Regulation of nonsense-mediated mRNA decay

Wiley Interdisciplinary Reviews: RNA

Volumn 3, Issue 6, 2012, Pages 807-828

  Huang, Lulu ^a   Wilkinson, Miles F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DHX34 PROTEIN; EIF4A3 PROTEIN; MAGOH PROTEIN; MEMBRANE PROTEIN; MESSENGER RNA; MICRORNA; MLN51 PROTEIN; NAG PROTEIN; PHOSPHOPROTEIN; PYM PROTEIN; RNA BINDING PROTEIN; RNPS1 PROTEIN; SMG1 PROTEIN; SMG5 PROTEIN; SMG6 PROTEIN; SMG7 PROTEIN; SMG8 PROTEIN; SMG9 PROTEIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; TRANSMEMBRANE CONDUCTANCE REGULATOR; UNCLASSIFIED DRUG; UPF1 PROTEIN; UPF2 PROTEIN; UPF3A PROTEIN; UPF3B PROTEIN; Y14 PROTEIN;

B LYMPHOCYTE; CAENORHABDITIS ELEGANS; CELL STRAIN MCF 7; CELL TYPE; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR MOUSE; DROSOPHILA; EMBRYO DEVELOPMENT; FEEDBACK SYSTEM; GENE EXPRESSION; GENE MUTATION; GENETIC ASSOCIATION; HELA CELL; MUSCLE DEVELOPMENT; NERVE CELL DIFFERENTIATION; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STABILITY; REGULATORY MECHANISM; REVIEW; STOP CODON; TISSUES; VERTEBRATE;

ANIMALS; FEEDBACK, PHYSIOLOGICAL; HUMANS; NONSENSE MEDIATED MRNA DECAY; ORGAN SPECIFICITY; TRANSCRIPTION, GENETIC;

EID: 84867592374     PISSN: 17577004     EISSN: 17577012     Source Type: Journal    
DOI: 10.1002/wrna.1137     Document Type: Review

References (152)

1. Bhuvanagiri M, Schlitter AM, Hentze MW, Kulozik AE. NMD: RNA biology meets human genetic medicine. Biochem J 2010, 430:365-377.
2. Nicholson P, Muhlemann O. Cutting the nonsense: the degradation of PTC-containing mRNAs. Biochem Soc Trans 2010, 38:1615-1620.
3. Lelivelt MJ, Culbertson MR. Yeast Upf proteins required for RNA surveillance affect global expression of the yeast transcriptome. Mol Cell Biol 1999, 19: 6710-6719.
4. He F, Li X, Spatrick P, Casillo R, Dong S, Jacobson A. Genome-wide analysis of mRNAs regulated by the nonsense-mediated and 5' to 3' mRNA decay pathways in yeast. Mol Cell 2003, 12:1439-1452.
5. 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:e203.
6. 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.
7. 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.
8. 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.
9. Wittmann J, Hol EM, Jack HM. hUPF2 silencing identifies physiologic substrates of mammalian nonsense-mediated mRNA decay. Mol Cell Biol 2006, 26: 1272-1287.
10. Chan WK, Huang L, Gudikote JP, Chang YF, Imam JS, MacLean JA, 2nd, Wilkinson MF. An alternative branch of the nonsense-mediated decay pathway. EMBO J 2007, 26:1820-1830.
11. Yoine M, Ohto MA, Onai K, Mita S, Nakamura K. The lba1 mutation of UPF1 RNA helicase involved in nonsense-mediated mRNA decay causes pleiotropic phenotypic changes and altered sugar signalling in Arabidopsis. Plant J 2006, 47:49-62.
12. Hori K, Watanabe Y. UPF3 suppresses aberrant spliced mRNA in Arabidopsis. Plant J 2005, 43: 530-540.
13. Oliveira CC, McCarthy JE. The relationship between eukaryotic translation and mRNA stability. A short upstream open reading frame strongly inhibits translational initiation and greatly accelerates mRNA degradation in the yeast Saccharomyces cerevisiae. J Biol Chem 1995, 270:8936-8943.
