In vivo determination of direct targets of the Nonsense-mediated decay pathway in Drosophila

G3: Genes, Genomes, Genetics

Volumn 4, Issue 3, 2014, Pages 485-496

  Chapin, Alex ^a   Hu, Hao ^a,c   Rynearson, Shawn G ^a   Hollien, Julie ^b   Yandell, Mark ^a   Metzstein, Mark M ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF UTAH   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Drosophila; NMD; rEactivation; RNA seq; Upf2

Indexed keywords

MESSENGER RNA;

3' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FEEDBACK SYSTEM; GENE CONTROL; GENE EXPRESSION; GENE TARGETING; GENETIC ASSOCIATION; IN VIVO STUDY; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; TRANSPOSON; UPREGULATION;

DROSOPHILA; NMD; REACTIVATION; RNA-SEQ; UPF2;

3' UNTRANSLATED REGIONS; ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; GENOME; LARVA; PHENOTYPE; RNA INTERFERENCE; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME; UP-REGULATION;

EID: 84896906968     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.113.009357     Document Type: Article

References (83)

1. Anders, S., and W. Huber, 2010 Differential expression analysis for sequence count data. Genome Biol. 11: R106.
2. Avery, P., M. Vicente-Crespo, Francis D., O. Nashchekina, Alonso C.R. et al., 2011 Drosophila Upf1 and Upf2 loss of function inhibits cell growth and causes animal death in a Upf--independent manner. RNA 17: 624- 638.
3. Azzalin C.M., and J. Lingner, 2006 The human RNA surveillance factor UPF1 is required for S phase progression and genome stability. Curr. Biol. 16: 433-439.
4. Barbera-Soler, S., Lambert N.J., and A. M. Zahler, 2009 Global analysis of alternative splicing uncovers developmental regulation of nonsensemediated decay in C. elegans. RNA 15: 1652-1660.
5. Becskei, A., and L. Serrano, 2000 Engineering stability in gene networks by autoregulation. Nature 405: 590-593.
6. Behm-Ansmant, I., Gatfield D., J. Rehwinkel, Hilgers V., and E. Izaurralde, 2007a A conserved role for cytoplasmic poly(A--binding protein 1 (PABPC1) in nonsens--mediated mRNA decay. EMBO J. 26: 1591-1601.
7. Behm-Ansmant, I., Kashima I., J. Rehwinkel, J. Saulière, N. Wittkopp et al., 2007b mRNA quality control: an ancient machinery recognizes and degrades mRNAs with nonsense codons. FEBS Lett. 581: 2845-2853.
8. Brand A.H., and N. Perrimon, 1993 Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
9. Brierley, C., and A. J. Flavell, 1990 The retrotransposon copia controls the relative levels of its gene products post-transcriptionally by differential expression from its two major mRNAs. Nucleic Acids Res. 18: 2947-2951.
10. Brogna, S., 1999 Nonsense mutations in the alcohol dehydrogenase gene of Drosophila melanogaster correlate with an abnormal 39 end processing of the corresponding pr--mRNA. RNA 5: 562-573.
11. Brogna, S., and J. Wen, 2009 Nonsense-mediated mRNA decay (NMD) mechanisms. Nat. Struct. Mol. Biol. 16: 107-113.
12. Bruno I.G., Karam R., L. Huang, Bhardwaj A., Lou C.H. et al., 2011 Identification of a microRNA that activates gene expression by repressing nonsense-mediated RNA decay. Mol. Cell 42: 500-510.
13. Chen, Z., Smith K.R., Batterham P., and C. Robin, 2005 Smg1 nonsense mutations do not abolish nonsense-mediated mRNA decay in Drosophila melanogaster. Genetics 171: 40--406.
14. Chomczynski, P., and N. Sacchi, 1987 Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 15--159.
15. Colak, D., S.-J. Ji, Porse B.T., and S. R. Jaffrey, 2013 Regulation of axon guidance by compartmentalized nonsense-mediated mRNA decay. Cell 153: 1252-1265.
16. de Turris, V., Nicholson P., Orozco R.Z., Singer R.H., and O. Muhlemann, 2011 Cotranscriptional effect of a premature termination codon revealed by live-cell imaging. RNA 17: 2094-2107.
17. Durand, S., Cougot N., F. Mahuteau-Betzer, C.-H. Nguyen, Grierson D.S. et al., 2007 Inhibition of nonsense-mediated mRNA decay (NMD) by a new chemical molecule reveals the dynamic of NMD factors in P-bodies. J. Cell Biol. 178: 1145-1160.
