Expression proteomics of UPF1 knockdown in HeLa cells reveals autoregulation of hnRNP A2/B1 mediated by alternative splicing resulting in nonsense-mediated mRNA decay

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  McGlincy, Nicholas J ^a,c   Tan, Lit Yeen ^a   Paul, Nicodeme ^b   Zavolan, Mihaela ^b   Lilley, Kathryn S ^a   Smith, Christopher W J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF BASEL   (Switzerland)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOHEXIMIDE; GREEN FLUORESCENT PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A2; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN B1; MESSENGER RNA; PROTEIN UPF1; REGULATOR PROTEIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; COMPLEMENTARY RNA; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A2 B1; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A2-B1; HNRNP A1; PHOSPHATIDYLINOSITOL 3 KINASE; SMG1 PROTEIN, HUMAN; TH1L PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR; UPF1 PROTEIN, HUMAN; UPF2 PROTEIN, HUMAN;

3' UNTRANSLATED REGION; ALTERNATIVE RNA SPLICING; ARTICLE; AUTOREGULATION; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE SILENCING; HELA CELL; HUMAN; HUMAN CELL; NONSENSE MEDIATED MRNA DECAY; OPEN READING FRAME; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; GENETICS; HOMEOSTASIS; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; PROTEIN SYNTHESIS; PROTEOMICS; REPRODUCIBILITY; RNA STABILITY; STOP CODON; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS;

3' UNTRANSLATED REGIONS; ALTERNATIVE SPLICING; CARRIER PROTEINS; CODON, NONSENSE; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP A-B; HOMEOSTASIS; HUMANS; MASS SPECTROMETRY; OPEN READING FRAMES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN BIOSYNTHESIS; PROTEOMICS; REPRODUCIBILITY OF RESULTS; RNA STABILITY; RNA, ANTISENSE; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TWO-DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS;

EID: 77957823301     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-565     Document Type: Article

References (115)

1. Shyu AB, Wilkinson MF, van Hoof A. Messenger RNA regulation: to translate or to degrade. Embo J 2008, 27(3):471-481. 10.1038/sj.emboj.7601977, 2241649, 18256698.
2. Isken O, Maquat LE. The multiple lives of NMD factors: balancing roles in gene and genome regulation. Nat Rev Genet 2008,
3. Brogna S, Wen J. Nonsense-mediated mRNA decay (NMD) mechanisms. Nat Struct Mol Biol 2009, 16(2):107-113. 10.1038/nsmb.1550, 19190664.
4. Nicholson P, Yepiskoposyan H, Metze S, Zamudio Orozco R, Kleinschmidt N, Muhlemann O. Nonsense-mediated mRNA decay in human cells: mechanistic insights, functions beyond quality control and the double-life of NMD factors. Cell Mol Life Sci 2010, 67(5):677-700. 10.1007/s00018-009-0177-1, 19859661.
5. Culbertson MR, Underbrink KM, Fink GR. Frameshift suppression Saccharomyces cerevisiae. II. Genetic properties of group II suppressors. Genetics 1980, 95(4):833-853. 1214272, 7009318.
6. Hodgkin J, Papp A, Pulak R, Ambros V, Anderson P. A new kind of informational suppression in the nematode Caenorhabditis elegans. Genetics 1989, 123(2):301-313. 1203802, 2583479.
7. Yamashita A, Kashima I, Ohno S. The role of SMG-1 in nonsense-mediated mRNA decay. Biochim Biophys Acta 2005, 1754(1-2):305-315.
8. 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(6):1591-1601. 10.1038/sj.emboj.7601588, 1829367, 17318186.
9. Ivanov PV, Gehring NH, Kunz JB, Hentze MW, Kulozik AE. Interactions between UPF1, eRFs, PABP and the exon junction complex suggest an integrated model for mammalian NMD pathways. Embo J 2008, 27(5):736-747. 10.1038/emboj.2008.17, 2265754, 18256688.
