Mammalian tissues defective in nonsense-mediated mRNA decay display highly aberrant splicing patterns

Genome Biology

Volumn 13, Issue 5, 2012, Pages

  Weischenfeldt, Joachim ^a,b,c   Waage, Johannes ^a,b,c   Tian, Geng ^d   Zhao, Jing ^d   Damgaard, Inge ^a,b,c   Jakobsen, Janus S ^a,b   Kristiansen, Karsten ^c   Krogh, Anders ^b,c   Wang, Jun ^c,d   Porse, Bo T ^a,b,c  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d BGI SHENZHEN   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; MESSENGER RNA; PROTEIN UPF2; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; DNA MODIFICATION; GENE EXPRESSION REGULATION; GENE MAPPING; GENETIC CONSERVATION; GENETIC SUSCEPTIBILITY; MOUSE; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RNA ANALYSIS; RNA SEQUENCE; UPREGULATION; ANIMAL; GENETICS; GENOME; MALE; MAMMAL; METABOLISM; STOP CODON;

MAMMALIA;

ALTERNATIVE SPLICING; ANIMALS; CODON, NONSENSE; GENOME; MALE; MAMMALS; MICE; NONSENSE MEDIATED MRNA DECAY; RNA, MESSENGER;

EID: 84861333042     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2012-13-5-r35     Document Type: Article

References (47)