18. Eberle A.B., Stalder L., H. Mathys, Orozco R.Z., and O. Mühlemann, 2008 Posttranscriptional gene regulation by spatial rearrangement of the 39 untranslated region. PLoS Biol. 6: e92.
19. Eberle A.B., S. Lykke-Andersen, O. Mühlemann, and T. H. Jensen, 2009 SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat. Struct. Mol. Biol. 16: 49-55.
20. Frizzell K.A., Rynearson S.G., and M. M. Metzstein, 2012 Drosophila mutants show NMD pathway activity is reduced, but not eliminated, in the absence of Smg6. RNA 18: 147--1486.
21. González C.I., Bhattacharya A., W. Wang, and S. W. Peltz, 2001 Nonsensemediated mRNA decay in Saccharomyces cerevisiae. Gene 274: 15-25.
22. Guan, Q., Zheng W., S. Tang, Liu X., Zinkel R.A. et al., 2006 Impact of nonsense-mediated mRNA decay on the global expression profile of budding yeast. PLoS Genet. 2: e203.
23. Haimovich, G., Medina D.A., Causse S.Z., Garber M., G. Millán-Zambrano et al., 2013 Gene expression is circular: factors for mRNA degradation also foster mRNA synthesis. Cell 153: 100--1011.
24. Hamada, M., Kiryu H., K. Sato, Mituyama T., and K. Asai, 2009 Prediction of RNA secondary structure using generalized centroid estimators. Bioinformatics 25: 465-473.
25. Hansen K.D., Lareau L.F., Blanchette M., Green R.E., Q. Meng et al., 2009 Genome-wide identification of alternative splice forms down-regulated by nonsense-mediated mRNA decay in Drosophila. PLoS Genet. 5: e1000525.
26. He, F., Li X., P. Spatrick, Casillo R., S. Dong et al., 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.
27. Hodgkin, J., Papp A., R. Pulak, Ambros V., and P. Anderson, 1989 A new kind of informational suppression in the nematode Caenorhabditis elegans. Genetics 123: 301-313.
28. Hogg J.R., and S. P. Goff, 2010 Upf1 senses 3'UTR length to potentiate mRNA decay. Cell 143: 379-389.
29. Huang, L., C.-H. Lou, Chan W., Shum E.Y., A. Shao et al., 2011 RNA homeostasis governed by cell type-specific and branched feedback loops acting on NMD. Mol. Cell 43: 950-961.
30. Hurt J.A., Robertson A.D., and C. B. Burge, 2013 Global analyses of UPF1 binding and function reveals expanded scope of nonsense-mediated mRNA decay. Genome Res. 23: 1636-1650.
31. Hwang, J., and L. E. Maquat, 2011 Nonsense-mediated mRNA decay (NMD) in animal embryogenesis: to die or not to die, that is the question. Curr. Opin. Genet. Dev. 21: 42--430.
32. Isken, O., and L. E. Maquat, 2008 The multiple lives of NMD factors: balancing roles in gene and genome regulation. Nat. Rev. Genet. 9: 699-712.
33. Johansson, O M.J.., He F., P. Spatrick, Li C., and A. Jacobson, 2007 Association of yeast Upf1p with direct substrates of the NMD pathway. Proc. Natl. Acad. Sci. USA 104: 20872-20877.
34. Jungreis, I., Lin M.F., Spokony R., Chan C.S., N. Negre et al., 2011 Evidence of abundant stop codon readthrough in Drosophila and other Metazoa. Genome Res. 21: 2096-2113.
35. Kebaara B.W., and A. L. Atkin, 2009 Long 3'-UTRs target wild-type mRNAs for nonsense-mediated mRNA decay in Saccharomyces cerevisiae. Nucleic Acids Res. 37: 2771-2778.
36. Kerényi, Z., Z. Mérai, Hiripi L., A. Benkovics, P. Gyula et al., 2008 Interkingdom conservation of mechanism of nonsense-mediated mRNA decay. EMBO J. 27: 1585-1595.
37. Kertész, S., Z. Kerényi, Z. Mérai, Bartos I., T. Pálfy et al., 2006 Both introns and long 3'-UTRs operate as cis-acting elements to trigger nonsensemediated decay in plants. Nucleic Acids Res. 34: 6147-6157.
38. Kervestin, S., and A. Jacobson, 2012 NMD: a multifaceted response to premature translational termination. Nat. Rev. Mol. Cell Biol. 13: 700- 712.
39. Le Hir, H., Izaurralde E., Maquat L.E., and M. J. Moore, 2000 The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 19: 6860-6869.
