Abstract
Nonsense-mediated mRNA decay (NMD) is a well characterized eukaryotic mRNA degradation pathway, responsible for the identification and degradation of transcripts harboring translation termination codons in premature contexts. Transcriptome-wide studies revealed that NMD is not only an mRNA surveillance pathway as initially thought, but is also a post-transcriptional regulatory mechanism of gene expression, as it fine-tunes the transcript levels of many wild-type genes. Hence, NMD contributes to the regulation of many essential biological processes, including pathophysiological mechanisms. In this chapter we discuss the importance of NMD and of its regulation to organism development and its link to the cellular stress responses, like the unfolded protein response (UPR) and the integrated stress response (ISR). Additionally, we describe how tumor cells have explored both NMD functions to promote tumorigenesis. Using published data and databases, we have also performed a network-based approach that further supports the link between NMD and these (patho) physiological processes.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
da Costa PJ, Menezes J, Romão L (2017) The role of alternative splicing coupled to nonsense-mediated mRNA decay in human disease. Int J Biochem Cell Biol 91:168–175
Popp MW, Maquat LE (2018) Nonsense-mediated mRNA Decay and Cancer. Curr Opin Genet Dev 48:44–50
Lykke-Andersen S, Jensen TH (2015) Nonsense-mediated mRNA decay: an intricate machinery that shapes transcriptomes. Nat Rev Mol Cell Biol 16:665–677
Popp MW-L, Maquat LE (2013) Organizing principles of mammalian nonsense-mediated mRNA decay. Annu Rev Genet 47:139–165
Goetz AE, Wilkinson M (2017) Stress and the nonsense-mediated RNA decay pathway. Cell Mol Life Sci 74:3509–3531
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
Chan W-K, Bhalla AD, Le Hir H, Nguyen LS, Huang L, Gécz J, Wilkinson MF (2009) A UPF3-mediated regulatory switch that maintains RNA surveillance. Nat Struct Mol Biol 16:747–753
Weischenfeldt J, Damgaard I, Bryder D, Theilgaard-Monch K, Thoren LA, Nielsen FC, Jacobsen SEW, 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
Chan W-K, Huang L, Gudikote JP, Chang Y-F, Imam JS, MacLean JA, Wilkinson MF (2007) An alternative branch of the nonsense-mediated decay pathway. EMBO J 26:1820–1830
Wittmann J, Hol EM, Jäck H-M (2006) hUPF2 silencing identifies physiologic substrates of mammalian nonsense-mediated mRNA decay. Mol Cell Biol 26:1272–1287
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
He F, Li X, Spatrick P, Casillo R, Dong S, Jacobson A (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
Lelivelt MJ, Culbertson MR (1999) Yeast Upf proteins required for RNA surveillance affect global expression of the yeast transcriptome. Mol Cell Biol 19:6710–6719
Yepiskoposyan H, Aeschimann F, Nilsson D, Okoniewski M, Muhlemann O (2011) Autoregulation of the nonsense-mediated mRNA decay pathway in human cells. RNA 17:2108–2118
Colombo M, Karousis ED, Bourquin J, Bruggmann R, Mühlemann O (2017) Transcriptome-wide identification of NMD-targeted human mRNAs reveals extensive redundancy between SMG6- and SMG7-mediated degradation pathways. RNA 23:189–201
Losson R, Lacroute F (1979) Interference of nonsense mutations with eukaryotic messenger RNA stability. Proc Natl Acad Sci 76:5134–5137
Maquat LE, Kinniburgh AJ, Rachmilewitz EA, Ross J (1981) Unstable β-globin mRNA in mRNA-deficient β0 thalassemia. Cell 27:543–553
Miller JN, Pearce DA (2014) Nonsense-mediated decay in genetic disease: Friend or foe? Mutat Res Rev Mutat Res 762:52–64
Metze S, Herzog VA, Ruepp M-D, Mühlemann O (2013) Comparison of EJC-enhanced and EJC-independent NMD in human cells reveals two partially redundant degradation pathways. RNA 19:1432–1448
Le Hir H, Izaurralde E, Maquat LE, Moore MJ (2000) The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J 19:6860–6869
Alexandrov A, Colognori D, Shu M-D, Steitz JA (2012) Human spliceosomal protein CWC22 plays a role in coupling splicing to exon junction complex deposition and nonsense-mediated decay. Proc Natl Acad Sci 109:21313–21318
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
Chan W, Huang L, Gudikote JP, Chang Y, Imam JS, MacLean JA, Wilkinson MF (2007) An alternative branch of the nonsense-mediated decay pathway. EMBO J 26:1820–1830
Ishigaki Y, Li X, Serin G, Maquat LE (2001) Evidence for a Pioneer Round of mRNA Translation. Cell 106:607–617
Lejeune F, Ishigaki Y, Li X, Maquat LE (2002) The exon junction complex is detected on CBP80-bound but not eIF4E-bound mRNA in mammalian cells: dynamics of mRNP remodeling. EMBO J 21:3536–3545
Gehring NH, Lamprinaki S, Kulozik AE, Hentze MW (2009) Disassembly of exon junction complexes by PYM. Cell 137:536–548
Kashima I, Yamashita A, Izumi N, Kataoka N, Morishita R, Hoshino S, Ohno M, Dreyfuss G, Ohno S (2006) Binding of a novel SMG-1-Upf1-eRF1-eRF3 complex (SURF) to the exon junction complex triggers Upf1 phosphorylation and nonsense-mediated mRNA decay. Genes Dev 20:355–367
Buchwald G, Ebert J, Basquin C, Sauliere J, Jayachandran U, Bono F, Le Hir H, Conti E (2010) Insights into the recruitment of the NMD machinery from the crystal structure of a core EJC-UPF3b complex. Proc Natl Acad Sci 107:10050–10055
Yamashita A, Izumi N, Kashima I, Ohnishi T, Saari B, Katsuhata Y, Muramatsu R, Morita T, Iwamatsu A, Hachiya T, Kurata R, Hirano H, Anderson P, Ohno S (2009) 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 23:1091–1105
Shum EY, Jones SH, Shao A, Dumdie J, Krause MD, Chan W-K, Lou C-H, Espinoza JL, Song H-W, Phan MH, Ramaiah M, Huang L, McCarrey JR, Peterson KJ, De Rooij DG, Cook-andersen H, Wilkinson MF (2016) The antagonistic gene paralogs Upf3a and Upf3b govern nonsense-mediated RNA decay. Cell 165:382–395
Neu-Yilik G, Raimondeau E, Eliseev B, Yeramala L, Amthor B, Deniaud A, Huard K, Kerschgens K, Hentze MW, Schaffitzel C, Kulozik AE (2017) Dual function of UPF3B in early and late translation termination. EMBO J 36:2968–2986
Mühlemann O, Karousis ED (2017) New functions in translation termination uncovered for NMD factor UPF3B. EMBO J 36:2928–2930
Arias-Palomo E, Yamashita A, Fernández IS, Núñez-Ramírez R, Bamba Y, Izumi N, Ohno S, Llorca O (2011) The nonsense-mediated mRNA decay SMG-1 kinase is regulated by large-scale conformational changes controlled by SMG-8. Genes Dev 25:153–164
Chamieh H, Ballut L, Bonneau F, Le Hir H (2008) NMD factors UPF2 and UPF3 bridge UPF1 to the exon junction complex and stimulate its RNA helicase activity. Nat Struct Mol Biol 15:85–93
Deniaud A, Karuppasamy M, Bock T, Masiulis S, Huard K, Garzoni F, Kerschgens K, Hentze MW, Kulozik AE, Beck M, Neu-Yilik G, Schaffitzel C (2015) A network of SMG-8, SMG-9 and SMG-1 C-terminal insertion domain regulates UPF1 substrate recruitment and phosphorylation. Nucleic Acids Res 43:7600–7611
Melero R, Uchiyama A, Castaño R, Kataoka N, Kurosawa H, Ohno S, Yamashita A, Llorca O (2014) Structures of SMG1-UPFs complexes: SMG1 contributes to regulate UPF2-dependent activation of UPF1 in NMD. Structure 22:1105–1119
Okada-Katsuhata Y, Yamashita A, Kutsuzawa K, Izumi N, Hirahara F, Ohno S (2012) N-and C-terminal Upf1 phosphorylations create binding platforms for SMG-6 and SMG-5:SMG-7 during NMD. Nucleic Acids Res 40:1251–1266
Hug N, Cáceres JF (2014) The RNA Helicase DHX34 Activates NMD by promoting a transition from the surveillance to the decay-inducing complex. Cell Rep 8:1845–1856
Melero R, Hug N, Lopez-Perrote A, Yamashita A, Caceres JF, Llorca O (2016) The RNA helicase DHX34 functions as a scaffold for SMG1-mediated UPF1 phosphorylation. Nat Commun 7:10585