10. Eberle AB, Stalder L, Mathys H, Orozco RZ, Muhlemann O. Posttranscriptional gene regulation by spatial rearrangement of the 3' untranslated region. PLoS Biol 2008, 6(4):e92. 10.1371/journal.pbio.0060092, 2689704, 18447580.
11. Silva AL, Ribeiro P, Inacio A, Liebhaber SA, Romao L. Proximity of the poly(A)-binding protein to a premature termination codon inhibits mammalian nonsense-mediated mRNA decay. Rna 2008, 14(3):563-576. 10.1261/rna.815108, 2248256, 18230761.
12. Singh G, Rebbapragada I, Lykke-Andersen J. A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol 2008, 6(4):e111. 10.1371/journal.pbio.0060111, 2689706, 18447585.
13. Rebbapragada I, Lykke-Andersen J. Execution of nonsense-mediated mRNA decay: what defines a substrate?. Curr Opin Cell Biol 2009, 21(3):394-402. 10.1016/j.ceb.2009.02.007, 19359157.
14. 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(18):9782-9785. 10.1073/pnas.94.18.9782, 23268, 9275202.
15. 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(10):1073-1078. 10.1038/ng1429, 15448691.
16. Neu-Yilik G, Gehring NH, Hentze MW, Kulozik AE. Nonsense-mediated mRNA decay: from vacuum cleaner to Swiss army knife. Genome Biol 2004, 5(4):218. 10.1186/gb-2004-5-4-218, 395777, 15059251.
17. 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(10):1530-1544. 10.1261/rna.2160905, 1370837, 16199763.
18. Guan Q, Zheng W, Tang S, Liu X, Zinkel RA, Tsui KW, Yandell BS, Culbertson MR. Impact of nonsense-mediated mRNA decay on the global expression profile of budding yeast. PLoS Genet 2006, 2(11):e203. 10.1371/journal.pgen.0020203, 1657058, 17166056.
19. Rehwinkel J, Raes J, Izaurralde E. Nonsense-mediated mRNA decay: Target genes and functional diversification of effectors. Trends Biochem Sci 2006, 31(11):639-646. 10.1016/j.tibs.2006.09.005, 17010613.
20. Hansen KD, Lareau LF, Blanchette M, Green RE, Meng Q, Rehwinkel J, Gallusser FL, Izaurralde E, Rio DC, Dudoit S, et al. Genome-wide identification of alternative splice forms down-regulated by nonsense-mediated mRNA decay in Drosophila. PLoS Genet 2009, 5(6):e1000525. 10.1371/journal.pgen.1000525, 2689934, 19543372.
21. 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(9):R101. 10.1186/gb-2009-10-9-r101, 2768976, 19778439.
22. Wittkopp N, Huntzinger E, Weiler C, Sauliere J, Schmidt S, Sonawane M, Izaurralde E. Nonsense-mediated mRNA decay effectors are essential for zebrafish embryonic development and survival. Mol Cell Biol 2009, 29(13):3517-3528. 10.1128/MCB.00177-09, 2698750, 19414594.
23. Medghalchi SM, Frischmeyer PA, Mendell JT, Kelly AG, Lawler AM, Dietz HC. Rent1, a trans-effector of nonsense-mediated mRNA decay, is essential for mammalian embryonic viability. Hum Mol Genet 2001, 10(2):99-105. 10.1093/hmg/10.2.99, 11152657.
24. Mignone F, Gissi C, Liuni S, Pesole G. Untranslated regions of mRNAs. Genome Biol 2002, 3(3):REVIEWS0004. 10.1186/gb-2002-3-3-reviews0004, 139023, 11897027.
25. Soergel DAW, Lareau LF, Brenner SE. Regulation of gene expression by the coupling of alternative splicing and nonsense-mediated mRNA decay. Nonsense-mediated mRNA decay 2006, Landes Bioscience, Maquat LE.