14. Maquat LE. Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nat Rev Mol Cell Biol 2004, 5:89-99.
15. 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.
16. Ni JZ, Grate L, Donohue JP, Preston C, Nobida N, O'Brien G, Shiue L, Clark TA, Blume JE, Ares M, Jr. Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay. Genes Dev 2007, 21:708-718.
17. 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.
18. Buhler M, Steiner S, Mohn F, Paillusson A, Muhlemann O. EJC-independent degradation of nonsense immunoglobulin-mu mRNA depends on 3' UTR length. Nat Struct Mol Biol 2006, 13:462-464.
19. 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:e111.
20. McGlincy NJ, Smith CW. Alternative splicing resulting in nonsense-mediated mRNA decay: what is the meaning of nonsense? Trends Biochem Sci 2008, 33: 385-393.
21. Muhlemann O. Recognition of nonsense mRNA: towards a unified model. Biochem Soc Trans 2008, 36: 497-501.
22. Gudikote JP, Imam JS, Garcia RF, Wilkinson MF. RNA splicing promotes translation and RNA surveillance. Nat Struct Mol Biol 2005, 12:801-809.
23. Li S, Wilkinson MF. Nonsense surveillance in lymphocytes? Immunity 1998, 8:135-141.
24. Gudikote JP, Wilkinson MF. NMD and the immune system. Nonsense-mediated mRNA Decay Landes Biosciences Press, Edited by Maquat LE 2006, 71-83.
25. Connor A, Wiersma E, Shulman MJ. On the linkage between RNA processing and RNA translatability. J Biol Chem 1994, 269:25178-25184.
26. Carter MS, Li S, Wilkinson MF. A splicing-dependent regulatory mechanism that detects translation signals. EMBO J 1996, 15:5965-5975.
27. Bateman JF, Freddi S, Nattrass G, Savarirayan R. Tissue-specific RNA surveillance? Nonsense-mediated mRNA decay causes collagen X haploinsufficiency in Schmid metaphyseal chondrodysplasia cartilage. Hum Mol Genet 2003, 12:217-225.
28. Tan JT, Kremer F, Freddi S, Bell KM, Baker NL, Lamande SR, Bateman JF. Competency for nonsense-mediated reduction in collagen X mRNA is specified by the 3' UTR and corresponds to the position of mutations in Schmid metaphyseal chondrodysplasia. Am J Hum Genet 2008, 82:786-793.
29. Resta N, Susca FC, Di Giacomo MC, Stella A, Bukvic N, Bagnulo R, Simone C, Guanti G. A homozygous frameshift mutation in the ESCO2 gene: evidence of intertissue and interindividual variation in Nmd efficiency. J Cell Physiol 2006, 209:67-73.
30. Clerici M, Mourao A, Gutsche I, Gehring NH, Hentze MW, Kulozik A, Kadlec J, Sattler M, Cusack S. Unusual bipartite mode of interaction between the nonsense-mediated decay factors, UPF1 and UPF2. EMBO J 2009, 28:2293-2306.
31. Takahashi S, Araki Y, Ohya Y, Sakuno T, Hoshino S, Kontani K, Nishina H, Katada T. Upf1 potentially serves as a RING-related E3 ubiquitin ligase via its association with Upf3 in yeast. RNA 2008, 14: 1950-1958.
32. 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, 27:736-747.
33. Isken O, Kim YK, Hosoda N, Mayeur GL, Hershey JW, Maquat LE. Upf1 phosphorylation triggers translational repression during nonsense-mediated mRNA decay. Cell 2008, 133:314-327.
34. Applequist SE, Selg M, Raman C, Jack HM. Cloning and characterization of HUPF1, a human homolog of the Saccharomyces cerevisiae nonsense mRNA-reducing UPF1 protein. Nucleic Acids Res 1997, 25: 814-821.
35. Bhattacharya A, Czaplinski K, Trifillis P, He F, Jacobson A, Peltz SW. Characterization of the biochemical properties of the human Upf1 gene product that is involved in nonsense-mediated mRNA decay. RNA 2000, 6:1226-1235.
36. 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.