Cho H, Kim KM, Kim YK (2009) Human proline-rich nuclear receptor coregulatory protein 2 mediates an interaction between mRNA surveillance machinery and decapping complex. Mol Cell 33:75–86
Eberle AB, Lykke-Andersen S, Mühlemann O, Jensen TH (2009) SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat Struct Mol Biol 16:49–55
Huntzinger E, Kashima I, Fauser M, Sauliere J, Izaurralde E (2008) SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA 14:2609–2617
Glavan F, Behm-Ansmant I, Izaurralde E, Conti E (2006) Structures of the PIN domains of SMG6 and SMG5 reveal a nuclease within the mRNA surveillance complex. EMBO J 25:5117–5125
Boehm V, Haberman N, Ottens F, Ule J, Gehring NH (2014) 3′ UTR length and messenger ribonucleoprotein composition determine endocleavage efficiencies at termination codons. Cell Rep 9:555–568
Schmidt SA, Foley PL, Jeong DH, Rymarquis LA, Doyle F, Tenenbaum SA, Belasco JG, Green PJ (2015) Identification of SMG6 cleavage sites and a preferred RNA cleavage motif by global analysis of endogenous NMD targets in human cells. Nucleic Acids Res 43:309–323
Lykke-Andersen S, Chen Y, Ardal BR, Lilje B, Waage J, Sandelin A, Jensen TH (2014) Human nonsense-mediated RNA decay initiates widely by endonucleolysis and targets snoRNA host genes. Genes Dev 28:2498
Fukuhara N, Ebert J, Unterholzner L, Lindner D, Izaurralde E, Conti E (2005) SMG7 is a 14-3-3-like adaptor in the nonsense-mediated mRNA decay pathway. Mol Cell 17:537–547
Gatfield D, Izaurralde E (2004) Nonsense-mediated messenger RNA decay is initiated by endonucleolytic cleavage in Drosophila. Nature 429:575–578
Lejeune F, Li X, Maquat LE (2003) Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol Cell 12:675–687
Unterholzner L, Izaurralde E (2004) SMG7 acts as a molecular link between mRNA surveillance and mRNA decay. Mol Cell 16:587–596
Eberle AB, Stalder L, Mathys H, Orozco RZ, Mühlemann O (2008) Posttranscriptional gene regulation by spatial rearrangement of the 3′ untranslated region. PLoS Biol 6:849–859
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
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
Silva AL, Ribeiro P, Inácio A, 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
Wang W, Czaplinski K, Rao Y, Peltz SW (2001) The role of Upf proteins in modulating the translation read-through of nonsense-containing transcripts. EMBO J 20:880–890
Kononenko AV, Mitkevich VA, Atkinson GC, Tenson T, Dubovaya VI, Frolova LY, Makarov AA, Hauryliuk V (2010) GTP-dependent structural rearrangement of the eRF1:eRF3 complex and eRF3 sequence motifs essential for PABP binding. Nucleic Acids Res 38:548–558
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
Roque S, Cerciat M, Gaugué S, Mora L, Floch AG, De Zamaroczy M, Heurgué-Hamard V, Kervestin S (2015) Interaction between the poly(A)-binding protein Pab1 and the eukaryotic release factor eRF3 regulates translation termination but not mRNA decay in Saccharomyces cerevisiae. RNA 21:124–134
Joncourt R, Eberle AB, Rufener SC, Mühlemann O (2014) Eukaryotic initiation factor 4G suppresses nonsense-mediated mRNA decay by two genetically separable mechanisms. PLoS One 9:e104391
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
Bühler 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
Huang L, Lou C-H, Chan W, Shum EY, Shao A, Stone E, Karam R, Song H-W, Wilkinson MF (2011) RNA homeostasis governed by cell type-specific and branched feedback loops acting on NMD. Mol Cell 43:950–961
Aznarez I, Nomakuchi TT, Tetenbaum-Novatt, Jaclyn Rahman MA, Fregoso O, Rees H, Krainer AR (2018) Mechanism of Nonsense-Mediated mRNA Decay Stimulation by Splicing Factor SRSF1. Cell Rep 23:2186–2198
Maquat LE (2004) Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nat Rev Mol Cell Biol 5:89–99
Oliveira CC, McCarthy JE (1995) 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 270:8936–8943
Hogg JR, Goff SP (2010) Upf1 senses 3’UTR length to potentiate mRNA decay. Cell 143:379–389
Amrani N, Ghosh S, Mangus DA, Jacobson A (2008) Translation factors promote the formation of two states of the closed-loop mRNP. Nature 453:1276–1280
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
Nasif S, Contu L, Mühlemann O (2018) Beyond quality control: the role of nonsense-mediated mRNA decay (NMD) in regulating gene expression. Semin Cell Dev Biol 75:78–87
Medghalchi SM, Frischmeyer PA, Mendell JT, Kelly AG, Lawler AM, Dietz HC (2001) Rent1, a trans-effector of nonsense-mediated mRNA decay, is essential for mammalian embryonic viability. Hum Mol Genet 10:99–105
Li T, Shi Y, Wang P, Guachalla LM, Sun B, Joerss T, Chen Y-S, Groth M, Krueger A, Platzer M, Yang Y-G, Rudolph KL, Wang Z-Q (2015) Smg6/Est1 licenses embryonic stem cell differentiation via nonsense-mediated mRNA decay. EMBO J 34:1630–1647
McIlwain DR, Pan Q, Reilly PT, Elia AJ, McCracken S, Wakeham AC, Itie-Youten A, Blencowe BJ, Mak TW (2010) Smg1 is required for embryogenesis and regulates diverse genes via alternative splicing coupled to nonsense-mediated mRNA decay. Proc Natl Acad Sci 107:12186–12191
Shaheen R, Anazi S, Ben-Omran T, Seidahmed MZ, Caddle LB, Palmer K, Ali R, Alshidi T, Hagos S, Goodwin L, Hashem M, Wakil SM, Abouelhoda M, Colak D, Murray SA, Alkuraya FS (2016) Mutations in SMG9, encoding an essential component of nonsense-mediated decay machinery, cause a multiple congenital anomaly syndrome in humans and mice. Am J Hum Genet 98:643–652
Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J (2007) Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318:798–801
Imamachi N, Tani H, Akimitsu N (2012) Up-frameshift protein 1 (UPF1): multitalented entertainer in RNA decay. Drug Discov Ther 6:55–61
Nelson JO, Moore KA, Chapin A, Hollien J, Metzstein MM (2016) Degradation of Gadd45 mRNA by nonsense-mediated decay is essential for viability. elife 5:e12876
Tani H, Torimura M, Akimitsu N (2013) The RNA degradation pathway regulates the function of GAS5 a non-coding RNA in mammalian cells. PLoS One 8:e55684
Mourtada-Maarabouni M, Williams GT (2013) Growth arrest on inhibition of nonsense-mediated decay is mediated by noncoding RNA GAS5. Biomed Res Int 2013:358015
Huang L, Wilkinson MF (2012) Regulation of nonsense-mediated mRNA decay. Wiley Interdiscip Rev RNA 3:807–828
Lou CH, Dumdie J, Goetz A, Shum EY, Brafman D, Liao X, Mora-Castilla S, Ramaiah M, Cook-Andersen H, Laurent L, Wilkinson MF (2016) Nonsense-mediated RNA decay influences human embryonic stem cell fate. Stem Cell Reports 6:844–857
Thoren LA, Nørgaard GA, Weischenfeldt J, Waage J, Jakobsen JS, Damgaard I, Bergström FC, Blom AM, Borup R, Bisgaard HC, Porse BT (2010) UPF2 is a critical regulator of liver development, function and regeneration. PLoS One 5:e11650
Bao J, Tang C, Yuan S, Porse BT, Yan W (2015) UPF2, a nonsense-mediated mRNA decay factor, is required for prepubertal Sertoli cell development and male fertility by ensuring fidelity of the transcriptome. Development 142:352–362
Bao J, Vitting-Seerup K, Waage J, Tang C, Ge Y, Porse BT, Yan W (2016) UPF2-dependent nonsense-mediated mRNA decay pathway is essential for spermatogenesis by selectively eliminating longer 3’UTR transcripts. PLoS Genet 12:e1005863
Fanourgakis G, Lesche M, Akpinar M, Dahl A, Jessberger R (2016) chromatoid body protein TDRD6 supports long 3’ UTR triggered nonsense mediated mRNA decay. PLoS Genet 12:e1005857
Kunz JB, Neu-Yilik G, Hentze MW, Kulozik AE, Gehring NH (2006) Functions of hUpf3a and hUpf3b in nonsense-mediated mRNA decay and translation. RNA 12:1015–1022