26. Sachs MS, Geballe AP. Downstream control of upstream open reading frames. Genes Dev 2006, 20(8):915-921. 10.1101/gad.1427006, 16618802.
27. Kaygun H, Marzluff WF. Regulated degradation of replication-dependent histone mRNAs requires both ATR and Upf1. Nat Struct Mol Biol 2005, 12(9):794-800. 10.1038/nsmb972, 16086026.
28. Kim YK, Furic L, Desgroseillers L, Maquat LE. Mammalian Staufen1 recruits Upf1 to specific mRNA 3'UTRs so as to elicit mRNA decay. Cell 2005, 120(2):195-208. 10.1016/j.cell.2004.11.050, 15680326.
29. Kim YK, Furic L, Parisien M, Major F, Desgroseillers L, Maquat LE. Staufen1 regulates diverse classes of mammalian transcripts. Embo J 2007, 26(11):2670-2681. 10.1038/sj.emboj.7601712, 1888674, 17510634.
30. 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(2):153-158. 10.1101/gad.1382806, 1356107, 16418482.
31. Wittmann J, Hol EM, Jack HM. hUPF2 silencing identifies physiologic substrates of mammalian nonsense-mediated mRNA decay. Mol Cell Biol 2006, 26(4):1272-1287. 10.1128/MCB.26.4.1272-1287.2006, 1367210, 16449641.
32. 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(6):708-718. 10.1101/gad.1525507, 1820944, 17369403.
33. 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, 2447145, 18443041.
34. Barberan-Soler S, Lambert NJ, Zahler AM. Global analysis of alternative splicing uncovers developmental regulation of nonsense-mediated decay in C. elegans. Rna 2009, 15(9):1652-1660. 10.1261/rna.1711109, 2743056, 19617316.
35. Scadden ADJ, Smith CW. Interactions between the terminal bases of mammalian introns are retained in inosine-containing pre-mRNAs. Embo J 1995, 14(13):3236-3246. 394385, 7621835.
36. Sureau A, Gattoni R, Dooghe Y, Stevenin J, Soret J. SC35 autoregulates its expression by promoting splicing events that destabilize its mRNAs. Embo J 2001, 20(7):1785-1796. 10.1093/emboj/20.7.1785, 145484, 11285241.
37. Gehring NH, Kunz JB, Neu-Yilik G, Breit S, Viegas MH, Hentze MW, Kulozik AE. Exon-junction complex components specify distinct routes of nonsense-mediated mRNA decay with differential cofactor requirements. Mol Cell 2005, 20(1):65-75. 10.1016/j.molcel.2005.08.012, 16209946.
38. Paillusson A, Hirschi N, Vallan C, Azzalin CM, Muhlemann O. A GFP-based reporter system to monitor nonsense-mediated mRNA decay. Nucleic Acids Res 2005, 33(6):e54. 10.1093/nar/gni052, 1072805, 15800205.
39. Boelz S, Neu-Yilik G, Gehring NH, Hentze MW, Kulozik AE. A chemiluminescence-based reporter system to monitor nonsense-mediated mRNA decay. Biochem Biophys Res Commun 2006, 349(1):186-191. 10.1016/j.bbrc.2006.08.017, 16934750.
40. Dreumont N, Maresca A, Boisclair-Lachance JF, Bergeron A, Tanguay RM. A minor alternative transcript of the fumarylacetoacetate hydrolase gene produces a protein despite being likely subjected to nonsense-mediated mRNA decay. BMC Mol Biol 2005, 6(1):1. 10.1186/1471-2199-6-1, 546004, 15638932.
41. Holbrook JA, Neu-Yilik G, Hentze MW, Kulozik AE. Nonsense-mediated decay approaches the clinic. Nat Genet 2004, 36(8):801-808. 10.1038/ng1403, 15284851.