37. Mendell JT, ap Rhys CM, Dietz HC. Separable roles for rent1/hUpf1 in altered splicing and decay of nonsense transcripts. Science 2002, 298:419-422.
38. Sun X, Perlick HA, Dietz HC, Maquat LE. 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 U S A 1998, 95:10009-10014.
39. Yamashita A, Ohnishi T, Kashima I, Taya Y, 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 2001, 15:2215-2228.
40. Wilkinson MF. The cycle of nonsense. Mol Cell 2003, 12:1059-1061.
41. Carastro LM, Tan CK, Selg M, Jack HM, So AG, Downey KM. Identification of delta helicase as the bovine homolog of HUPF1: demonstration of an interaction with the third subunit of DNA polymerase delta. Nucleic Acids Res 2002, 30:2232-2243.
42. Azzalin CM, Lingner J. The human RNA surveillance factor UPF1 is required for S phase progression and genome stability. Curr Biol 2006, 16:433-439.
43. 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, 120:195-208.
44. Sittman DB, Graves RA, Marzluff WF. Histone mRNA concentrations are regulated at the level of transcription and mRNA degradation. Proc Natl Acad Sci U S A 1983, 80:1849-1853.
45. Kaygun H, Marzluff WF. Regulated degradation of replication-dependent histone mRNAs requires both ATR and Upf1. Nat Struct Mol Biol 2005, 12: 794-800.
46. Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 2007, 318:798-801.
47. Chamieh H, Ballut L, Bonneau F, Le Hir H. NMD factors UPF2 and UPF3 bridge UPF1 to the exon junction complex and stimulate its RNA helicase activity. Nat Struct Mol Biol 2008, 15:85-93.
48. Johns L, Grimson A, Kuchma SL, Newman CL, Anderson P. Caenorhabditis elegans SMG-2 selectively marks mRNAs containing premature translation termination codons. Mol Cell Biol 2007, 27:5630-5638.
49. Wang W, Cajigas IJ, Peltz SW, Wilkinson MF, Gonzalez CI. Role for Upf2p phosphorylation in Saccharomyces cerevisiae nonsense-mediated mRNA decay. Mol Cell Biol 2006, 26:3390-3400.
50. Kadlec J, Guilligay D, Ravelli RB, Cusack S. Crystal structure of the UPF2-interacting domain of nonsense-mediated mRNA decay factor UPF1. RNA 2006, 12:1817-1824.
51. 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, 20:65-75.
52. Ohnishi T, Yamashita A, Kashima I, Schell T, Anders KR, Grimson A, Hachiya T, Hentze MW, Anderson P, Ohno S. Phosphorylation of hUPF1 induces formation of mRNA surveillance complexes containing hSMG-5 and hSMG-7. Mol Cell 2003, 12:1187-1200.
53. Page MF, Carr B, Anders KR, Grimson A, Anderson P. SMG-2 is a phosphorylated protein required for mRNA surveillance in Caenorhabditis elegans and related to Upf1p of yeast. Mol Cell Biol 1999, 19:5943-5951.
54. Serin G, Gersappe A, Black JD, Aronoff R, Maquat LE. Identification and characterization of human orthologues to Saccharomyces cerevisiae Upf2 protein and Upf3 protein (Caenorhabditis elegans SMG-4). Mol Cell Biol 2001, 21:209-223.
55. Mendell JT, Medghalchi SM, Lake RG, Noensie EN, Dietz HC. Novel Upf2p orthologues suggest a functional link between translation initiation and nonsense surveillance complexes. Mol Cell Biol 2000, 20:8944-8957.
56. Wang J, Vock VM, Li S, Olivas OR, Wilkinson MF. A quality control pathway that down-regulates aberrant T-cell receptor (TCR) transcripts by a mechanism requiring UPF2 and translation. J Biol Chem 2002, 277:18489-18493.
57. Kunz JB, Neu-Yilik G, Hentze MW, Kulozik AE, Gehring NH. Functions of hUpf3a and hUpf3b in nonsense-mediated mRNA decay and translation. RNA 2006, 12:1015-1022.