Turner JMA (2007) Meiotic sex chromosome inactivation. Development 134:1823–1831
Kim YK, Furic L, Parisien M, Major F, DesGroseillers L, Maquat LE (2007) Staufen1 regulates diverse classes of mammalian transcripts. EMBO J 26:2670–2681
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
Bruno IG, Karam R, Huang L, Bhardwaj A, Lou CH, Shum EY, Song H-W, Corbett MA, Gifford WD, Gecz J, Pfaff SL, Wilkinson MF (2011) Identification of a microRNA that activates gene expression by repressing nonsense-mediated RNA decay. Mol Cell 42:500–510
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
Preitner N, Quan J, Flanagan JG (2013) This message will self-destruct: NMD regulates axon guidance. Cell 153:1185–1187
Colak D, Ji S-J, Porse BT, Jaffrey SR (2013) Regulation of axon guidance by compartmentalized nonsense-mediated mRNA decay. Cell 153:1252–1265
Nguyen LS, Jolly L, Shoubridge C, Chan WK, Huang L, Laumonnier F, Raynaud M, Hackett A, Field M, Rodriguez J, Srivastava AK, Lee Y, Long R, Addington AM, Rapoport JL, Suren S, Hahn CN, Gamble J, Wilkinson MF, Corbett MA, Gecz J (2012) Transcriptome profiling of UPF3B/NMD-deficient lymphoblastoid cells from patients with various forms of intellectual disability. Mol Psychiatry 17:1103–1115
Laumonnier F, Shoubridge C, Antar C, Nguyen LS, Van Esch H, Kleefstra T, Briault S, Fryns JP, Hamel B, Chelly J, Ropers HH, Ronce N, Blesson S, Moraine C, Gécz J, Raynaud M (2010) 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 15:767–776
Tarpey PS, Lucy Raymond F, Nguyen LS, Rodriguez J, Hackett A, Vandeleur L, Smith R, Shoubridge C, Edkins S, Stevens C, O’Meara S, Tofts C, Barthorpe S, Buck G, Cole J, Halliday K, Hills K, Jones D, Mironenko T, Perry J, Varian J, West S, Widaa S, Teague J, Dicks E, Butler A, Menzies A, Richardson D, Jenkinson A, Shepherd R, Raine K, Moon J, Luo Y, Parnau J, Bhat SS, Gardner A, Corbett M, Brooks D, Thomas P, Parkinson-Lawrence E, Porteous ME, Warner JP, Sanderson T, Pearson P, Simensen RJ, Skinner C, Hoganson G, Superneau D, Wooster R, Bobrow M, Turner G, Stevenson RE, Schwartz CE, Andrew Futreal P, Srivastava AK, Stratton MR, Gécz J (2007) Mutations in UPF3B, a member of the nonsense-mediated mRNA decay complex, cause syndromic and nonsyndromic mental retardation. Nat Genet 39:1127–1133
Nguyen LS, Kim H-G, Rosenfeld JA, Shen Y, Gusella JF, Lacassie Y, Layman LC, Shaffer LG, Gécz J (2013) Contribution of copy number variants involving nonsense-mediated mRNA decay pathway genes to neuro-developmental disorders. Hum Mol Genet 22:1816–1825
Wang D, Zavadil J, Martin L, Parisi F, Friedman E, Levy D, Harding H, Ron D, Gardner LB (2011) Inhibition of nonsense-mediated RNA decay by the tumor microenvironment promotes tumorigenesis. Mol Cell Biol 31:3670–3680
Oren YS, McClure ML, Rowe SM, Sorscher EJ, Bester AC, Manor M, Kerem E, Rivlin J, Zahdeh F, Mann M, Geiger T, Kerem B (2014) The unfolded protein response affects readthrough of premature termination codons. EMBO Mol Med 6:685–701
Pakos-Zebrucka K, Koryga I, Mnich K, Ljujic M, Samali A, Gorman AM (2016) The integrated stress response. EMBO Rep 17:1374–1395
Hetz C (2012) The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 13:89–102
Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107:881–891
Karam R, Lou C-H, Kroeger H, Huang L, Lin JH, Wilkinson MF (2015) The unfolded protein response is shaped by the NMD pathway. EMBO Rep 16:599–609
Gardner LB (2008) Hypoxic inhibition of nonsense-mediated RNA decay regulates gene expression and the integrated stress response. Mol Cell Biol 28:3729–3741
Martin L, Gardner LB (2015) Stress-induced inhibition of nonsense-mediated RNA decay regulates intracellular cystine transport and intracellular glutathione through regulation of the cystine/glutamate exchanger SLC7A11. Oncogene 34:4211–4218
Wang D, Wengrod J, Gardner LB (2011) Overexpression of the c-myc oncogene inhibits nonsense-mediated RNA decay in B lymphocytes. J Biol Chem 286:40038–40043
Li Z, Vuong JK, Zhang M, Stork C, Zheng S (2017) Inhibition of nonsense-mediated RNA decay by ER stress. RNA 23:378–394
Sieber J, Hauer C, Bhuvanagiri M, Leicht S, Krijgsveld J, Neu-Yilik G, Hentze MW, Kulozik AE (2016) Proteomic analysis reveals branch-specific regulation of the unfolded protein response by nonsense-mediated mRNA decay. Mol Cell Proteomics 15:1584–1597
Buzina A, Shulman MJ (1999) Infrequent translation of a nonsense codon is sufficient to decrease mRNA level. Mol Biol Cell 10:515–524
Karam R, Wengrod J, Gardner LB, Wilkinson MF (2013) Regulation of nonsense-mediated mRNA decay: implications for physiology and disease. Biochim Biophys Acta 1829:624–633
Zheng D, Chen C-YA, Shyu A-B (2011) Unraveling regulation and new components of human P-bodies through a protein interaction framework and experimental validation. RNA 17:1619–1634
McEwen E, Kedersha N, Song B, Scheuner D, Gilks N, Han A, Chen JJ, Anderson P, Kaufman RJ (2005) Heme-regulated inhibitor kinase-mediated phosphorylation of eukaryotic translation initiation factor 2 inhibits translation, induces stress granule formation, and mediates survival upon arsenite exposure. J Biol Chem 280:16925–16933
Kimball SR, Horetsky RL, Ron D, Jefferson LS, Harding HP (2003) Mammalian stress granules represent sites of accumulation of stalled translation initiation complexes. Am J Physiol Physiol 284:C273–C284
Brown JAL, Roberts TL, Richards R, Woods R, Birrell G, Lim YC, Ohno S, Yamashita A, Abraham RT, Gueven N, Lavin MF (2011) A novel role for hSMG-1 in stress granule formation. Mol Cell Biol 31:4417–4429
Jia J, Werkmeister E, Gonzalez-Hilarion S, Leroy C, Gruenert DC, Lafont F, Tulasne D, Lejeune F (2017) Premature termination codon readthrough in human cells occurs in novel cytoplasmic foci and requires UPF proteins. J Cell Sci 130:3009–3022
Vattem KM, Wek RC (2004) Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc Natl Acad Sci U S A 101:11269–11274
Palam LR, Baird TD, Wek RC (2011) Phosphorylation of eIF2 facilitates ribosomal bypass of an inhibitory upstream ORF to enhance CHOP translation. J Biol Chem 286:10939–10949
Abastado JP, Miller PF, Jackson BM, Hinnebusch AG (1991) Suppression of ribosomal reinitiation at upstream open reading frames in amino acid-starved cells forms the basis for GCN4 translational control. Mol Cell Biol 11:486–496
Sakaki K, Yoshina S, Shen X, Han J, DeSantis MR, Xiong M, Mitani S, Kaufman RJ (2012) RNA surveillance is required for endoplasmic reticulum homeostasis. Proc Natl Acad Sci U S A 109:8079–8084
Gardner LB (2010) Nonsense-mediated RNA decay regulation by cellular stress: implications for tumorigenesis. Mol Cancer Res 8:295–308
Mort M, Ivanov D, Cooper DN, Chuzhanova NA (2008) A meta-analysis of nonsense mutations causing human genetic disease. Hum Mutat 29:1037–1047
Pinyol M, Bea S, Pla L, Ribrag V, Bosq J, Rosenwald A, Campo E, Jares P (2007) Inactivation of RB1 in mantle-cell lymphoma detected by nonsense-mediated mRNA decay pathway inhibition and microarray analysis. Blood 109:5422–5429
Anczuków O, Ware MD, Buisson M, Zetoune AB, Stoppa-Lyonnet D, Sinilnikova OM, Mazoyer S (2008) Does the nonsense-mediated mRNA decay mechanism prevent the synthesis of truncated BRCA1, CHK2, and p53 proteins? Hum Mutat 29:65–73
Karam R, Carvalho J, Bruno I, Graziadio C, Senz J, Huntsman D, Carneiro F, Seruca R, Wilkinson MF, Oliveira C (2008) The NMD mRNA surveillance pathway downregulates aberrant E-cadherin transcripts in gastric cancer cells and in CDH1 mutation carriers. Oncogene 27:4255–4260