42. Brumbaugh KM, Otterness DM, Geisen C, Oliveira V, Brognard J, Li X, Lejeune F, Tibbetts RS, Maquat LE, Abraham RT. The mRNA surveillance protein hSMG-1 functions in genotoxic stress response pathways in mammalian cells. Mol Cell 2004, 14(5):585-598. 10.1016/j.molcel.2004.05.005, 15175154.
43. Alban A, David SO, Bjorkesten L, Andersson C, Sloge E, Lewis S, Currie I. A novel experimental design for comparative two-dimensional gel analysis: two-dimensional difference gel electrophoresis incorporating a pooled internal standard. Proteomics 2003, 3(1):36-44. 10.1002/pmic.200390006, 12548632.
44. Vanden Bergh G, Arckens L. Fluorescent two-dimensional difference gel electrophoresis unveils the potential of gel-based proteomics. Curr Opin Biotechnol 2004, 15(1):38-43. 10.1016/j.copbio.2003.12.001, 15102464.
45. Pacheco TR, Gomes AQ, Barbosa-Morais NL, Benes V, Ansorge W, Wollerton M, Smith CW, Valcarcel J, Carmo-Fonseca M. Diversity of vertebrate splicing factor U2AF35: identification of alternatively spliced U2AF1 mRNAS. J Biol Chem 2004, 279(26):27039-27049. 10.1074/jbc.M402136200, 15096518.
46. Karp NA, Griffin JL, Lilley KS. Application of partial least squares discriminant analysis to two-dimensional difference gel studies in expression proteomics. Proteomics 2005, 5(1):81-90. 10.1002/pmic.200400881, 15744836.
47. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20(18):3551-3567. 10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2, 10612281.
48. Chang YF, Imam JS, Wilkinson MF. The nonsense-mediated decay RNA surveillance pathway. Annu Rev Biochem 2007, 76:51-74. 10.1146/annurev.biochem.76.050106.093909, 17352659.
49. Karp NA, Lilley KS. Maximising sensitivity for detecting changes in protein expression: experimental design using minimal CyDyes. Proteomics 2005, 5(12):3105-3115. 10.1002/pmic.200500083, 16035117.
50. Lenth RV. Java Applets for Power and Sample Size. 2006,
51. Viegas MH, Gehring NH, Breit S, Hentze MW, Kulozik AE. 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 2007, 1935013, 17586820.
52. Haas BJ, Delcher AL, Mount SM, Wortman JR, Smith RK, Hannick LI, Maiti R, Ronning CM, Rusch DB, Town CD, et al. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res 2003, 31(19):5654-5666. 10.1093/nar/gkg770, 206470, 14500829.
53. Pontius JU, Wagner L, Schuler GD. UniGene: a unified view of the transcriptome. The NCBI Handbook 2003, Bethesda (MD): National Center for Biotechnology Information.
54. van Nimwegen E, Paul N, Sheridan R, Zavolan M. SPA: a probabilistic algorithm for spliced alignment. PLoS Genet 2006, 2(4):e24. 10.1371/journal.pgen.0020024, 1449883, 16683023.
55. 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(7138):926-929. 10.1038/nature05676, 17361132.
56. Kent WJ. BLAT--the BLAST-like alignment tool. Genome Res 2002, 12(4):656-664. 187518, 11932250.
57. Kuersten S, Goodwin EB. The power of the 3' UTR: translational control and development. Nat Rev Genet 2003, 4(8):626-637. 10.1038/nrg1125, 12897774.
58. Wollerton MC, Gooding C, Wagner EJ, Garcia-Blanco MA, Smith CW. Autoregulation of polypyrimidine tract binding protein by alternative splicing leading to nonsense-mediated decay. Mol Cell 2004, 13(1):91-100. 10.1016/S1097-2765(03)00502-1, 14731397.
59. Bejerano G, Pheasant M, Makunin I, Stephen S, Kent WJ, Mattick JS, Haussler D. Ultraconserved elements in the human genome. Science 2004, 304(5675):1321-1325. 10.1126/science.1098119, 15131266.