58. Schell T, Kocher T, Wilm M, Seraphin B, Kulozik AE, Hentze MW. Complexes between the nonsense-mediated mRNA decay pathway factor human upf1 (up-frameshift protein 1) and essential nonsense-mediated mRNA decay factors in HeLa cells. Biochem J 2003, 373:775-783.
59. Lykke-Andersen J. Identification of a human decapping complex associated with hUpf proteins in nonsense-mediated decay. Mol Cell Biol 2002, 22:8114-8121.
60. Buchwald G, Ebert J, Basquin C, Sauliere J, Jayachandran U, Bono F, Le Hir H, Conti E. Insights into the recruitment of the NMD machinery from the crystal structure of a core EJC-UPF3b complex. Proc Natl Acad Sci U S A 2010, 107:10050-10055.
61. Chan WK, Bhalla AD, Le Hir H, Nguyen LS, Huang L, Gecz J, Wilkinson MF. A UPF3-mediated regulatory switch that maintains RNA surveillance. Nat Struct Mol Biol 2009, 16:747-753.
62. Kim VN, Kataoka N, Dreyfuss G. Role of the nonsense-mediated decay factor hUpf3 in the splicing-dependent exon-exon junction complex. Science 2001, 293:1832-1836.
63. Denning G, Jamieson L, Maquat LE, Thompson EA, Fields AP. Cloning of a novel phosphatidylinositol kinase-related kinase: characterization of the human SMG-1 RNA surveillance protein. J Biol Chem 2001, 276:22709-22714.
64. Kashima I, Jonas S, Jayachandran U, Buchwald G, Conti E, Lupas AN, Izaurralde E. SMG6 interacts with the exon junction complex via two conserved EJC-binding motifs (EBMs) required for nonsense-mediated mRNA decay. Genes Dev 2010, 24:2440-2450.
65. Grimson A, O'Connor S, Newman CL, Anderson P. SMG-1 is a phosphatidylinositol kinase-related protein kinase required for nonsense-mediated mRNA decay in Caenorhabditis elegans. Mol Cell Biol 2004, 24:7483-7490.
66. Yamashita A, Kashima I, Ohno S. The role of SMG-1 in nonsense-mediated mRNA decay. Biochim Biophys Acta 2005, 1754:305-315.
67. 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, 14:585-598.
68. Gehen SC, Staversky RJ, Bambara RA, Keng PC, O'Reilly MA. hSMG-1 and ATM sequentially and independently regulate the G1 checkpoint during oxidative stress. Oncogene 2008, 27:4065-4074.
69. Oliveira V, Romanow WJ, Geisen C, Otterness DM, Mercurio F, Wang HG, Dalton WS, Abraham RT. A protective role for the human SMG-1 kinase against tumor necrosis factor-alpha-induced apoptosis. J Biol Chem 2008, 283:13174-13184.
70. Anders KR, Grimson A, Anderson P. SMG-5, required for C. elegans nonsense-mediated mRNA decay, associates with SMG-2 and protein phosphatase 2A. EMBO J 2003, 22:641-650.
71. Glavan F, Behm-Ansmant I, Izaurralde E, Conti E. Structures of the PIN domains of SMG6 and SMG5 reveal a nuclease within the mRNA surveillance complex. EMBO J 2006, 25:5117-5125.
72. Eberle AB, Lykke-Andersen S, Muhlemann O, Jensen TH. SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat Struct Mol Biol 2009, 16:49-55.
73. Fukuhara N, Ebert J, Unterholzner L, Lindner D, Izaurralde E, Conti E. SMG7 is a 14-3-3-like adaptor in the nonsense-mediated mRNA decay pathway. Mol Cell 2005, 17:537-547.
74. Unterholzner L, Izaurralde E. SMG7 acts as a molecular link between mRNA surveillance and mRNA decay. Mol Cell 2004, 16:587-596.
75. Cali BM, Kuchma SL, Latham J, Anderson P. smg-7 is required for mRNA surveillance in Caenorhabditis elegans. Genetics 1999, 151:605-616.
76. Yamashita A, Izumi N, Kashima I, Ohnishi T, Saari B, Katsuhata Y, Muramatsu R, Morita T, Iwamatsu A, Hachiya T, et al. SMG-8 and SMG-9, two novel subunits of the SMG-1 complex, regulate remodeling of the mRNA surveillance complex during nonsense-mediated mRNA decay. Genes Dev 2009, 23: 1091-1105.