1. Black DL. Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 2003, 72:291-336. 10.1146/annurev.biochem.72.121801.161720, 12626338.
2. Pan Q, Shai O, Lee L, Frey B, Blencowe BJ. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 2008, 40:1413-1415. 10.1038/ng.259, 18978789.
3. Wang E, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore S, Schroth G, Burge CB. Alternative isoform regulation in human tissue transcriptomes. Nature 2008, 456:470-476. 10.1038/nature07509, 2593745, 18978772.
4. Lewis BP, Green RE, Brenner SE. Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc Natl Acad Sci USA 2003, 100:189-192. 10.1073/pnas.0136770100, 140922, 12502788.
5. Rehwinkel J, Letunic I, Raes J, Bork P, Izaurralde E. Nonsense-mediated mRNA decay factors act in concert to regulate common mRNA targets. RNA 2005, 11:1530-1544. 10.1261/rna.2160905, 1370837, 16199763.
6. Wittmann J, Hol EM, Jäck H-M. hUPF2 silencing identifies physiologic substrates of mammalian nonsense-mediated mRNA decay. Mol Cell Biol 2006, 26:1272-1287. 10.1128/MCB.26.4.1272-1287.2006, 1367210, 16449641.
7. Weischenfeldt J, Damgaard I, Bryder D, Theilgaard-Mönch K, Thoren LA, Nielsen FC, Jacobsen SEW, Nerlov C, Porse BT. NMD is essential for hematopoietic stem and progenitor cells and for eliminating by-products of programmed DNA rearrangements. Genes Dev 2008, 22:1381-1396. 10.1101/gad.468808, 2377192, 18483223.
8. Gardner LB. Nonsense-mediated RNA decay regulation by cellular stress: implications for tumorigenesis. Mol Cancer Res 2010, 8:295-308. 10.1158/1541-7786.MCR-09-0502, 2841721, 20179151.
9. Perlick HA, Medghalchi SM, Spencer FA, Kendzior RJ, Dietz HC. Mammalian orthologues of a yeast regulator of nonsense transcript stability. Proc Natl Acad Sci USA 1996, 93:10928-10932. 10.1073/pnas.93.20.10928, 38260, 8855285.
10. Lykke-Andersen J, Shu MD, Steitz JA. Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell 2000, 103:1121-1131. 10.1016/S0092-8674(00)00214-2, 11163187.
11. Le Hir H, Gatfield D, Izaurralde E, Moore MJ. The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO J 2001, 20:4987-4997. 10.1093/emboj/20.17.4987, 125616, 11532962.
12. Nagy E, Maquat LE. A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem Sci 1998, 23:198-199. 10.1016/S0968-0004(98)01208-0, 9644970.
13. Behm-Ansmant I, Gatfield D, Rehwinkel J, Hilgers V, Izaurralde E. A conserved role for cytoplasmic poly(A)-binding protein 1 (PABPC1) in nonsense-mediated mRNA decay. EMBO J 2007, 26:1591-1601. 10.1038/sj.emboj.7601588, 1829367, 17318186.
14. Eberle AB, Stalder L, Mathys H, Orozco RZ, Mühlemann O. Posttranscriptional gene regulation by spatial rearrangement of the 3' untranslated region. PloS Biol 2008, 6:e92. 10.1371/journal.pbio.0060092, 2689704, 18447580.
15. Wang J, Gudikote JP, Olivas OR, Wilkinson MF. Boundary-independent polar nonsense-mediated decay. EMBO Rep 2002, 3:274-279. 10.1093/embo-reports/kvf036, 1084009, 11850396.
16. Bühler M, Steiner S, Mohn F, Paillusson A, Mühlemann O. EJC-independent degradation of nonsense immunoglobulin-mu mRNA depends on 3' UTR length. Nat Struct Mol Biol 2006, 13:462-464. 10.1038/nsmb1081, 16622410.
17. Morrison M, Harris KS, Roth MB. smg mutants affect the expression of alternatively spliced SR protein mRNAs in Caenorhabditis elegans. Proc Natl Acad Sci USA 1997, 94:9782-9785. 10.1073/pnas.94.18.9782, 23268, 9275202.
18. Ni JZ, Grate L, Donohue JP, Preston C, Nobida N, O'Brien G, Shiue L, Clark TA, Blume JE, Ares M. Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay. Genes Dev 2007, 21:708-718. 10.1101/gad.1525507, 1820944, 17369403.
19. Saltzman AL, Kim YK, Pan Q, Fagnani MM, Maquat LE, Blencowe BJ. Regulation of multiple core spliceosomal proteins by alternative splicing-coupled nonsense-mediated mRNA decay. Mol Cell Biol 2008, 28:4320-4330. 10.1128/MCB.00361-08, 2447145, 18443041.
20. Lareau LF, Inada M, Green RE, Wengrod JC, Brenner SE. Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements. Nature 2007, 446:926-929. 10.1038/nature05676, 17361132.
21. Saltzman AL, Pan Q, Blencowe BJ. Regulation of alternative splicing by the core spliceosomal machinery. Genes Dev 2011, 25:373-384. 10.1101/gad.2004811, 3042160, 21325135.
22. Pinol-Roma S, Choi YD, Matunis MJ, Dreyfuss G. Immunopurification of heterogeneous nuclear ribonucleoprotein particles reveals an assortment of RNA-binding proteins. Genes Dev 1988, 2:215-227. 10.1101/gad.2.2.215, 3129338.
23. Han SP, Tang YH, Smith R. Functional diversity of the hnRNPs: past, present and perspectives. Biochem J 2010, 430:379-392. 10.1042/BJ20100396, 20795951.