60. Rossbach O, Hung LH, Schreiner S, Grishina I, Heiner M, Hui J, Bindereif A. Auto- and cross-regulation of the hnRNP L proteins by alternative splicing. Mol Cell Biol 2009, 29(6):1442-1451. 10.1128/MCB.01689-08, 2648227, 19124611.
61. Heintzen C, Nater M, Apel K, Staiger D. AtGRP7, a nuclear RNA-binding protein as a component of a circadian-regulated negative feedback loop in Arabidopsis thaliana. Proc Natl Acad Sci USA 1997, 94(16):8515-8520. 10.1073/pnas.94.16.8515, 22981, 9238008.
62. Lejeune F, Cavaloc Y, Stevenin J. Alternative splicing of intron 3 of the serine/arginine-rich protein 9G8 gene. Identification of flanking exonic splicing enhancers and involvement of 9G8 as a trans-acting factor. J Biol Chem 2001, 276(11):7850-7858. 10.1074/jbc.M009510200, 11096110.
63. Spellman R, Llorian M, Smith CW. Crossregulation and functional redundancy between the splicing regulator PTB and its paralogs nPTB and ROD1. Mol Cell 2007, 27(3):420-434. 10.1016/j.molcel.2007.06.016, 1940037, 17679092.
64. Staiger D, Zecca L, Wieczorek Kirk DA, Apel K, Eckstein L. The circadian clock regulated RNA-binding protein AtGRP7 autoregulates its expression by influencing alternative splicing of its own pre-mRNA. Plant J 2003, 33(2):361-371. 10.1046/j.1365-313X.2003.01629.x, 12535349.
65. Stoilov P, Daoud R, Nayler O, Stamm S. Human tra2-beta1 autoregulates its protein concentration by influencing alternative splicing of its pre-mRNA. Hum Mol Genet 2004, 13(5):509-524. 10.1093/hmg/ddh051, 14709600.
66. Sun S, Zhang Z, Sinha R, Karni R, Krainer AR. SF2/ASF autoregulation involves multiple layers of post-transcriptional and translational control. Nat Struct Mol Biol 2010, 2921916, 20139984.
67. Green RE, Lewis BP, Hillman RT, Blanchette M, Lareau LF, Garnett AT, Rio DC, Brenner SE. Widespread predicted nonsense-mediated mRNA decay of alternatively-spliced transcripts of human normal and disease genes. Bioinformatics 2003, 19(1):i118-121. 10.1093/bioinformatics/btg1015, 12855447.
68. Hillman RT, Green RE, Brenner SE. An unappreciated role for RNA surveillance. Genome Biol 2004, 5(2):R8. 10.1186/gb-2004-5-2-r8, 395752, 14759258.
69. Chan WK, Huang L, Gudikote JP, Chang YF, Imam JS, MacLean JA, Wilkinson MF. An alternative branch of the nonsense-mediated decay pathway. Embo J 2007, 26(7):1820-1830. 10.1038/sj.emboj.7601628, 1847659, 17363904.
70. Donnadieu E, Jouvin MH, Rana S, Moffatt MF, Mockford EH, Cookson WO, Kinet JP. Competing functions encoded in the allergy-associated F(c)epsilonRIbeta gene. Immunity 2003, 18(5):665-674. 10.1016/S1074-7613(03)00115-8, 12753743.
71. Kumar S, Lopez AJ. Negative feedback regulation among SR splicing factors encoded by Rbp1 and Rbp1-like in Drosophila. Embo J 2005, 24(14):2646-2655. 10.1038/sj.emboj.7600723, 1176452, 15961996.
72. Lee HC, Oh N, Cho H, Choe J, Kim YK. Nonsense-mediated translational repression involves exon junction complex downstream of premature translation termination codon. FEBS Lett 2010, 584(4):795-800. 10.1016/j.febslet.2010.01.003, 20067791.