Perrin-Vidoz L, Sinilnikova OM, Stoppa-Lyonnet D, Lenoir GM, Mazoyer S (2002) The nonsense-mediated mRNA decay pathway triggers degradation of most BRCA1 mRNAs bearing premature termination codons. Hum Mol Genet 11:2805–2814
Ware MD, DeSilva D, Sinilnikova OM, Stoppa-Lyonnet D, Tavtigian SV, Mazoyer S (2006) Does nonsense-mediated mRNA decay explain the ovarian cancer cluster region of the BRCA2 gene? Oncogene 25:323–328
Reddy JC, Morris JC, Wang J, English MA, Haber DA, Shi Y, Licht JD (1995) WT1-mediated transcriptional activation is inhibited by dominant negative mutant proteins. J Biol Chem 270:10878–10884
Liu C, Karam R, Zhou Y, Su F, Ji Y, Li G, Xu G, Lu L, Wang C, Song M, Zhu J, Wang Y, Zhao Y, Foo WC, Zuo M, Valasek MA, Javle M, Wilkinson MF, Lu Y (2014) The UPF1 RNA surveillance gene is commonly mutated in pancreatic adenosquamous carcinoma. Nat Med 20:596–598
Lindeboom RGH, Supek F, Lehner B (2016) The rules and impact of nonsense-mediated mRNA decay in human cancers. Nat Genet 48:1112–1118
Lu J, Plank T-D, Su F, Shi X, Liu C, Ji Y, Li S, Huynh A, Shi C, Zhu B, Yang G, Wu Y, Wilkinson MF, Lu Y (2016) The nonsense-mediated RNA decay pathway is disrupted in inflammatory myofibroblastic tumors. J Clin Invest 126:3058–3062
Chang L, Li C, Guo T, Wang H, Ma W, Yuan Y, Liu Q, Ye Q, Liu Z (2016) The human RNA surveillance factor UPF1 regulates tumorigenesis by targeting Smad7 in hepatocellular carcinoma. J Exp Clin Cancer Res 35:8
Cao L, Qi L, Zhang L, Song W, Yu Y, Xu C, Li L, Guo Y, Yang L, Liu C, Huang Q, Wang Y, Sun B, Meng B, Zhang B, Cao W (2017) Human nonsense-mediated RNA decay regulates EMT by targeting the TGF-ß signaling pathway in lung adenocarcinoma. Cancer Lett 403:246–259
Giampietri C, Petrungaro S, Conti S, Facchiano A, Filippini A, Ziparo E (2015) Cancer microenvironment and endoplasmic reticulum stress response. Mediat Inflamm 2015:417281
Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, Mukherjee C, Shi Y, Gélinas C, Fan Y, Nelson DA, Jin S, White E (2006) Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10:51–64
Ye J, Kumanova M, Hart LS, Sloane K, Zhang H, De Panis DN, Bobrovnikova-Marjon E, Diehl JA, Ron D, Koumenis C (2010) The GCN2-ATF4 pathway is critical for tumour cell survival and proliferation in response to nutrient deprivation. EMBO J 29:2082–2096
Wengrod J, Martin L, Wang D, Frischmeyer-Guerrerio P, Dietz HC, Gardner LB (2013) Inhibition of nonsense-mediated RNA decay activates autophagy. Mol Cell Biol 33:2128–2135
Jia J, Furlan A, Gonzalez-Hilarion S, Leroy C, Gruenert DC, Tulasne D, Lejeune F (2015) Caspases shutdown nonsense-mediated mRNA decay during apoptosis. Cell Death Differ 22:1754–1763
Popp MW, Maquat LE (2015) Attenuation of nonsense-mediated mRNA decay facilitates the response to chemotherapeutics. Nat Commun 6:6632
Dotan-Cohen D, Letovsky S, Melkman AA, Kasif S (2009) Biological process linkage networks. PLoS One 4:e5313
Forbes SA, Beare D, Boutselakis H, Bamford S, Bindal N, Tate J, Cole CG, Ward S, Dawson E, Ponting L, Stefancsik R, Harsha B, Kok CY, Jia M, Jubb H, Sondka Z, Thompson S, De T, Campbell PJ (2017) COSMIC: somatic cancer genetics at high-resolution. Nucleic Acids Res 45:D777–D783
COSMIC [Internet]. [cited 2018 Jul 18]. Available from: https://cancer.sanger.ac.uk / cosmic
Fabregat A, Jupe S, Matthews L, Sidiropoulos K, Gillespie M, Garapati P, Haw R, Jassal B, Korninger F, May B, Milacic M, Roca CD, Rothfels K, Sevilla C, Shamovsky V, Shorser S, Varusai T, Viteri G, Weiser J, Wu G, Stein L, Hermjakob H, D’Eustachio P (2018) The reactome pathway knowledgebase. Nucleic Acids Res 46:D649–D655
Reactome project [Internet]. [cited 2018 Jul 18]. Available from: https://reactome.org / download-data
Hug N, Longman D, Cáceres JF (2016) Mechanism and regulation of the nonsense-mediated decay pathway. Nucleic Acids Res 44:1483–1495
Yang X, Coulombe-Huntington J, Kang S, Sheynkman GM, Hao T, Richardson A, Sun S, Yang F, Shen YA, Murray RR, Spirohn K, Begg BE, Duran-Frigola M, MacWilliams A, Pevzner SJ, Zhong Q, Trigg SA, Tam S, Ghamsari L, Sahni N, Yi S, Rodriguez MD, Balcha D, Tan G, Costanzo M, Andrews B, Boone C, Zhou XJ, Salehi-Ashtiani K, Charloteaux B, Chen AA, Calderwood MA, Aloy P, Roth FP, Hill DE, Iakoucheva LM, Xia Y, Vidal M (2016) Widespread expansion of protein interaction capabilities by alternative splicing. Cell 164:805–817
Rolland T, Taşan M, Charloteaux B, Pevzner SJ, Zhong Q, Sahni N, Yi S, Lemmens I, Fontanillo C, Mosca R, Kamburov A, Ghiassian SD, Yang X, Ghamsari L, Balcha D, Begg BE, Braun P, Brehme M, Broly MP, Carvunis A-R, Convery-Zupan D, Corominas R, Coulombe-Huntington J, Dann E, Dreze M, Dricot A, Fan C, Franzosa E, Gebreab F, Gutierrez BJ, Hardy MF, Jin M, Kang S, Kiros R, Lin GN, Luck K, MacWilliams A, Menche J, Murray RR, Palagi A, Poulin MM, Rambout X, Rasla J, Reichert P, Romero V, Ruyssinck E, Sahalie JM, Scholz A, Shah AA, Sharma A, Shen Y, Spirohn K, Tam S, Tejeda AO, Trigg SA, Twizere J-C, Vega K, Walsh J, Cusick ME, Xia Y, Barabási A-L, Iakoucheva LM, Aloy P, De Las Rivas J, Tavernier J, Calderwood MA, Hill DE, Hao T, Roth FP, Vidal M (2014) A proteome-scale map of the human interactome network. Cell 159:1212–1226
Venkatesan K, Rual J-F, Vazquez A, Stelzl U, Lemmens I, Hirozane-Kishikawa T, Hao T, Zenkner M, Xin X, Goh K-I, Yildirim MA, Simonis N, Heinzmann K, Gebreab F, Sahalie JM, Cevik S, Simon C, de Smet A-S, Dann E, Smolyar A, Vinayagam A, Yu H, Szeto D, Borick H, Dricot A, Klitgord N, Murray RR, Lin C, Lalowski M, Timm J, Rau K, Boone C, Braun P, Cusick ME, Roth FP, Hill DE, Tavernier J, Wanker EE, Barabási A-L, Vidal M (2009) An empirical framework for binary interactome mapping. Nat Methods 6:83–90
Yu H, Tardivo L, Tam S, Weiner E, Gebreab F, Fan C, Svrzikapa N, Hirozane-Kishikawa T, Rietman E, Yang X, Sahalie J, Salehi-Ashtiani K, Hao T, Cusick ME, Hill DE, Roth FP, Braun P, Vidal M (2011) Next-generation sequencing to generate interactome datasets. Nat Methods 8:478–480
Rual J-F, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, Li N, Berriz GF, Gibbons FD, Dreze M, Ayivi-Guedehoussou N, Klitgord N, Simon C, Boxem M, Milstein S, Rosenberg J, Goldberg DS, Zhang LV, Wong SL, Franklin G, Li S, Albala JS, Lim J, Fraughton C, Llamosas E, Cevik S, Bex C, Lamesch P, Sikorski RS, Vandenhaute J, Zoghbi HY, Smolyar A, Bosak S, Sequerra R, Doucette-Stamm L, Cusick ME, Hill DE, Roth FP, Vidal M (2005) Towards a proteome-scale map of the human protein–protein interaction network. Nature 437:1173–1178
Alonso-López D, Gutiérrez MA, Lopes KP, Prieto C, Santamaría R, De Las Rivas J (2016) APID interactomes: providing proteome-based interactomes with controlled quality for multiple species and derived networks. Nucleic Acids Res 44:W529–W535
Türei D, Korcsmáros T, Saez-Rodriguez J (2016) OmniPath: guidelines and gateway for literature-curated signaling pathway resources. Nat Methods 13:966–967
Li T, Wernersson R, Hansen RB, Horn H, Mercer J, Slodkowicz G, Workman CT, Rigina O, Rapacki K, Stærfeldt HH, Brunak S, Jensen TS, Lage K (2017) A scored human protein-protein interaction network to catalyze genomic interpretation. Nat Methods 14:61–64
Martinez NJ, Walhout AJM (2009) The interplay between transcription factors and microRNAs in genome-scale regulatory networks. BioEssays 31:435–445
Xu Y, Yue W, Yao Shugart Y, Li S, Cai L, Li Q, Cheng Z, Wang G, Zhou Z, Jin C, Yuan J, Tian L, Wang J, Zhang K, Zhang K, Liu S, Song Y, Zhang F (2016) Exploring transcription factors-microRNAs co-regulation networks in schizophrenia. Schizophr Bull 42:1037–1045