40. Leeds, P., Peltz S.W., Jacobson A., and M. R. Culbertson, 1991 The product of the yeast UPF1 gene is required for rapid turnover of mRNAs containing a premature translational termination codon. Genes Dev. 5: 2303- 2314.
41. Lelivelt M.J., and M. R. Culbertson, 1999 Yeast Upf proteins required for RNA surveillance affect global expression of the yeast transcriptome. Mol. Cell. Biol. 19: 6710-6719.
42. Lloyd, B J.P.., and B. Davies, 2013 SMG1 is an ancient nonsense-mediated mRNA decay effector. Plant J. 76: 800-810.
43. Longman, D., Plasterk R., I. Johnstone, and J. Caceres, 2007 Mechanistic insights and identification of two novel factors in the C. elegans NMD pathway. Genes Dev. 21: 1075-1085.
44. Maderazo A.B., Belk J.P., He F., and A. Jacobson, 2003 Nonsensecontaining mRNAs that accumulate in the absence of a functional nonsense-mediated mRNA decay pathway are destabilized rapidly upon its restitution. Mol. Cell. Biol. 23: 842-851.
45. Matia-González A.M., Hasan A., Moe G.H., Mata J., and M. A. Rodríguez-Gabriel, 2013 Functional characterization of Upf1 targets in Schizosaccharomyces pombe. RNA Biol. 10: 1057-1065.
46. Mayr, C., and D. P. Bartel, 2009 Widespread shortening of 3'UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138: 673-684.
47. McIlwain D.R., Pan Q., Reilly P.T., Elia A.J., S. McCracken et al., 2010 Smg1 is required for embryogenesis and regulates diverse genes via alternative splicing coupled to nonsense-mediated mRNA decay. Proc. Natl. Acad. Sci. USA 107: 12186-12191.
48. Medghalchi S.M., Frischmeyer P.A., Mendell J.T., Kelly A.G., Lawler A.M. et al., 2001 Rent1, a trans-effector of nonsense-mediated mRNA decay, is essential for mammalian embryonic viability. Hum. Mol. Genet. 10: 99-105.
49. Mendell J.T., Medghalchi S.M., Lake R.G., Noensie E.N., and H. C. Dietz, 2000 Novel Upf2p orthologues suggest a functional link between translation initiation and nonsense surveillance complexes. Mol. Cell. Biol. 20: 8944-8957.
50. Mendell J.T., Sharifi N.A., Meyers J.L., F. Martinez-Murillo, and H. C. Dietz, 2004 Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat. Genet. 36: 1073-1078.
51. Metze, S., Herzog V.A., M.-D. Ruepp, and O. Mühlemann, 2013 Comparison of EJC-enhanced and EJC-independent NMD in human cells reveals two partially redundant degradation pathways. RNA 19: 1432-1448.
52. Metzstein M.M., and M. A. Krasnow, 2006 Functions of the nonsensemediated mRNA decay pathway in Drosophila development. PLoS Genet. 2: e180.
53. Neu-Yilik, G., Gehring N., M. Hentze, and A. Kulozik, 2004 Nonsensemediated mRNA decay: from vacuum cleaner to Swiss army knife. Genome Biol. 5: 218.
54. Nicholson, P., Yepiskoposyan H., S. Metze, R. Zamudio Orozco, N. Kleinschmidt et al., 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.
55. Nix D.A., Courdy S.J., and K. M. Boucher, 2008 Empirical methods for controlling false positives and estimating confidence in ChIP-Seq peaks. BMC Genomics 9: 523.
56. Palacios I.M., 2013 Nonsense-mediated mRNA decay: from mechanistic insights to impacts on human health. Brief. Funct. Genomics 12: 25-36.
57. Peltz S.W., Brown A.H., and A. Jacobson, 1993 mRNA destabilization triggered by premature translational termination depends on at least three cis-acting sequence elements and one trans-acting factor. Genes Dev. 7: 1737-1754.
58. Ramani A.K., Nelson A.C., Kapranov P., I. Bell, Gingeras T.R. et al., 2009 High resolution transcriptome maps for wild-type and nonsensemediated decay-defective Caenorhabditis elegans. Genome Biol. 10: R101.
59. Rayson, S., L. Arciga-Reyes, Wootton L., M. De Torres Zabala, W. Truman et al., 2012 A role for nonsense-mediated mRNA decay in plants: pathogen responses are induced in Arabidopsis thaliana NMD mutants. PLoS ONE 7: e31917.
60. Rehwinkel, J., Letunic I., J. Raes, Bork P., and E. Izaurralde, 2005 Nonsense-mediated mRNA decay factors act in concert to regulate common mRNA targets. RNA 11: 1530-1544.