73. You KT, Li LS, Kim NG, Kang HJ, Koh KH, Chwae YJ, Kim KM, Kim YK, Park SM, Jang SK, et al. Selective translational repression of truncated proteins from frameshift mutation-derived mRNAs in tumors. PLoS Biol 2007, 5(5):e109. 10.1371/journal.pbio.0050109, 1854916, 17456004.
74. Barnes CA. Upf1 and Upf2 proteins mediate normal yeast mRNA degradation when translation initiation is limited. Nucleic Acids Res 1998, 26(10):2433-2441. 10.1093/nar/26.10.2433, 147546, 9580697.
75. Heikkinen HL, Llewellyn SA, Barnes CA. Initiation-mediated mRNA decay in yeast affects heat-shock mRNAs, and works through decapping and 5'-to-3' hydrolysis. Nucleic Acids Res 2003, 31(14):4006-4016. 10.1093/nar/gkg474, 167635, 12853617.
76. Popielarz M, Cavaloc Y, Mattei MG, Gattoni R, Stevenin J. The gene encoding human splicing factor 9G8. Structure, chromosomal localization, and expression of alternatively processed transcripts. J Biol Chem 1995, 270(30):17830-17835. 10.1074/jbc.270.30.17830, 7629084.
77. Stockklausner C, Breit S, Neu-Yilik G, Echner N, Hentze MW, Kulozik AE, Gehring NH. The uORF-containing thrombopoietin mRNA escapes nonsense-mediated decay (NMD). Nucleic Acids Res 2006, 34(8):2355-2363. 10.1093/nar/gkl277, 1458284, 16679454.
78. Silva AL, Pereira FJ, Morgado A, Kong J, Martins R, Faustino P, Liebhaber SA, Romao L. The canonical UPF1-dependent nonsense-mediated mRNA decay is inhibited in transcripts carrying a short open reading frame independent of sequence context. Rna 2006, 12(12):2160-2170. 10.1261/rna.201406, 1664719, 17077274.
79. Zhang J, Maquat LE. Evidence that translation reinitiation abrogates nonsense-mediated mRNA decay in mammalian cells. Embo J 1997, 16(4):826-833. 10.1093/emboj/16.4.826, 1169683, 9049311.
80. Poyry TA, Kaminski A, Jackson RJ. What determines whether mammalian ribosomes resume scanning after translation of a short upstream open reading frame?. Genes Dev 2004, 18(1):62-75. 10.1101/gad.276504, 314277, 14701882.
81. Roy B, Vaughn JN, Kim BH, Zhou F, Gilchrist MA, Von Arnim AG. The h subunit of eIF3 promotes reinitiation competence during translation of mRNAs harboring upstream open reading frames. Rna 2010, 16(4):748-761. 10.1261/rna.2056010, 2844622, 20179149.
82. Calvo SE, Pagliarini DJ, Mootha VK. Upstream open reading frames cause widespread reduction of protein expression and are polymorphic among humans. Proc Natl Acad Sci USA 2009, 106(18):7507-7512. 10.1073/pnas.0810916106, 2669787, 19372376.
83. Morris DR, Geballe AP. Upstream open reading frames as regulators of mRNA translation. Mol Cell Biol 2000, 20(23):8635-8642. 10.1128/MCB.20.23.8635-8642.2000, 86464, 11073965.
84. Ruiz-Echevarria MJ, Peltz SW. The RNA binding protein Pub1 modulates the stability of transcripts containing upstream open reading frames. Cell 2000, 101(7):741-751. 10.1016/S0092-8674(00)80886-7, 10892745.
85. Krecic AM, Swanson MS. hnRNP complexes: composition, structure, and function. Curr Opin Cell Biol 1999, 11(3):363-371. 10.1016/S0955-0674(99)80051-9, 10395553.
86. Matlin AJ, Clark F, Smith CW. Understanding alternative splicing: towards a cellular code. Nat Rev Mol Cell Biol 2005, 6(5):386-398. 10.1038/nrm1645, 15956978.