Chou C-H, Shrestha S, Yang C-D, Chang N-W, Lin Y-L, Liao K-W, Huang W-C, Sun T-H, Tu S-J, Lee W-H, Chiew M-Y, Tai C-S, Wei T-Y, Tsai T-R, Huang H-T, Wang C-Y, Wu H-Y, Ho S-Y, Chen P-R, Chuang C-H, Hsieh P-J, Wu Y-S, Chen W-L, Li M-J, Wu Y-C, Huang X-Y, Ng FL, Buddhakosai W, Huang P-C, Lan K-C, Huang C-Y, Weng S-L, Cheng Y-N, Liang C, Hsu W-L, Huang H-D (2018) miRTarBase update 2018: a resource for experimentally validated microRNA-target interactions. Nucleic Acids Res 46:D296–D302
Rouillard AD, Gundersen GW, Fernandez NF, Wang Z, Monteiro CD, McDermott MG, Ma’ayan A (2016) The harmonizome: a collection of processed datasets gathered to serve and mine knowledge about genes and proteins. Database 2016:baw100
Li YF, Altman RB (2018) Systematic target function annotation of human transcription factors. BMC Biol 16:4
Han H, Cho J-W, Lee S, Yun A, Kim H, Bae D, Yang S, Kim CY, Lee M, Kim E, Lee S, Kang B, Jeong D, Kim Y, Jeon H-N, Jung H, Nam S, Chung M, Kim J-H, Lee I (2018) TRRUST v2: an expanded reference database of human and mouse transcriptional regulatory interactions. Nucleic Acids Res 46:D380–D386
van Dam S, Craig T, de Magalhães JP (2015) GeneFriends: a human RNA-seq-based gene and transcript co-expression database. Nucleic Acids Res 43:D1124–D1132
Ishigaki Y, Li X, Serin G, Maquat LE (2001) Evidence for a pioneer round of mRNA translation: mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20. Cell 106:607–617
Lejeune F, Ranganathan AC, Maquat LE (2004) eIF4G is required for the pioneer round of translation in mammalian cells. Nat Struct Mol Biol 11:992–1000
Ohnishi T, Yamashita A, Kashima I, Schell T, Anders KR, Grimson A, Hachiya T, Hentze MW, Anderson P, Ohno S (2003) Phosphorylation of hUPF1 induces formation of mRNA surveillance complexes containing hSMG-5 and hSMG-7. Mol Cell 12:1187–1200
Cowen LE, Tang Y (2017) Identification of nonsense-mediated mRNA decay pathway as a critical regulator of p53 isoform β. Sci Rep 7:17535
Brumbaugh KM, Otterness DM, Geisen C, Oliveira V, Brognard J, Li X, Lejeune F, Tibbetts RS, Maquat LE, Abraham RT (2004) The mRNA surveillance protein hSMG-1 functions in genotoxic stress response pathways in mammalian cells. Mol Cell 14:585–598
Abraham RT (2004) The ATM-related kinase, hSMG-1, bridges genome and RNA surveillance pathways. DNA Repair (Amst) 3:919–925
Welch MD, Iwamatsu A, Mitchison TJ (1997) Actin polymerization is induced by Arp 2/3 protein complex at the surface of Listeria monocytogenes. Nature 385:265–269
Acknowledgements
This work was partially supported by Fundação para a Ciência e a Tecnologia (FCT; Portugal) (PTFC/BIM-MEC/3749/2014 to LR and UID/MULTI/04046/2013 Research Unit grant to BioISI), and by National Institute of Health Dr. Ricardo Jorge. RF is recipient of a fellowship from BioSys PhD programme (SFRH/BD/114392/2016) from FCT (Portugal). GN is recipient of a fellowship from BioSys PhD programme (PD/BD/130959/2017) from FCT (Portugal). PJC is recipient of a fellowship from BioSys PhD programme (PD/BD/52495/2014) from FCT (Portugal).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Annex 1: Table of Network Proteins and Their Attributes
Annex 1: Table of Network Proteins and Their Attributes
Uniprot ID | Gene Symbol | Biological Process | NMD links | NMD-factors | Coexpression | miRNA Coregulation | TF Coregulation | NMD Target |
Q9NQ94 | A1CF | Cancer | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 0 | 2 | 1 | 0 |
Q9NRG9 | AAAS | Stress | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 9 | 2 | 10 | 1 |
P49748 | ACADVL | Stress | 1 | EIF4A3 | 2 | 1 | 4 | 1 |
O95573 | ACSL3 | Cancer | 3 | UPF2 / RUVBL1 / RUVBL2 | 1 | 1 | 13 | 1 |
P60709 | ACTB | Development | 7 | UPF1 / MAGOH / EIF4A3 / SEC13 / GNL2 / RUVBL1 / RUVBL2 | 0 | 5 | 12 | 1 |
P63261 | ACTG1 | Development | 5 | UPF1 / SEC13 / GNL2 / RUVBL1 / RUVBL2 | 3 | 7 | 5 | 1 |
P61160 | ACTR2 | Development | 3 | GNL2 / RUVBL1 / RUVBL2 | 1 | 2 | 19 | 0 |
P61158 | ACTR3 | Development | 2 | GNL2 / RUVBL1 | 4 | 0 | 15 | 0 |
Q9UHB7 | AFF4 | Cancer | 1 | MAGOH | 2 | 2 | 17 | 0 |
O00468 | AGRN | Development | 1 | MOV10 | 3 | 1 | 2 | 1 |
P05091 | ALDH2 | Cancer | 3 | GNL2 / RUVBL1 / RUVBL2 | 0 | 2 | 4 | 1 |
O95782 | AP2A1 | Development | 2 | UPF1 / RNPS1 | 4 | 1 | 6 | 1 |
O94973 | AP2A2 | Development | 2 | UPF1 / MOV10 | 3 | 3 | 11 | 1 |
Q96BI3 | APH1A | Development | 1 | MOV10 | 3 | 0 | 9 | 1 |
P10275 | AR | Cancer | 2 | RUVBL1 / PNRC2 | 0 | 1 | 4 | 0 |
Q8N6T3 | ARFGAP1 | Stress | 1 | UPF1 | 6 | 0 | 13 | 1 |
O14497 | ARID1A | Cancer | 2 | MOV10 / RUVBL1 | 7 | 5 | 5 | 1 |
Q8NFD5 | ARID1B | Cancer | 1 | RUVBL1 | 5 | 1 | 4 | 1 |
Q68CP9 | ARID2 | Cancer | 1 | RUVBL1 | 2 | 0 | 1 | 0 |
Q92747 | ARPC1A | Development | 2 | GNL2 / RUVBL1 | 2 | 0 | 12 | 1 |
O15143 | ARPC1B | Development | 3 | GNL2 / MOV10 / RUVBL1 | 2 | 0 | 8 | 1 |
O15144 | ARPC2 | Development | 3 | GNL2 / RUVBL1 / RUVBL2 | 2 | 2 | 6 | 1 |
O15145 | ARPC3 | Development | 2 | GNL2 / RUVBL1 | 1 | 1 | 10 | 1 |
P59998 | ARPC4 | Development | 3 | GNL2 / MOV10 / RUVBL1 | 1 | 0 | 10 | 1 |
O15511 | ARPC5 | Development | 2 | GNL2 / RUVBL1 | 1 | 1 | 6 | 0 |
O43681 | ASNA1 | Stress | 2 | RUVBL1 / RUVBL2 | 6 | 3 | 8 | 1 |
P18848 | ATF4 | Stress | 1 | MOV10 | 5 | 0 | 11 | 1 |
Q13315 | ATM | Cancer Stress | 5 | UPF1 / SMG1 / MOV10 / RUVBL1 / RUVBL2 | 5 | 1 | 16 | 0 |
P05023 | ATP1A1 | Cancer | 1 | RUVBL2 | 1 | 5 | 6 | 1 |
Q13535 | ATR | Cancer Stress | 4 | UPF1 / SMG1 / RUVBL1 / RUVBL2 | 3 | 0 | 19 | 0 |
P61769 | B2M | Cancer | 1 | SEC13 | 1 | 1 | 11 | 0 |
O95817 | BAG3 | Stress | 2 | SEC13 / RUVBL2 | 0 | 1 | 1 | 1 |
O95429 | BAG4 | Stress | 1 | MOV10 | 6 | 1 | 7 | 0 |
P20749 | BCL3 | Cancer | 2 | RUVBL1 / RUVBL2 | 2 | 1 | 9 | 1 |
Q9NYF8 | BCLAF1 | Cancer | 5 | RNPS1 / MAGOH / EIF4A3 / MOV10 / PNRC2 | 5 | 3 | 21 | 0 |
P11274 | BCR | Cancer | 1 | SEC13 | 3 | 0 | 8 | 1 |
Q13489 | BIRC3 | Cancer | 2 | RUVBL1 / RUVBL2 | 1 | 0 | 14 | 1 |
P54132 | BLM | Cancer | 3 | UPF2 / MAGOH / EIF4A3 | 7 | 1 | 7 | 0 |
Q12982 | BNIP2 | Development | 1 | MOV10 | 5 | 2 | 8 | 1 |
Q15059 | BRD3 | Cancer | 1 | RUVBL2 | 4 | 1 | 2 | 1 |
O60885 | BRD4 | Cancer | 1 | MAGOH | 4 | 3 | 1 | 1 |
O60566 | BUB1B | Cancer | 1 | SEC13 | 7 | 1 | 12 | 0 |
P27797 | CALR | Cancer Stress | 1 | UPF2 | 3 | 1 | 15 | 1 |
Q8WVQ1 | CANT1 | Cancer | 1 | MOV10 | 2 | 0 | 11 | 1 |
P04632 | CAPNS1 | Development | 1 | RUVBL1 | 1 | 2 | 12 | 1 |
Q14790 | CASP8 | Cancer | 1 | CASC3 | 3 | 1 | 12 | 1 |
P04040 | CAT | Stress | 2 | UPF1 / MOV10 | 0 | 0 | 12 | 0 |
Q8N163 | CCAR2 | Stress | 1 | RUVBL2 | 10 | 0 | 13 | 0 |
P04233 | CD74 | Cancer | 1 | SEC13 | 0 | 0 | 4 | 1 |
Q9NYV4 | CDK12 | Cancer | 1 | RNPS1 | 3 | 1 | 12 | 1 |
Q00534 | CDK6 | Cancer | 1 | CASC3 | 0 | 6 | 9 | 0 |
P49715 | CEBPA | Cancer Development | 2 | RNPS1 / EIF4A3 | 0 | 0 | 14 | 1 |
P23528 | CFL1 | Development | 2 | RUVBL1 / RUVBL2 | 4 | 3 | 5 | 1 |
O14647 | CHD2 | Cancer | 2 | RUVBL1 / RUVBL2 | 4 | 0 | 6 | 1 |
O96017 | CHEK2 | Cancer | 2 | RUVBL1 / RUVBL2 | 5 | 1 | 10 | 1 |
Q7Z460 | CLASP1 | Development | 1 | SEC13 | 2 | 1 | 12 | 1 |
O75122 | CLASP2 | Development | 2 | SEC13 / MOV10 | 0 | 0 | 17 | 0 |
P30622 | CLIP1 | Cancer | 1 | SEC13 | 0 | 0 | 9 | 1 |
Q92989 | CLP1 | Cancer | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / SEC13 | 7 | 0 | 10 | 1 |
P09496 | CLTA | Development | 1 | RBM8A | 2 | 2 | 10 | 1 |
P09497 | CLTB | Development | 1 | SEC13 | 1 | 0 | 8 | 1 |
Q00610 | CLTC | Cancer Development | 4 | SEC13 / GNL2 / RUVBL1 / RUVBL2 | 3 | 5 | 24 | 0 |
P53675 | CLTCL1 | Cancer Development | 4 | GNL2 / MOV10 / RUVBL1 / RUVBL2 | 0 | 0 | 1 | 1 |
P62633 | CNBP | Cancer | 4 | UPF2 / MAGOH / GNL2 / RUVBL1 | 8 | 1 | 18 | 1 |