77. Arias-Palomo E, Yamashita A, Fernandez IS, Nunez-Ramirez R, Bamba Y, Izumi N, Ohno S, Llorca O. The nonsense-mediated mRNA decay SMG-1 kinase is regulated by large-scale conformational changes controlled by SMG-8. Genes Dev 2011, 25:153-164.
78. Fernandez IS, Yamashita A, Arias-Palomo E, Bamba Y, Bartolome RA, Canales MA, Teixido J, Ohno S, Llorca O. Characterization of SMG-9, an essential component of the nonsense-mediated mRNA decay SMG1C complex. Nucleic Acids Res 2010, 39: 347-358.
79. Anastasaki C, Longman D, Capper A, Patton EE, Caceres JF. Dhx34 and Nbas function in the NMD pathway and are required for embryonic development in zebrafish. Nucleic Acids Res 2011, 39:3686-3694.
80. Shibuya T, Tange TO, Sonenberg N, Moore MJ. eIF4AIII binds spliced mRNA in the exon junction complex and is essential for nonsense-mediated decay. Nat Struct Mol Biol 2004, 11:346-351.
81. Shibuya T, Tange TO, Stroupe ME, Moore MJ. Mutational analysis of human eIF4AIII identifies regions necessary for exon junction complex formation and nonsense-mediated mRNA decay. RNA 2006, 12: 360-374.
82. Nott A, Le Hir H, Moore MJ. Splicing enhances translation in mammalian cells: an additional function of the exon junction complex. Genes Dev 2004, 18: 210-222.
83. Gehring NH, Lamprinaki S, Hentze MW, Kulozik AE. The hierarchy of exon-junction complex assembly by the spliceosome explains key features of mammalian nonsense-mediated mRNA decay. PLoS Biol 2009, 7:e1000120.
84. Gehring NH, Neu-Yilik G, Schell T, Hentze MW, Kulozik AE. Y14 and hUpf3b form an NMD-activating complex. Mol Cell 2003, 11:939-949.
85. 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.
86. Fribourg S, Gatfield D, Izaurralde E, Conti E. A novel mode of RBD-protein recognition in the Y14-Mago complex. Nat Struct Biol 2003, 10:433-439.
87. Lau CK, Diem MD, Dreyfuss G, Van Duyne GD. Structure of the Y14-Magoh core of the exon junction complex. Curr Biol 2003, 13:933-941.
88. 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, 35: 4542-4551.
89. Bono F, Ebert J, Unterholzner L, Guttler T, Izaurralde E, Conti E. Molecular insights into the interaction of PYM with the Mago-Y14 core of the exon junction complex. EMBO Rep 2004, 5:304-310.
90. Gehring NH, Lamprinaki S, Kulozik AE, Hentze MW. Disassembly of exon junction complexes by PYM. Cell 2009, 137:536-548.
91. Linde L, Boelz S, Neu-Yilik G, Kulozik AE, Kerem B. The efficiency of nonsense-mediated mRNA decay is an inherent character and varies among different cells. Eur J Hum Genet 2007, 15:1156-1162.
92. Usuki F, Yamashita A, Kashima I, Higuchi I, Osame M, Ohno S. Specific inhibition of nonsense-mediated mRNA decay components, SMG-1 or Upf1, rescues the phenotype of Ullrich disease fibroblasts. Mol Ther 2006, 14:351-360.
93. Frischmeyer-Guerrerio PA, Montgomery RA, Warren DS, Cooke SK, Lutz J, Sonnenday CJ, Guerrerio AL, Dietz HC. Perturbation of thymocyte development in nonsense-mediated decay (NMD)-deficient mice. Proc Natl Acad Sci U S A 2011, 108:10638-10643.
94. Zetoune AB, Fontaniere S, Magnin D, Anczukow O, Buisson M, Zhang CX, Mazoyer S. Comparison of nonsense-mediated mRNA decay efficiency in various murine tissues. BMC Genet 2008, 9:83.