61. Riehs, N., Akimcheva S., J. Puizina, Bulankova P., Idol R.A. et al., 2008 Arabidopsis SMG7 protein is required for exit from meiosis. J. Cell Sci. 121: 2208-2216.
62. Roberts T.L., Ho U., J. Luff, Lee C.S., Apte S.H. et al., 2013 Smg1 haploinsufficiency predisposes to tumor formation and inflammation. Proc. Natl. Acad. Sci. USA 110: E285-E294.
63. Rodríguez-Gabriel M.A., Watt S., J. Bähler, and P. Russell, 2006 Upf1, an RNA helicase required for nonsense-mediated mRNA decay, modulates the transcriptional response to oxidative stress in fission yeast. Mol. Cell. Biol. 26: 6347-6356.
64. Roman, G., He J., and R. L. Davis, 2000 kurtz, a novel nonvisual arrestin, is an essential neural gene in Drosophila. Genetics 155: 1281-1295.
65. Schweingruber, C., Rufener S.C., D. Zünd, Yamashita A., and O. Mühlemann, 2013 Nonsense-mediated mRNA decay-Mechanisms of substrate mRNA recognition and degradation in mammalian cells. Biochim. Biophys. Acta. 1829: 612-623.
66. Singh, G., Rebbapragada I., and J. Lykke-Andersen, 2008 A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol. 6: e111.
67. Smyth G.K., and T. Speed, 2003 Normalization of cDNA microarray data. Methods 31: 26--273.
68. Stapleton, M., Liao G., P. Brokstein, Hong L., P. Carninci et al., 2002 The Drosophila gene collection: identification of putative full-length cDNAs for 70% of D. melanogaster genes. Genome Res. 12: 1294-1300.
69. Strand D.J., and J. F. McDonald, 1985 Copia is transcriptionally responsive to environmental stress. Nucleic Acids Res. 13: 4401-4410.
70. Sullivan, W., Ashburner M., and R. S. Hawley, 2000 Drosophila Protocols. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
71. Sun, M., Schwalb B., N. Pirkl, Maier K.C., A. Schenk et al., 2013 Global analysis of eukaryotic mRNA degradation reveals xrn1-dependent buffering of transcript levels. Mol. Cell 52: 52-62
72. Tani, H., Imamachi N., Salam K.A., Mizutani R., K. Ijiri et al., 2012a Identification of hundreds of novel UPF1 target transcripts by direct determination of whole transcriptome stability. RNA Biol. 9: 1370-1379.
73. Tani, H., Mizutani R., Salam K.A., Tano K., K. Ijiri et al., 2012b Genomewide determination of RNA stability reveals hundreds of short-lived noncoding transcripts in mammals. Genome Res. 22: 947-956.
74. Trapnell, C., Roberts A., L. Goff, Pertea G., D. Kim et al., 2012 Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7: 562-578.
75. Varsally, W., and S. Brogna, 2012 UPF1 involvement in nuclear functions. Biochem. Soc. Trans. 40: 778-783.
76. Viegas M.H., Gehring N.H., Breit S., Hentze M.W., and A. E. Kulozik, 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.
77. Weischenfeldt, J., Damgaard I., D. Bryder, K. Theilgaard-Mönch, Thoren L.A. et al., 2008 NMD is essential for hematopoietic stem and progenitor cells and for eliminating by-products of programmed DNA rearrangements. Genes Dev. 22: 1381-1396.
78. Weischenfeldt, J., Waage J., G. Tian, Zhao J., I. Damgaard et al., 2012 Mammalian tissues defective in nonsense-mediated mRNA decay display highly aberrant splicing patterns. Genome Biol. 13: R35.
79. Wittkopp, N., Huntzinger E., C. Weiler, J. Saulière, S. Schmidt et al., 2009 Nonsense-mediated mRNA decay effectors are essential for zebrafish embryonic development and survival. Mol. Cell. Biol. 29: 351-- 3528.
80. Wittmann, J., Hol E.M., and H.-M. Jäck, 2006 hUPF2 silencing identifies physiologic substrates of mammalian nonsense-mediated mRNA decay. Mol. Cell. Biol. 26: 1272-1287.
81. Xu, T., and G. Rubin, 1993 Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117: 1223-1237.
82. Yepiskoposyan, H., Aeschimann F., D. Nilsson, Okoniewski M., and O. Mühlemann, 2011 Autoregulation of the nonsense-mediated mRNA decay pathway in human cells. RNA 17: 2108-2118.
83. Zünd, D., Gruber A.R., Zavolan M., and O. Mühlemann, 2013 Translationdependent displacement of UPF1 from coding sequences causes its enrichment in 39 UTRs. Nat. Struct. Mol. Biol. 20: 936-943.