O75175 | CNOT3 | Cancer | 1 | RUVBL2 | 9 | 0 | 6 | 1 |
Q9ULM6 | CNOT6 | Development | 2 | RUVBL1 / RUVBL2 | 7 | 1 | 11 | 0 |
Q92600 | CNOT9 | Development | 1 | RUVBL2 | 1 | 0 | 0 | 0 |
Q7Z7A1 | CNTRL | Cancer | 1 | UPF1 | 4 | 1 | 0 | 1 |
Q01955 | COL4A3 | Development | 1 | MOV10 | 0 | 0 | 1 | 0 |
O43889 | CREB3 | Stress | 1 | MOV10 | 2 | 0 | 19 | 1 |
Q8TEY5 | CREB3L4 | Stress | 1 | MOV10 | 1 | 0 | 7 | 0 |
Q9BZJ0 | CRNKL1 | Cancer | 5 | UPF1 / MAGOH / EIF4A3 / GNL2 / RUVBL2 | 6 | 0 | 11 | 1 |
P68400 | CSNK2A1 | Development | 5 | RNPS1 / SEC13 / MOV10 / RUVBL1 / RUVBL2 | 9 | 2 | 11 | 0 |
P19784 | CSNK2A2 | Development | 3 | RNPS1 / SEC13 / RUVBL2 | 8 | 0 | 2 | 1 |
P67870 | CSNK2B | Development | 6 | UPF1 / RNPS1 / SEC13 / MOV10 / RUVBL1 / RUVBL2 | 3 | 0 | 6 | 1 |
P35222 | CTNNB1 | Cancer Development | 3 | MOV10 / RUVBL1 / RUVBL2 | 1 | 1 | 19 | 0 |
Q13617 | CUL2 | Stress Development | 3 | SMG6 / RNPS1 / MOV10 | 6 | 2 | 11 | 1 |
Q13618 | CUL3 | Cancer | 8 | UPF1 / SMG6 / RNPS1 / EIF4A3 / SEC13 / MOV10 / RUVBL1 / RUVBL2 | 5 | 2 | 6 | 1 |
Q14999 | CUL7 | Stress | 5 | RNPS1 / EIF4A3 / GNL2 / RUVBL1 / RUVBL2 | 4 | 0 | 8 | 1 |
P13498 | CYBA | Stress | 1 | UPF2 | 2 | 0 | 3 | 1 |
Q8IU60 | DCP2 | Stress | 5 | UPF1 / UPF2 / UPF3A / UPF3B / PNRC2 | 7 | 1 | 8 | 0 |
Q14203 | DCTN1 | Cancer Stress | 2 | UPF1 / MOV10 | 1 | 1 | 6 | 1 |
Q13206 | DDX10 | Cancer | 1 | UPF1 | 4 | 1 | 4 | 1 |
Q96FC9 | DDX11 | Stress | 2 | SMG9 / DHX34 | 9 | 1 | 10 | 0 |
O00571 | DDX3X | Cancer | 4 | MAGOH / EIF4A3 / RUVBL1 / RUVBL2 | 4 | 3 | 4 | 0 |
P17844 | DDX5 | Cancer | 5 | UPF1 / EIF4A3 / SEC13 / RUVBL1 / RUVBL2 | 4 | 2 | 17 | 1 |
P26196 | DDX6 | Cancer | 4 | UPF1 / GNL2 / RUVBL2 / PNRC2 | 4 | 7 | 19 | 0 |
P35659 | DEK | Cancer | 1 | UPF1 | 10 | 0 | 13 | 0 |
Q8WYQ5 | DGCR8 | Cancer | 3 | UPF1 / GNL2 / MOV10 | 9 | 0 | 17 | 1 |
Q9UPY3 | DICER1 | Cancer | 6 | UPF1 / EIF4A3 / GNL2 / MOV10 / RUVBL1 / RUVBL2 | 4 | 3 | 12 | 0 |
Q9Y2L1 | DIS3 | Stress | 1 | RUVBL2 | 4 | 1 | 9 | 1 |
P25685 | DNAJB1 | Cancer Stress | 3 | UPF2 / GNL2 / RUVBL2 | 0 | 1 | 13 | 1 |
Q99615 | DNAJC7 | Stress | 1 | SMG8 | 10 | 1 | 7 | 1 |
P50570 | DNM2 | Cancer Development | 1 | RUVBL2 | 5 | 2 | 18 | 1 |
Q7L190 | DPPA4 | Development | 2 | UPF1 / MAGOH | 0 | 1 | 1 | 1 |
Q02413 | DSG1 | Development | 1 | RUVBL1 | 0 | 0 | 0 | 0 |
P15924 | DSP | Development | 2 | RUVBL1 / RUVBL2 | 0 | 2 | 2 | 1 |
O75530 | EED | Cancer Development | 9 | UPF1 / RNPS1 / RBM8A / MAGOH / MAGOHB / EIF4A3 / MOV10 / RUVBL1 / RUVBL2 | 6 | 2 | 25 | 0 |
P68104 | EEF1A1 | Stress | 8 | UPF1 / MAGOH / EIF4A3 / SEC13 / GNL2 / MOV10 / RUVBL1 / RUVBL2 | 2 | 8 | 20 | 1 |
P52798 | EFNA4 | Development | 1 | MOV10 | 2 | 1 | 3 | 1 |
P47813 | EIF1AX | Cancer | 2 | RBM8A / MAGOH | 6 | 3 | 0 | 0 |
P05198 | EIF2S1 | Stress | 3 | UPF1 / EIF4A3 / RUVBL2 | 7 | 2 | 15 | 0 |
Q14240 | EIF4A2 | Cancer | 9 | UPF3B / SMG1 / RNPS1 / RBM8A / MAGOH / MAGOHB / EIF4A3 / RUVBL1 / RUVBL2 | 1 | 3 | 14 | 0 |
Q04637 | EIF4G1 | Development | 15 | UPF1 / UPF2 / UPF3A / UPF3B / SMG1 / SMG5 / SMG6 / SMG7 / SMG8 / SMG9 / RNPS1 / RBM8A / MAGOH / CASC3 / EIF4A3 | 8 | 2 | 10 | 1 |
Q99814 | EPAS1 | Cancer Stress Development | 1 | RUVBL1 | 0 | 0 | 3 | 1 |
P21709 | EPHA1 | Development | 3 | SMG1 / SMG8 / SMG9 | 0 | 0 | 1 | 1 |
P18074 | ERCC2 | Cancer | 1 | RUVBL2 | 7 | 0 | 3 | 1 |
Q92889 | ERCC4 | Cancer | 1 | RUVBL2 | 3 | 0 | 10 | 0 |
Q96HE7 | ERO1A | Stress | 2 | EIF4A3 / SEC13 | 0 | 0 | 0 | 0 |
P03372 | ESR1 | Cancer | 6 | UPF1 / EIF4A3 / GNL2 / RUVBL1 / RUVBL2 / PNRC2 | 0 | 2 | 7 | 1 |
P62495 | ETF1 | Development | 15 | UPF1 / UPF2 / UPF3A / UPF3B / SMG1 / SMG5 / SMG6 / SMG7 / SMG8 / SMG9 / RNPS1 / RBM8A / MAGOH / CASC3 / EIF4A3 | 8 | 2 | 14 | 0 |
P41161 | ETV5 | Cancer | 1 | MOV10 | 1 | 0 | 10 | 1 |
Q01844 | EWSR1 | Cancer | 5 | UPF1 / RBM8A / CASC3 / SEC13 / RUVBL1 | 11 | 2 | 11 | 1 |
Q9Y3B2 | EXOSC1 | Stress | 1 | UPF2 | 11 | 1 | 11 | 0 |
Q13868 | EXOSC2 | Stress | 5 | UPF1 / UPF2 / UPF3A / UPF3B / RUVBL2 | 11 | 2 | 11 | 1 |
Q9NPD3 | EXOSC4 | Stress | 4 | UPF1 / UPF2 / UPF3A / UPF3B | 8 | 0 | 24 | 1 |
Q5RKV6 | EXOSC6 | Stress | 1 | UPF2 | 4 | 1 | 8 | 1 |
Q96B26 | EXOSC8 | Stress | 2 | UPF2 / MOV10 | 4 | 0 | 8 | 1 |
Q15910 | EZH2 | Cancer Development | 4 | UPF1 / MAGOH / RUVBL1 / RUVBL2 | 11 | 4 | 12 | 0 |
P25445 | FAS | Cancer | 1 | RUVBL2 | 0 | 0 | 6 | 1 |
Q969H0 | FBXW7 | Cancer | 2 | EIF4A3 / MOV10 | 4 | 1 | 6 | 1 |
P39748 | FEN1 | Cancer | 1 | MOV10 | 11 | 2 | 16 | 1 |
O95684 | FGFR1OP | Cancer | 1 | UPF3A | 1 | 3 | 17 | 1 |
P22607 | FGFR3 | Cancer | 1 | SMG7 | 1 | 1 | 0 | 1 |
P22455 | FGFR4 | Cancer | 1 | CASC3 | 1 | 1 | 5 | 1 |
P49789 | FHIT | Cancer | 1 | UPF1 | 1 | 1 | 4 | 1 |
Q6UN15 | FIP1L1 | Cancer | 1 | RNPS1 | 3 | 1 | 7 | 1 |
P21333 | FLNA | Cancer | 3 | SEC13 / RUVBL1 / RUVBL2 | 0 | 8 | 1 | 1 |
P58012 | FOXL2 | Cancer | 1 | MOV10 | 0 | 0 | 0 | 0 |
Q96AE4 | FUBP1 | Cancer | 1 | PNRC2 | 9 | 2 | 13 | 0 |
P35637 | FUS | Cancer | 8 | UPF1 / UPF2 / UPF3A / UPF3B / RNPS1 / RBM8A / MAGOH / SEC13 | 10 | 2 | 20 | 0 |
P35557 | GCK | Development | 3 | SEC13 / RUVBL1 / RUVBL2 | 0 | 0 | 2 | 1 |
Q06210 | GFPT1 | Stress | 2 | RUVBL1 / RUVBL2 | 3 | 1 | 11 | 1 |
Q9Y2X7 | GIT1 | Development | 1 | RNPS1 | 3 | 1 | 4 | 1 |
Q9HD26 | GOPC | Cancer | 1 | MOV10 | 4 | 0 | 10 | 0 |
P51654 | GPC3 | Cancer | 2 | UPF2 / RNPS1 | 0 | 0 | 0 | 0 |
P78333 | GPC5 | Cancer | 2 | UPF2 / RNPS1 | 0 | 0 | 2 | 0 |
Q96SL4 | GPX7 | Stress | 1 | UPF1 | 0 | 1 | 3 | 1 |
Q8TED1 | GPX8 | Stress | 1 | UPF1 | 1 | 0 | 3 | 0 |
P62993 | GRB2 | Development | 4 | CASC3 / EIF4A3 / RUVBL1 / RUVBL2 | 5 | 2 | 12 | 1 |
P49840 | GSK3A | Stress | 1 | RUVBL2 | 5 | 1 | 13 | 1 |
P49841 | GSK3B | Stress Development | 3 | UPF3A / DHX34 / RUVBL2 | 5 | 4 | 15 | 0 |
P15170 | GSPT1 | Development | 6 | UPF1 / UPF2 / UPF3A / SMG1 / RBM8A / RUVBL1 | 3 | 1 | 17 | 1 |
Q8IYD1 | GSPT2 | Development | 16 | UPF1 / UPF2 / UPF3A / UPF3B / SMG1 / SMG5 / SMG6 / SMG7 / SMG8 / SMG9 / RNPS1 / RBM8A / MAGOH / CASC3 / EIF4A3 / MOV10 | 0 | 1 | 0 | 1 |
P0C5Y9 | H2AFB1 | Development | 2 | RUVBL1 / RUVBL2 | 0 | 0 | 0 | 0 |
Q9BTM1 | H2AFJ | Development | 4 | RBM8A / SEC13 / RUVBL1 / RUVBL2 | 1 | 0 | 8 | 1 |
Q71UI9 | H2AFV | Development | 2 | RUVBL1 / RUVBL2 | 3 | 2 | 24 | 0 |
P16104 | H2AFX | Development | 4 | UPF1 / SEC13 / RUVBL1 / RUVBL2 | 7 | 2 | 24 | 1 |
P0C0S5 | H2AFZ | Development | 2 | RUVBL1 / RUVBL2 | 10 | 0 | 9 | 0 |
P84243 | H3F3A | Cancer Development | 3 | GNL2 / RUVBL1 / RUVBL2 | 6 | 0 | 8 | 0 |
P51858 | HDGF | Stress | 2 | MOV10 / RUVBL1 | 5 | 6 | 16 | 0 |
Q16665 | HIF1A | Cancer Stress | 1 | RUVBL2 | 0 | 2 | 10 | 1 |
P04908 | HIST1H2AB | Development | 4 | SEC13 / MOV10 / RUVBL1 / RUVBL2 | 0 | 1 | 6 | 1 |
Q93077 | HIST1H2AC | Development | 3 | SEC13 / RUVBL1 / RUVBL2 | 0 | 1 | 8 | 1 |
P20671 | HIST1H2AD | Development | 5 | MAGOH / EIF4A3 / SEC13 / RUVBL1 / RUVBL2 | 0 | 1 | 5 | 1 |
Q99878 | HIST1H2AJ | Development | 4 | RBM8A / SEC13 / RUVBL1 / RUVBL2 | 0 | 2 | 3 | 1 |
Q96A08 | HIST1H2BA | Development | 2 | RUVBL1 / RUVBL2 | 0 | 0 | 0 | 1 |
P33778 | HIST1H2BB | Development | 2 | RUVBL1 / RUVBL2 | 0 | 0 | 1 | 1 |
P62807 | HIST1H2BC | Development | 5 | UPF3B / MAGOH / EIF4A3 / RUVBL1 / RUVBL2 | 0 | 2 | 9 | 1 |
P58876 | HIST1H2BD | Development | 2 | RUVBL1 / RUVBL2 | 0 | 4 | 10 | 1 |
Q93079 | HIST1H2BH | Development | 2 | RUVBL1 / RUVBL2 | 0 | 0 | 1 | 1 |
P06899 | HIST1H2BJ | Development | 2 | RUVBL1 / RUVBL2 | 0 | 2 | 13 | 1 |
O60814 | HIST1H2BK | Development | 2 | RUVBL1 / RUVBL2 | 4 | 2 | 12 | 1 |
Q99880 | HIST1H2BL | Development | 2 | RUVBL1 / RUVBL2 | 0 | 1 | 4 | 1 |
Q99879 | HIST1H2BM | Development | 2 | RUVBL1 / RUVBL2 | 0 | 0 | 3 | 1 |