87. Martinez-Contreras R, Fisette J-F, ois Nasim F, Madden R, Cordeau M, lanie Chabot B. Intronic Binding Sites for hnRNP A/B and hnRNP F/H Proteins Stimulate Pre-mRNA Splicing. PLoS Biology 2006, 4(2):e21. 10.1371/journal.pbio.0040021, 1326234, 16396608.
88. Fahling M, Mrowka R, Steege A, Martinka P, Persson PB, Thiele BJ. Heterogeneous nuclear ribonucleoprotein-A2/B1 modulate collagen prolyl 4-hydroxylase, alpha (I) mRNA stability. J Biol Chem 2006, 281(14):9279-9286. 10.1074/jbc.M510925200, 16464861.
89. Black DL. Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 2003, 72:291-336. 10.1146/annurev.biochem.72.121801.161720, 12626338.
90. Goina E, Skoko N, Pagani F. Binding of DAZAP1 and hnRNPA1/A2 to an exonic splicing silencer in a natural BRCA1 exon 18 mutant. Mol Cell Biol 2008, 28(11):3850-3860. 10.1128/MCB.02253-07, 2423284, 18391021.
91. Venables JP, Koh CS, Froehlich U, Lapointe E, Couture S, Inkel L, Bramard A, Paquet ER, Watier V, Durand M, et al. Multiple and specific mRNA processing targets for the major human hnRNP proteins. Mol Cell Biol 2008, 28(19):6033-6043. 10.1128/MCB.00726-08, 2547008, 18644864.
92. Fisette JF, Toutant J, Dugre-Brisson S, Desgroseillers L, Chabot B. hnRNP A1 and hnRNP H can collaborate to modulate 5' splice site selection. Rna 2010, 16(1):228-238. 10.1261/rna.1890310, 2802032, 19926721.
93. Patry C, Bouchard L, Labrecque P, Gendron D, Lemieux B, Toutant J, Lapointe E, Wellinger R, Chabot B. Small interfering RNA-mediated reduction in heterogeneous nuclear ribonucleoparticule A1/A2 proteins induces apoptosis in human cancer cells but not in normal mortal cell lines. Cancer Res 2003, 63(22):7679-7688.
94. 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(13):1636-1652. 10.1101/gad.1558107, 1899473, 17606642.
95. Makeyev EV, Zhang J, Carrasco MA, Maniatis T. The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell 2007, 27(3):435-448. 10.1016/j.molcel.2007.07.015, 17679093.
96. McGlincy NJ, Smith CW. Alternative splicing resulting in nonsense-mediated mRNA decay: what is the meaning of nonsense?. Trends Biochem Sci 2008,
97. Yan-Sanders Y, Hammons GJ, Lyn-Cook BD. Increased expression of heterogeneous nuclear ribonucleoprotein A2/B1 (hnRNP) in pancreatic tissue from smokers and pancreatic tumor cells. Cancer Lett 2002, 183(2):215-220. 10.1016/S0304-3835(02)00168-4, 12065097.
98. Zhou J, Allred DC, Avis I, Martinez A, Vos MD, Smith L, Treston AM, Mulshine JL. Differential expression of the early lung cancer detection marker, heterogeneous nuclear ribonucleoprotein-A2/B1 (hnRNP-A2/B1) in normal breast and neoplastic breast cancer. Breast Cancer Res Treat 2001, 66(3):217-224. 10.1023/A:1010631915831, 11510693.
99. Kim SH, Dierssen M, Ferreres JC, Fountoulakis M, Lubec G. Increased protein levels of heterogeneous nuclear ribonucleoprotein A2/B1 in fetal Down syndrome brains. J Neural Transm Suppl 2001, (61):273-280.