95. Huang L, Lou CH, Chan W, Shum EY, Shao A, Stone E, Karam R, Song HW, Wilkinson MF. RNA homeostasis governed by cell type-specific and branched feedback loops acting on NMD. Mol Cell 2011, 43:950-961.
96. Kebaara B, Nazarenus T, Taylor R, Atkin AL. Genetic background affects relative nonsense mRNA accumulation in wild-type and upf mutant yeast strains. Curr Genet 2003, 43:171-177.
97. Linde L, Boelz S, Nissim-Rafinia M, Oren YS, Wilschanski M, Yaacov Y, Virgilis D, Neu-Yilik G, Kulozik AE, Kerem E, Kerem B. Nonsense-mediated mRNA decay affects nonsense transcript levels and governs response of cystic fibrosis patients to gentamicin. J Clin Invest 2007, 117:683-692.
98. Cheng J, Belgrader P, Zhou X, Maquat LE. Introns are cis effectors of the nonsense-codon-mediated reduction in nuclear mRNA abundance. Mol Cell Biol 1994, 14:6317-6325.
99. Li S, Leonard D, Wilkinson MF. T cell receptor (TCR) mini-gene mRNA expression regulated by nonsense codons: a nuclear-associated translation-like mechanism. J Exp Med 1997, 185:985-992.
100. Gardner LB. Hypoxic inhibition of nonsense-mediated RNA decay regulates gene expression and the integrated stress response. Mol Cell Biol 2008, 28: 3729-3741.
101. 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, 10:99-105.
102. Weischenfeldt J, Damgaard I, Bryder D, Theilgaard-Monch 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.
103. 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 U S A 2010, 107:12186-12191.
104. Thoren LA, Norgaard GA, Weischenfeldt J, Waage J, Jakobsen JS, Damgaard I, Bergstrom 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.
105. Anderson P. NMD in Caenorhabditis elegans. Nonsense-mediated mRNA Decay Landes Biosciences Press, Edited by Maquat LE 2006, 139-150.
106. Pulak R, Anderson P. mRNA surveillance by the Caenorhabditis elegans smg genes. Genes Dev 1993, 7: 1885-1897.
107. Hodgkin J, Papp A, Pulak R, Ambros V, Anderson P. A new kind of informational suppression in the nematode Caenorhabditis elegans. Genetics 1989, 123:301-313.
108. Domeier ME, Morse DP, Knight SW, Portereiko M, Bass BL, Mango SE. A link between RNA interference and nonsense-mediated decay in Caenorhabditis elegans. Science 2000, 289:1928-1931.
109. 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, 29:3517-3528.
110. Metzstein MM, Krasnow MA. Functions of the nonsense-mediated mRNA decay pathway in Drosophila development. PLoS Genet 2006, 2:e180.
111. Avery P, Vicente-Crespo M, Francis D, Nashchekina O, Alonso CR, Palacios IM. Drosophila Upf1 and Upf2 loss of function inhibits cell growth and causes animal death in a Upf3-independent manner. RNA 2011, 17:624-638.
112. Chen Z, Smith KR, Batterham P, Robin C. Smg1 nonsense mutations do not abolish nonsense-mediated mRNA decay in Drosophila melanogaster. Genetics 2005, 171:403-406.
113. Tarpey PS, Raymond FL, Nguyen LS, Rodriguez J, Hackett A, Vandeleur L, Smith R, Shoubridge C, Edkins S, Stevens C, et al. Mutations in UPF3B, a member of the nonsense-mediated mRNA decay complex, cause syndromic and nonsyndromic mental retardation. Nat Genet 2007, 39:1127-1133.
114. Alonso CR, Akam M. A Hox gene mutation that triggers nonsense-mediated RNA decay and affects alternative splicing during Drosophila development. Nucleic Acids Res 2003, 31:3873-3880.
115. Filichkin SA, Priest HD, Givan SA, Shen R, Bryant DW, Fox SE, Wong WK, Mockler TC. Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res 2009, 20:45-58.
116. Barberan-Soler S, Lambert NJ, Zahler AM. Global analysis of alternative splicing uncovers developmental regulation of nonsense-mediated decay in C. elegans. RNA 2009, 15:1652-1660.