Q99877 | HIST1H2BN | Development | 2 | RUVBL1 / RUVBL2 | 0 | 0 | 5 | 1 |
P23527 | HIST1H2BO | Development | 3 | MOV10 / RUVBL1 / RUVBL2 | 0 | 0 | 7 | 1 |
P68431 | HIST1H3A | Cancer Development | 3 | GNL2 / RUVBL1 / RUVBL2 | 0 | 0 | 3 | 1 |
P62805 | HIST1H4A | Cancer Development | 7 | UPF1 / MAGOH / EIF4A3 / SEC13 / MOV10 / RUVBL1 / RUVBL2 | 3 | 0 | 8 | 0 |
Q6FI13 | HIST2H2AA3 | Development | 3 | SEC13 / RUVBL1 / RUVBL2 | 0 | 3 | 1 | 0 |
Q16777 | HIST2H2AC | Development | 3 | SEC13 / RUVBL1 / RUVBL2 | 0 | 0 | 12 | 1 |
Q16778 | HIST2H2BE | Development | 2 | RUVBL1 / RUVBL2 | 0 | 3 | 9 | 1 |
Q71DI3 | HIST2H3A; | Development | 3 | GNL2 / RUVBL1 / RUVBL2 | 0 | 0 | 0 | 0 |
Q8N257 | HIST3H2BB | Development | 2 | RUVBL1 / RUVBL2 | 1 | 0 | 3 | 1 |
P17096 | HMGA1 | Cancer | 1 | UPF2 | 3 | 6 | 8 | 1 |
P52926 | HMGA2 | Cancer | 6 | RBM8A / MAGOH / EIF4A3 / SEC13 / RUVBL1 / RUVBL2 | 1 | 3 | 4 | 0 |
P41235 | HNF4A | Development | 8 | UPF1 / UPF3B / SMG9 / MAGOH / NBAS / MOV10 / RUVBL2 / PNRC2 | 0 | 0 | 7 | 1 |
Q14541 | HNF4G | Development | 1 | PNRC2 | 0 | 0 | 0 | 1 |
P22626 | HNRNPA2B1 | Cancer | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 6 | 4 | 20 | 1 |
P09016 | HOXD4 | Development | 1 | RNPS1 | 0 | 0 | 0 | 1 |
P07900 | HSP90AA1 | Cancer Stress Development | 7 | SMG1 / SMG5 / SMG6 / SEC13 / GNL2 / RUVBL1 / RUVBL2 | 7 | 4 | 13 | 1 |
P08238 | HSP90AB1 | Cancer Stress Development | 9 | UPF1 / UPF2 / EIF4A3 / DHX34 / SEC13 / GNL2 / MOV10 / RUVBL1 / RUVBL2 | 3 | 5 | 16 | 1 |
P14625 | HSP90B1 | Stress | 2 | SMG1 / RUVBL2 | 1 | 3 | 12 | 1 |
P0DMV8 | HSPA1A | Stress | 8 | UPF1 / MAGOH / EIF4A3 / SEC13 / GNL2 / MOV10 / RUVBL1 / RUVBL2 | 0 | 1 | 1 | 1 |
P0DMV9 | HSPA1B | Stress | 9 | UPF1 / UPF2 / MAGOH / EIF4A3 / SEC13 / GNL2 / MOV10 / RUVBL1 / RUVBL2 | 0 | 8 | 3 | 1 |
P34931 | HSPA1L | Stress | 7 | UPF1 / UPF2 / EIF4A3 / SEC13 / GNL2 / RUVBL1 / RUVBL2 | 1 | 2 | 0 | 1 |
P54652 | HSPA2 | Stress | 7 | UPF1 / UPF2 / EIF4A3 / SEC13 / GNL2 / RUVBL1 / RUVBL2 | 2 | 1 | 7 | 1 |
P34932 | HSPA4 | Stress | 7 | UPF1 / UPF2 / SMG1 / GNL2 / MOV10 / RUVBL1 / RUVBL2 | 11 | 2 | 14 | 0 |
O95757 | HSPA4L | Stress | 6 | UPF1 / UPF2 / MAGOH / GNL2 / RUVBL1 / RUVBL2 | 2 | 2 | 8 | 0 |
P11021 | HSPA5 | Stress | 4 | GNL2 / MOV10 / RUVBL1 / RUVBL2 | 0 | 1 | 15 | 1 |
P17066 | HSPA6 | Stress | 7 | UPF1 / UPF2 / EIF4A3 / SEC13 / GNL2 / RUVBL1 / RUVBL2 | 0 | 0 | 2 | 1 |
P11142 | HSPA8 | Stress Development | 9 | UPF1 / UPF2 / RNPS1 / MAGOH / EIF4A3 / SEC13 / GNL2 / RUVBL1 / RUVBL2 | 4 | 7 | 16 | 1 |
P38646 | HSPA9 | Stress | 7 | MAGOH / EIF4A3 / DHX34 / GNL2 / MOV10 / RUVBL1 / RUVBL2 | 10 | 2 | 19 | 1 |
Q92598 | HSPH1 | Stress | 5 | UPF1 / UPF2 / GNL2 / RUVBL1 / RUVBL2 | 5 | 3 | 11 | 0 |
Q9Y4L1 | HYOU1 | Stress | 1 | MOV10 | 2 | 4 | 15 | 1 |
O75874 | IDH1 | Cancer | 2 | UPF1 / MOV10 | 0 | 0 | 10 | 1 |
P48735 | IDH2 | Cancer | 1 | UPF1 | 0 | 1 | 8 | 1 |
Q13422 | IKZF1 | Cancer | 1 | MAGOHB | 3 | 1 | 12 | 1 |
P56199 | ITGA1 | Development | 1 | MAGOH | 0 | 0 | 5 | 0 |
P23458 | JAK1 | Cancer | 2 | MAGOH / EIF4A3 | 2 | 1 | 10 | 1 |
P52333 | JAK3 | Cancer | 1 | RNPS1 | 1 | 0 | 3 | 0 |
Q86VZ6 | JAZF1 | Cancer | 1 | RUVBL1 | 1 | 0 | 1 | 0 |
P05412 | JUN | Cancer Development | 8 | UPF1 / UPF2 / UPF3B / RNPS1 / EIF4A3 / MOV10 / RUVBL1 / RUVBL2 | 0 | 3 | 11 | 1 |
Q92794 | KAT6A | Cancer | 1 | RNPS1 | 5 | 2 | 16 | 0 |
Q8WYB5 | KAT6B | Cancer | 2 | RUVBL1 / RUVBL2 | 2 | 0 | 10 | 0 |
P29375 | KDM5A | Cancer | 1 | RBM8A | 7 | 0 | 11 | 1 |
O95239 | KIF4A | Development | 1 | MOV10 | 2 | 2 | 4 | 1 |
P33176 | KIF5B | Cancer | 1 | EIF4A3 | 2 | 2 | 11 | 0 |
Q9BQ90 | KLHDC3 | Stress | 1 | MOV10 | 1 | 2 | 8 | 0 |
Q8NG31 | KNL1 | Cancer | 2 | SEC13 / RUVBL1 | 2 | 0 | 0 | 0 |
Q9Y448 | KNSTRN | Cancer | 1 | MOV10 | 8 | 1 | 3 | 0 |
P04264 | KRT1 | Development | 2 | MAGOH / EIF4A3 | 0 | 0 | 0 | 1 |
P13645 | KRT10 | Development | 2 | MAGOH / EIF4A3 | 0 | 1 | 1 | 0 |
P02533 | KRT14 | Development | 2 | MAGOH / EIF4A3 | 0 | 0 | 0 | 1 |
P08779 | KRT16 | Development | 1 | EIF4A3 | 0 | 0 | 1 | 1 |
P05783 | KRT18 | Development | 1 | UPF2 | 0 | 1 | 4 | 1 |
P08727 | KRT19 | Development | 2 | MAGOH / EIF4A3 | 0 | 1 | 3 | 1 |
P35908 | KRT2 | Development | 2 | MAGOH / EIF4A3 | 0 | 0 | 1 | 1 |
O76011 | KRT34 | Development | 1 | SMG9 | 1 | 0 | 1 | 1 |
P13647 | KRT5 | Development | 2 | MAGOH / EIF4A3 | 0 | 0 | 2 | 1 |
P04259 | KRT6B | Development | 1 | EIF4A3 | 0 | 0 | 0 | 1 |
Q3SY84 | KRT71 | Development | 1 | EIF4A3 | 0 | 0 | 0 | 1 |
O95678 | KRT75 | Development | 2 | MAGOHB / EIF4A3 | 0 | 0 | 0 | 1 |
P35527 | KRT9 | Development | 2 | MAGOH / EIF4A3 | 0 | 0 | 0 | 1 |
Q07627 | KRTAP1–1 | Development | 1 | MAGOHB | 1 | 0 | 0 | 0 |
Q52LG2 | KRTAP13–2 | Development | 1 | MAGOHB | 0 | 0 | 0 | 0 |
Q3LI66 | KRTAP6–2 | Development | 1 | CASC3 | 0 | 0 | 0 | 0 |
Q9UJU2 | LEF1 | Cancer | 1 | RUVBL1 | 1 | 1 | 0 | 1 |
P53671 | LIMK2 | Development | 1 | RUVBL2 | 2 | 0 | 8 | 1 |
Q9H9Z2 | LIN28A | Development | 2 | UPF1 / MOV10 | 0 | 2 | 0 | 1 |
P02545 | LMNA | Cancer Stress | 4 | SMG1 / GNL2 / MOV10 / RUVBL1 | 0 | 1 | 13 | 1 |
Q8N653 | LZTR1 | Cancer | 2 | EIF4A3 / RUVBL1 | 5 | 0 | 19 | 1 |
P36507 | MAP2K2 | Cancer Development | 2 | RUVBL1 / RUVBL2 | 5 | 1 | 7 | 1 |
P28482 | MAPK1 | Cancer Stress Development | 3 | UPF1 / RUVBL1 / RUVBL2 | 6 | 2 | 20 | 1 |
P27361 | MAPK3 | Stress Development | 3 | UPF1 / RUVBL1 / RUVBL2 | 2 | 0 | 2 | 1 |
P49137 | MAPKAPK2 | Stress | 1 | MOV10 | 1 | 3 | 1 | 1 |
Q14703 | MBTPS1 | Stress | 1 | MOV10 | 5 | 1 | 13 | 1 |
Q93074 | MED12 | Cancer Development | 1 | CASC3 | 7 | 1 | 0 | 0 |
Q9UHV7 | MED13 | Development | 1 | PNRC2 | 8 | 2 | 1 | 0 |
Q71F56 | MED13L | Development | 1 | PNRC2 | 2 | 2 | 3 | 1 |
A0JLT2 | MED19 | Development | 2 | RNPS1 / RUVBL1 | 5 | 1 | 8 | 1 |
Q9H204 | MED28 | Development | 1 | MOV10 | 9 | 2 | 2 | 0 |
Q9NX70 | MED29 | Development | 1 | MOV10 | 5 | 1 | 11 | 1 |
Q9Y3C7 | MED31 | Development | 1 | MOV10 | 6 | 1 | 4 | 0 |
Q9NPJ6 | MED4 | Development | 2 | RNPS1 / SEC13 | 6 | 0 | 8 | 0 |
Q96G25 | MED8 | Development | 1 | MOV10 | 5 | 2 | 8 | 1 |
Q14814 | MEF2D | Development | 1 | MOV10 | 2 | 4 | 14 | 1 |
P40692 | MLH1 | Cancer | 2 | RUVBL1 / RUVBL2 | 3 | 0 | 18 | 1 |
Q9BVC4 | MLST8 | Stress | 4 | SEC13 / GNL2 / MOV10 / RUVBL2 | 8 | 0 | 14 | 1 |
P43246 | MSH2 | Cancer | 2 | RUVBL1 / RUVBL2 | 10 | 1 | 15 | 0 |
P52701 | MSH6 | Cancer | 1 | RUVBL2 | 10 | 4 | 12 | 0 |
P42345 | MTOR | Cancer Stress | 7 | UPF1 / UPF3B / SMG1 / EIF4A3 / MOV10 / RUVBL1 / RUVBL2 | 10 | 1 | 6 | 1 |
P10242 | MYB | Cancer | 1 | UPF2 | 1 | 2 | 7 | 1 |
P12524 | MYCL | Cancer | 2 | RUVBL1 / RUVBL2 | 0 | 0 | 1 | 0 |
Q969H8 | MYDGF | Stress | 1 | MOV10 | 3 | 0 | 0 | 0 |
P35580 | MYH10 | Development | 3 | MAGOH / EIF4A3 / RUVBL2 | 1 | 0 | 3 | 1 |
Q7Z406 | MYH14 | Development | 1 | RUVBL2 | 0 | 3 | 1 | 1 |
P35579 | MYH9 | Cancer Development | 3 | MAGOH / EIF4A3 / RUVBL2 | 1 | 7 | 16 | 1 |
Q9H9S0 | NANOG | Development | 4 | SEC13 / MOV10 / RUVBL1 / RUVBL2 | 3 | 0 | 1 | 1 |
O60934 | NBN | Cancer | 1 | CASC3 | 4 | 0 | 17 | 0 |
Q09161 | NCBP1 | Development | 16 | UPF1 / UPF2 / UPF3A / UPF3B / SMG1 / SMG5 / SMG6 / SMG7 / SMG8 / SMG9 / RNPS1 / RBM8A / MAGOH / CASC3 / EIF4A3 / RUVBL1 | 1 | 1 | 15 | 0 |
P52298 | NCBP2 | Development | 15 | UPF1 / UPF2 / UPF3A / UPF3B / SMG1 / SMG5 / SMG6 / SMG7 / SMG8 / SMG9 / RNPS1 / RBM8A / MAGOH / CASC3 / EIF4A3 | 9 | 1 | 24 | 0 |
Q92597 | NDRG1 | Cancer | 2 | UPF1 / RUVBL2 | 0 | 1 | 19 | 1 |
Q00653 | NFKB2 | Cancer | 3 | MOV10 / RUVBL1 / RUVBL2 | 3 | 1 | 13 | 1 |
O00221 | NFKBIE | Cancer | 1 | RUVBL2 | 0 | 1 | 5 | 1 |
P23511 | NFYA | Stress | 1 | MOV10 | 3 | 0 | 16 | 0 |