24. Boutz PL, Stoilov P, Li Q, Lin CH, Chawla G, Ostrow K, Shiue L, Ares M, Black DL. A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons. Genes Dev 2007, 21:1636-1652. 10.1101/gad.1558107, 1899473, 17606642.
25. Hanamura A, Caceres JF, Mayeda A, Franza BR, Krainer AR. Regulated tissue-specific expression of antagonistic pre-mRNA splicing factors. RNA 1998, 4:430-444. 1369629, 9630249.
26. Bai Y, Lee D, Yu T, Chasin LA. Control of 3' splice site choice in vivo by ASF/SF2 and hnRNP A1. Nucleic Acids Res 1999, 27:1126-1134. 10.1093/nar/27.4.1126, 148294, 9927747.
27. Chen M, Manley JL. Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat Rev Mol Cell Biol 2009, 10:741-754. 2958924, 19773805.
28. Pan Q, Saltzman AL, Kim YK, Misquitta C, Shai O, Maquat LE, Frey BJ, Blencowe BJ. Quantitative microarray profiling provides evidence against widespread coupling of alternative splicing with nonsense-mediated mRNA decay to control gene expression. Genes Dev 2006, 20:153-158. 10.1101/gad.1382806, 1356107, 16418482.
29. Ramani AK, Nelson AC, Kapranov P, Bell I, Gingeras TR, Fraser AG. High resolution transcriptome maps for wild-type and nonsense-mediated decay-defective Caenorhabditis elegans. Genome Biol 2009, 10:R101. 10.1186/gb-2009-10-9-r101, 2768976, 19778439.
30. Thoren LA, Nørgaard GA, Weischenfeldt J, Waage J, Jakobsen JS, Damgaard I, Bergström FC, Blom AM, Borup R, Bisgaard HC, Porse BT. UPF2 Is a Critical Regulator of Liver Development, Function and Regeneration. PLoS ONE 2010, 5:e11650. 10.1371/journal.pone.0011650, 2906512, 20657840.
31. Trapnell C, Pachter L, Salzberg S. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-1111. 10.1093/bioinformatics/btp120, 2672628, 19289445.
32. McIlwain DR, Pan Q, Reilly PT, Elia AJ, McCracken S, Wakeham AC, Itie-Youten A, Blencowe BJ, Mak TW. Smg1 is required for embryogenesis and regulates diverse genes via alternative splicing coupled to nonsense-mediated mRNA decay. Proc Natl Acad Sci USA 2010, 107:12186-12191. 10.1073/pnas.1007336107, 2901484, 20566848.
33. Christofk HR, Vander Heiden MG, Harris MH, Ramanathan A, Gerszten RE, Wei R, Fleming MD, Schreiber SL, Cantley LC. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 2008, 452:230-233. 10.1038/nature06734, 18337823.
34. Yeo G, Holste D, Kreiman G, Burge CB. Variation in alternative splicing across human tissues. Genome Biol 2004, 5:R74. 10.1186/gb-2004-5-10-r74, 545594, 15461793.
35. Kim E, Goren A, Ast G. Alternative splicing: current perspectives. Bioessays 2008, 30:38-47. 10.1002/bies.20692, 18081010.
36. Mitrovich QM, Anderson P. mRNA surveillance of expressed pseudogenes in C. elegans. Curr Biol 2005, 15:963-967. 10.1016/j.cub.2005.04.055, 15916954.
37. Mendell JT, Sharifi NA, Meyers JL, Martinez-Murillo F, Dietz HC. Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat Genet 2004, 36:1073-1078. 10.1038/ng1429, 15448691.
38. Sayani S, Janis M, Lee CY, Toesca I, Chanfreau GF. Widespread impact of nonsense-mediated mRNA decay on the yeast intronome. Mol Cell 2008, 31:360-370. 10.1016/j.molcel.2008.07.005, 2600495, 18691968.
39. Langmead B, Trapnell C, Pop M, Salzberg S. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25. 10.1186/gb-2009-10-3-r25, 2690996, 19261174.
40. Hillman RT, Green RE, Brenner SE. An unappreciated role for RNA surveillance. Genome Biol 2004, 5:R8. 10.1186/gb-2004-5-2-r8, 395752, 14759258.
41. Cases S. ACAT-2, A second mammalian Acyl-CoA:cholesterol acyltransferase. Its cloning, expression, and characterization. J Biol Chem 1998, 273:26755-26764. 10.1074/jbc.273.41.26755, 9756919.
42. Simons-Evelyn M, Young HA, Anderson SK. Characterization of the mouse Nktr gene and promoter. Genomics 1997, 40:94-100. 10.1006/geno.1996.4562, 9070924.
43. Weischenfeldt J, Damgaard I, Bryder D, Theilgaard-Mönch K, Thoren LA, Nielsen FC, Jacobsen SE, Nerlov C, Porse BT. NMD is essential for hematopoietic stem and progenitor cells and for eliminating by-products of programmed DNA rearrangements. Genes Dev 2008, 22:1381-1396. 10.1101/gad.468808, 2377192, 18483223.
44. Hogg JR, Goff SP. Upf1 Senses 3'UTR Length to Potentiate mRNA Decay. Cell 2010, 143:379-389. 10.1016/j.cell.2010.10.005, 2981159, 21029861.
45. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 2012, 7:562-578. 10.1038/nprot.2012.016, 22383036.
46. Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 2010, 11:R25. 10.1186/gb-2010-11-3-r25, 2864565, 20196867.
47. RAINMAN (RnAseq-based Isoform detection and NMd ANalysis pipeline). , http://people.binf.ku.dk/jwaage/RAINMAN/