117. Hansen KD, Lareau LF, Blanchette M, Green RE, Meng Q, Rehwinkel J, Gallusser FL, Izaurralde E, Rio DC, Dudoit S, Brenner SE. Genome-wide identification of alternative splice forms down-regulated by nonsense-mediated mRNA decay in Drosophila. PLoS Genet 2009, 5:e1000525.
118. Lareau LF, Brooks AN, Soergel DA, Meng Q, Brenner SE. The coupling of alternative splicing and nonsense-mediated mRNA decay. Adv Exp Med Biol 2007, 623:190-211.
119. Kim YK, Furic L, Parisien M, Major F, DesGroseillers L, Maquat LE. Staufen1 regulates diverse classes of mammalian transcripts. EMBO J 2007, 26:2670-2681.
120. Gong C, Kim YK, Woeller CF, Tang Y, Maquat LE. SMD and NMD are competitive pathways that contribute to myogenesis: effects on PAX3 and myogenin mRNAs. Genes Dev 2009, 23:54-66.
121. Figueroa A, Cuadrado A, Fan J, Atasoy U, Muscat GE, Munoz-Canoves P, Gorospe M, Munoz A. Role of HuR in skeletal myogenesis through coordinate regulation of muscle differentiation genes. Mol Cell Biol 2003, 23:4991-5004.
122. Bruno IG, Karam R, Huang L, Bhardwaj A, Lou CH, Shum EY, Song HW, Corbett MA, Gifford WD, Gecz J, et al. Identification of a microRNA that activates gene expression by repressing nonsense-mediated RNA decay. Mol Cell 2011, 42:500-510.
123. Kulozik AE. Stay tuned: miRNA expression and nonsense-mediated decay in brain development. Mol Cell 2011, 42:407-408.
124. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010, 11:597-610.
125. 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 2009, 67:677-700.
126. Smirnova L, Grafe A, Seiler A, Schumacher S, Nitsch R, Wulczyn FG. Regulation of miRNA expression during neural cell specification. Eur J Neurosci 2005, 21:1469-1477.
127. Laumonnier F, Shoubridge C, Antar C, Nguyen LS, Van Esch H, Kleefstra T, Briault S, Fryns JP, Hamel B, Chelly J, et al. Mutations of the UPF3B gene, which encodes a protein widely expressed in neurons, are associated with nonspecific mental retardation with or without autism. Mol Psychiatry 2009, 15:767-776.
128. Delpy L, Sirac C, Magnoux E, Duchez S, Cogne M. RNA surveillance down-regulates expression of nonfunctional kappa alleles and detects premature termination within the last kappa exon. Proc Natl Acad Sci U S A 2004, 101:7375-7380.
129. Chemin G, Tinguely A, Sirac C, Lechouane F, Duchez S, Cogne M, Delpy L. Multiple RNA surveillance mechanisms cooperate to reduce the amount of nonfunctional Ig kappa transcripts. J Immunol 2010, 184:5009-5017.
130. Carter MS, Doskow J, Morris P, Li S, Nhim RP, Sandstedt S, Wilkinson MF. A regulatory mechanism that detects premature nonsense codons in T-cell receptor transcripts in vivo is reversed by protein synthesis inhibitors in vitro. J Biol Chem 1995, 270: 28995-29003.
131. Tinguely A, Chemin G, Peron S, Sirac C, Reynaud S, Cogne M, Delpy L. Cross talk between immunoglobulin heavy-chain transcription and RNA surveillance during B cell development. Mol Cell Biol 2011, 32:107-117.
132. Imam JS, Gudikote JP, Chan WK, Wilkinson MF. Frame-disrupting mutations elicit pre-mRNA accumulation independently of frame disruption. Nucleic Acids Res 2009, 38:1559-1574.
133. Muhlemann O, Mock-Casagrande CS, Wang J, Li S, Custodio N, Carmo-Fonseca M, Wilkinson MF, Moore MJ. Precursor RNAs harboring nonsense codons accumulate near the site of transcription. Mol Cell 2001, 8:33-43.
