aberrant mRNA. EMBO J 17: 575-589.
39. Schmid M, Jensen TH. 2010. Nuclear quality control of RNA polymerase II transcripts. Wiley Interdiscip Rev RNA 1: 474-485.
40. Schweingruber C, Rufener SC, Zund D, Yamashita A, Mühlemann O. 2013. Nonsense-mediated mRNA decay - mechanisms of substrate mRNA recognition and degradation in mammalian cells. Biochim Biophys Acta 1829: 612-623.
41. Silva AL, Ribeiro P, Inácio Â, Liebhaber SA, 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.
42. Singh G, Lykke-Andersen J. 2003. New insights into the formation of active nonsense-mediated decay complexes. Trends Biochem Sci 28: 464-466.
43. Singh G, Jakob S, Kleedehn MG, Lykke-Andersen J. 2007. Communication with the exon-junction complex and activation of nonsense-mediated decay by human Upf proteins occur in the cytoplasm. Mol Cell 27: 780-792.
44. Singh G, Rebbapragada I, Lykke-Andersen J. 2008. A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol 6: e111.
45. Sladic RT, Lagnado CA, Bagley CJ, Goodall GJ. 2004. Human PABP binds AU-rich RNA via RNA-binding domains 3 and 4. Eur J Biochem 271: 450-457.
46. Tani H, Imamachi N, Salam KA, Mizutani R, Ijiri K, Irie T, Yada T, Suzuki Y, Akimitsu N. 2012. Identification of hundreds of novel UPF1 target transcripts by direct determination of whole transcriptome stability. RNA Biol 9: 1370-1379.
47. Viegas MH, Gehring NH, Breit S, Hentze MW, Kulozik AE. 2007. The abundance of RNPS1, a protein component of the exon junction complex, can determine the variability in efficiency of the Nonsense Mediated Decay pathway. Nucleic Acids Res 35: 4542-4551.
48. Weil JE, Beemon KL. 2006. A 3′ UTR sequence stabilizes termination codons in the unspliced RNA of Rous sarcoma virus. RNA 12: 102-110.
49. Weischenfeldt J, Damgaard I, Bryder D, Theilgaard-Mönch K, Thoren LA, Nielsen FC, Jacobsen SE, Nerlov C, Porse BT. 2008. NMD is essential for hematopoietic stem and progenitor cells and for eliminating by-products of programmed DNA rearrangements. Genes Dev 22: 1381-1396.
50. Wittmann J, Hol EM, Jäck HM. 2006. hUPF2 silencing identifies physiologic substrates of mammalian nonsense-mediated mRNA decay. Mol Cell Biol 26: 1272-1287.
51. Yepiskoposyan H, Aeschimann F, Nilsson D, Okoniewski M, Mühlemann O. 2011. Autoregulation of the nonsense-mediated mRNA decay pathway in human cells. RNA 17: 2108-2118.