100. Clower CV, Chatterjee D, Wang Z, Cantley LC, Vander Heiden MG, Krainer AR. The alternative splicing repressors hnRNP A1/A2 and PTB influence pyruvate kinase isoform expression and cell metabolism. Proc Natl Acad Sci USA 2010, 107(5):1894-1899. 10.1073/pnas.0914845107, 2838216, 20133837.
101. David CJ, Chen M, Assanah M, Canoll P, Manley JL. HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer. Nature 2010, 463(7279):364-368. 10.1038/nature08697, 2950088, 20010808.
102. Moran-Jones K, Grindlay J, Jones M, Smith R, Norman JC. hnRNP A2 regulates alternative mRNA splicing of TP53INP2 to control invasive cell migration. Cancer Res 2009, 69(24):9219-9227. 10.1158/0008-5472.CAN-09-1852, 19934309.
103. Gromak N, Rideau A, Southby J, Scadden AD, Gooding C, Huttelmaier S, Singer RH, Smith CW. The PTB interacting protein raver1 regulates alpha-tropomyosin alternative splicing. Embo J 2003, 22(23):6356-6364. 10.1093/emboj/cdg609, 291850, 14633994.
104. Wagner EJ, Garcia-Blanco MA. RNAi-mediated PTB depletion leads to enhanced exon definition. Mol Cell 2002, 10(4):943-949. 10.1016/S1097-2765(02)00645-7, 12419237.
105. Mendell JT, ap Rhys CM, Dietz HC. Separable roles for rent1/hUpf1 in altered splicing and decay of nonsense transcripts. Science 2002, 298(5592):419-422. 10.1126/science.1074428, 12228722.
106. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254. 10.1016/0003-2697(76)90527-3, 942051.
107. Tichopad A, Dilger M, Schwarz G, Pfaffl MW. Standardized determination of real-time PCR efficiency from a single reaction set-up. Nucleic Acids Res 2003, 31(20):e122. 10.1093/nar/gng122, 219490, 14530455.
108. Wang X, Seed B. A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res 2003, 31(24):e154. 10.1093/nar/gng154, 291882, 14654707.
109. Rozen S, Skaletsky HJ. Primer3 on the WWW for general users and for biologist programmers. Bioinformatics Methods and Protocols: Methods in Molecular Biology 2000, 365-386. Totowa, NJ: Humana Press, Krawetz S, Misener S.
110. Ririe KM, Rasmussen RP, Wittwer CT. Product differentiation by analysis of DNA melting curves during the polymerase chain reaction. Anal Biochem 1997, 245(2):154-160. 10.1006/abio.1996.9916, 9056205.
111. Karp NA, Kreil DP, Lilley KS. Determining a significant change in protein expression with DeCyder during a pair-wise comparison using two-dimensional difference gel electrophoresis. Proteomics 2004, 4(5):1421-1432. 10.1002/pmic.200300681, 15188411.
112. Zavolan M, Kondo S, Schonbach C, Adachi J, Hume DA, Hayashizaki Y, Gaasterland T. Impact of alternative initiation, splicing, and termination on the diversity of the mRNA transcripts encoded by the mouse transcriptome. Genome Res 2003, 13(6B):1290-1300. 10.1101/gr.1017303, 403716, 12819126.
113. Zavolan M, van Nimwegen E, Gaasterland T. Splice variation in mouse full-length cDNAs identified by mapping to the mouse genome. Genome Res 2002, 12(9):1377-1385. 10.1101/gr.191702, 186662, 12213775.
114. Karolchik D, Baertsch R, Diekhans M, Furey TS, Hinrichs A, Lu YT, Roskin KM, Schwartz M, Sugnet CW, Thomas DJ, et al. The UCSC Genome Browser Database. Nucleic Acids Res 2003, 31(1):51-54. 10.1093/nar/gkg129, 165576, 12519945.
115. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, Clawson H, Spieth J, Hillier LW, Richards S, et al. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 2005, 15(8):1034-1050. 10.1101/gr.3715005, 1182216, 16024819.