134. Bhalla AD, Gudikote JP, Wang J, Chan WK, Chang YF, Olivas OR, Wilkinson MF. Nonsense codons trigger an RNA partitioning shift. J Biol Chem 2009, 284: 4062-4072.
135. Wang J, Chang YF, Hamilton JI, Wilkinson MF. Nonsense-associated altered splicing: a frame-dependent response distinct from nonsense-mediated decay. Mol Cell 2002, 10:951-957.
136. Masel J, Trotter MV. Robustness and evolvability. Trends Genet 2010, 26:406-414.
137. Frankel N, Davis GK, Vargas D, Wang S, Payre F, Stern DL. Phenotypic robustness conferred by apparently redundant transcriptional enhancers. Nature 2010, 466:490-493.
138. Hwang J, Maquat LE. Nonsense-mediated mRNA decay (NMD) in animal embryogenesis: to die or not to die, that is the question. Curr Opin Genet Dev 2011, 21:422-430.
139. Vicente-Crespo M, Palacios IM. Nonsense-mediated mRNA decay and development: shoot the messenger to survive? Biochem Soc Trans 2010, 38:1500-1505.
140. Yepiskoposyan H, Aeschimann F, Nilsson D, Okoniewski M, Muhlemann O. Autoregulation of the nonsense-mediated mRNA decay pathway in human cells. RNA 2011, 17:2108-2118.
141. Saul H, Elharrar E, Gaash R, Eliaz D, Valenci M, Akua T, Avramov M, Frankel N, Berezin I, Gottlieb D, et al. The upstream open reading frame of the Arabidopsis AtMHX gene has a strong impact on transcript accumulation through the nonsense-mediated mRNA decay pathway. Plant J 2009, 60: 1031-1042.
142. Kerenyi Z, Merai Z, Hiripi L, Benkovics A, Gyula P, Lacomme C, Barta E, Nagy F, Silhavy D. Inter-kingdom conservation of mechanism of nonsense-mediated mRNA decay. EMBO J 2008, 27: 1585-1595.
143. 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:e92.
144. Chang YF, Imam JS, Wilkinson MF. The nonsense-mediated decay RNA surveillance pathway. Annu Rev Biochem 2007, 76:51-74.
145. Johansson MJ, He F, Spatrick P, Li C, Jacobson A. Association of yeast Upf1p with direct substrates of the NMD pathway. Proc Natl Acad Sci U S A 2007, 104: 20872-20877.
146. Nguyen LS, Jolly L, Shoubridge C, Chan WK, Huang L, Laumonnier F, Raynaud M, Hackett A, Field M, Rodriguez J, et al. Transcriptome profiling of UPF3B/NMD-deficient lymphoblastoid cells from patients with various forms of intellectual disability. Mol Psychiatry 2011, 163.
147. Addington AM, Gauthier J, Piton A, Hamdan FF, Raymond A, Gogtay N, Miller R, Tossell J, Bakalar J, Germain G, et al. A novel frameshift mutation in UPF3B identified in brothers affected with childhood onset schizophrenia and autism spectrum disorders. Mol Psychiatry 2010, 17:468.
148. Szyszka P, Sharp SI, Dedman A, Gurling HM, McQuillin A. A nonconservative amino acid change in the UPF3B gene in a patient with schizophrenia. Psychiatr Genet 2011, 22:150-151.
149. Gardner LB, Corn PG. Hypoxic regulation of mRNA expression. Cell Cycle 2008, 7:1916-1924.
150. Wang D, Zavadil J, Martin L, Parisi F, Friedman E, Levy D, Harding H, Ron D, Gardner LB. Inhibition of nonsense-mediated RNA decay by the tumor microenvironment promotes tumorigenesis. Mol Cell Biol 2011, 31:3670-3680.
151. Gardner LB. Nonsense-mediated RNA decay regulation by cellular stress: implications for tumorigenesis. Mol Cancer Res 2010, 8:295-308.
152. Holbrook JA, Neu-Yilik G, Hentze MW, Kulozik AE. Nonsense-mediated decay approaches the clinic. Nat Genet 2004, 36:801-808.