Q8N4C6 | NIN | Cancer | 1 | UPF1 | 3 | 2 | 6 | 0 |
Q15155 | NOMO1 | Development | 1 | UPF2 | 2 | 0 | 1 | 1 |
Q5JPE7 | NOMO2 | Development | 1 | MOV10 | 1 | 0 | 1 | 1 |
Q15233 | NONO | Cancer | 1 | RNPS1 | 11 | 4 | 9 | 0 |
P06748 | NPM1 | Cancer | 6 | UPF1 / EIF4A3 / GNL2 / MOV10 / RUVBL1 / RUVBL2 | 8 | 3 | 19 | 0 |
Q13285 | NR5A1 | Development | 2 | EIF4A3 / PNRC2 | 1 | 0 | 2 | 0 |
O00482 | NR5A2 | Development | 1 | PNRC2 | 0 | 0 | 1 | 1 |
O96028 | NSD2 | Cancer | 1 | RUVBL2 | 7 | 0 | 0 | 0 |
P78549 | NTHL1 | Cancer | 2 | MOV10 / RUVBL2 | 10 | 3 | 18 | 1 |
O95631 | NTN1 | Development | 6 | UPF1 / SMG5 / EIF4A3 / DHX34 / GNL2 / RUVBL2 | 0 | 0 | 0 | 0 |
O00634 | NTN3 | Development | 6 | UPF1 / SMG5 / EIF4A3 / DHX34 / GNL2 / RUVBL2 | 0 | 0 | 1 | 0 |
Q9HB63 | NTN4 | Development | 1 | MOV10 | 0 | 0 | 1 | 1 |
P04629 | NTRK1 | Cancer | 9 | UPF1 / UPF2 / SMG8 / EIF4A3 / GNL2 / NBAS / MOV10 / RUVBL1 / RUVBL2 | 0 | 0 | 4 | 1 |
Q14980 | NUMA1 | Cancer | 2 | MOV10 / RUVBL1 | 5 | 0 | 13 | 1 |
P57740 | NUP107 | Stress | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / SEC13 | 8 | 1 | 16 | 0 |
Q8WUM0 | NUP133 | Stress | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / SEC13 | 2 | 0 | 13 | 0 |
P49790 | NUP153 | Stress | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 8 | 3 | 19 | 0 |
O75694 | NUP155 | Stress | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 5 | 4 | 12 | 0 |
Q12769 | NUP160 | Stress | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / SEC13 | 10 | 1 | 4 | 0 |
Q5SRE5 | NUP188 | Stress | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 10 | 1 | 8 | 1 |
Q92621 | NUP205 | Stress | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / MOV10 | 10 | 2 | 24 | 0 |
Q8TEM1 | NUP210 | Stress | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 8 | 1 | 8 | 1 |
P35658 | NUP214 | Cancer Stress | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 5 | 3 | 18 | 1 |
Q8NFH5 | NUP35 | Stress | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 2 | 2 | 10 | 0 |
Q8NFH4 | NUP37 | Stress | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / SEC13 | 2 | 1 | 4 | 0 |
Q8NFH3 | NUP43 | Stress | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / SEC13 | 2 | 2 | 5 | 0 |
Q9UKX7 | NUP50 | Stress | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 6 | 3 | 13 | 1 |
Q7Z3B4 | NUP54 | Stress | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 10 | 1 | 9 | 0 |
Q9BVL2 | NUP58 | Stress | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 8 | 0 | 0 | 0 |
P37198 | NUP62 | Stress | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / EIF4A3 | 2 | 1 | 19 | 1 |
Q9BW27 | NUP85 | Stress | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / SEC13 | 12 | 0 | 12 | 1 |
Q99567 | NUP88 | Stress | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 8 | 0 | 13 | 1 |
Q8N1F7 | NUP93 | Stress | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / GNL2 | 9 | 0 | 6 | 1 |
P52948 | NUP98 | Cancer Stress | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / SEC13 | 3 | 2 | 20 | 1 |
O15504 | NUPL2 | Stress | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 8 | 0 | 11 | 0 |
P07237 | P4HB | Stress | 2 | RBM8A / RUVBL2 | 1 | 3 | 1 | 1 |
P11940 | PABPC1 | Cancer Development | 18 | UPF1 / UPF2 / UPF3A / UPF3B / SMG1 / SMG5 / SMG6 / SMG7 / SMG8 / SMG9 / RNPS1 / RBM8A / MAGOH / CASC3 / EIF4A3 / MOV10 / RUVBL1 / RUVBL2 | 4 | 2 | 12 | 1 |
O75914 | PAK3 | Development | 1 | SMG6 | 0 | 0 | 0 | 1 |
Q86YC2 | PALB2 | Cancer | 1 | MOV10 | 4 | 0 | 16 | 0 |
O95453 | PARN | Stress | 4 | UPF1 / UPF2 / UPF3A / UPF3B | 2 | 0 | 5 | 1 |
P23759 | PAX7 | Cancer | 1 | MAGOHB | 0 | 0 | 1 | 0 |
Q86U86 | PBRM1 | Cancer | 1 | RUVBL1 | 6 | 2 | 8 | 0 |
Q15365 | PCBP1 | Cancer | 6 | UPF3B / RNPS1 / RBM8A / MAGOH / RUVBL1 / RUVBL2 | 5 | 0 | 7 | 0 |
P35227 | PCGF2 | Development | 1 | MOV10 | 0 | 0 | 1 | 1 |
Q15154 | PCM1 | Cancer | 2 | SMG5 / SMG7 | 4 | 0 | 17 | 1 |
P01127 | PDGFB | Cancer | 1 | GNL2 | 0 | 2 | 0 | 1 |
P16234 | PDGFRA | Cancer | 1 | RNPS1 | 0 | 3 | 1 | 1 |
Q8IWS0 | PHF6 | Cancer | 1 | MAGOH | 7 | 1 | 1 | 0 |
Q13492 | PICALM | Cancer | 1 | SEC13 | 2 | 0 | 17 | 0 |
O60331 | PIP5K1C | Development | 1 | MOV10 | 1 | 3 | 3 | 1 |
P30613 | PKLR | Development | 2 | EIF4A3 / GNL2 | 1 | 0 | 3 | 1 |
P55347 | PKNOX1 | Development | 1 | MOV10 | 0 | 1 | 12 | 1 |
Q9Y446 | PKP3 | Development | 1 | RBM8A | 0 | 0 | 0 | 1 |
Q99569 | PKP4 | Development | 1 | MOV10 | 4 | 0 | 6 | 1 |
P29590 | PML | Cancer | 1 | RBM8A | 2 | 0 | 4 | 1 |
P54277 | PMS1 | Cancer | 1 | MOV10 | 7 | 1 | 10 | 0 |
P54278 | PMS2 | Cancer | 2 | RUVBL1 / RUVBL2 | 7 | 0 | 8 | 0 |
P28340 | POLD1 | Cancer | 2 | UPF1 / UPF2 | 9 | 1 | 9 | 1 |
Q07864 | POLE | Cancer | 1 | UPF1 | 8 | 4 | 16 | 1 |
P24928 | POLR2A | Development | 8 | UPF1 / UPF3B / RNPS1 / RBM8A / MAGOH / MOV10 / RUVBL1 / RUVBL2 | 7 | 5 | 22 | 1 |
P30876 | POLR2B | Development | 7 | UPF3B / RNPS1 / RBM8A / MAGOH / GNL2 / RUVBL1 / RUVBL2 | 9 | 1 | 2 | 1 |
P19387 | POLR2C | Development | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / RUVBL2 | 6 | 2 | 5 | 1 |
O15514 | POLR2D | Development | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 8 | 1 | 11 | 1 |
P19388 | POLR2E | Development | 8 | UPF3B / SMG1 / RNPS1 / RBM8A / MAGOH / SEC13 / RUVBL1 / RUVBL2 | 7 | 1 | 13 | 1 |
P61218 | POLR2F | Development | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 7 | 1 | 4 | 1 |
P62487 | POLR2G | Development | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 9 | 1 | 8 | 1 |
P52434 | POLR2H | Development | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / RUVBL2 | 7 | 2 | 10 | 1 |
P36954 | POLR2I | Development | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 6 | 1 | 8 | 1 |
P52435 | POLR2J | Development | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / RUVBL1 | 2 | 0 | 1 | 1 |
P53803 | POLR2K | Development | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / MOV10 | 8 | 0 | 8 | 0 |
P62875 | POLR2L | Development | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / RUVBL2 | 2 | 3 | 12 | 1 |
Q96HA1 | POM121 | Stress | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 7 | 4 | 4 | 1 |
Q86W92 | PPFIBP1 | Cancer | 1 | MOV10 | 0 | 0 | 6 | 0 |
P30153 | PPP2R1A | Cancer | 17 | UPF1 / UPF2 / UPF3A / UPF3B / SMG1 / SMG5 / SMG6 / SMG7 / SMG8 / SMG9 / RNPS1 / RBM8A / MAGOH / CASC3 / EIF4A3 / GNL2 / RUVBL1 | 6 | 3 | 10 | 1 |
Q15173 | PPP2R5B | Stress | 1 | RUVBL1 | 0 | 0 | 6 | 1 |
P16298 | PPP3CB | Development | 1 | RUVBL2 | 0 | 0 | 7 | 1 |
Q06830 | PRDX1 | Stress | 2 | MAGOH / EIF4A3 | 6 | 1 | 16 | 1 |
P32119 | PRDX2 | Stress | 2 | RUVBL1 / RUVBL2 | 2 | 1 | 8 | 1 |
Q6NWY9 | PRPF40B | Cancer | 1 | RUVBL2 | 4 | 1 | 7 | 1 |
O75475 | PSIP1 | Cancer | 2 | EIF4A3 / PNRC2 | 6 | 1 | 13 | 0 |
P25788 | PSMA3 | Stress Development | 2 | RUVBL1 / RUVBL2 | 8 | 0 | 12 | 1 |
P20618 | PSMB1 | Stress Development | 2 | RBM8A / SEC13 | 8 | 1 | 7 | 1 |
P49721 | PSMB2 | Stress Development | 2 | GNL2 / RUVBL2 | 11 | 0 | 6 | 1 |
P49720 | PSMB3 | Stress Development | 2 | GNL2 / RUVBL2 | 0 | 0 | 17 | 1 |
P62191 | PSMC1 | Stress Development | 2 | RUVBL1 / RUVBL2 | 2 | 2 | 2 | 1 |
P35998 | PSMC2 | Stress Development | 2 | RUVBL1 / RUVBL2 | 5 | 2 | 1 | 1 |
P17980 | PSMC3 | Stress Development | 3 | MOV10 / RUVBL1 / RUVBL2 | 2 | 1 | 12 | 1 |
P43686 | PSMC4 | Stress Development | 3 | MOV10 / RUVBL1 / RUVBL2 | 10 | 4 | 17 | 1 |
P62195 | PSMC5 | Stress Development | 3 | GNL2 / RUVBL1 / RUVBL2 | 9 | 2 | 17 | 1 |
P62333 | PSMC6 | Stress Development | 2 | RUVBL1 / RUVBL2 | 6 | 1 | 9 | 0 |
Q99460 | PSMD1 | Stress Development | 4 | GNL2 / MOV10 / RUVBL1 / RUVBL2 | 9 | 1 | 6 | 1 |
O75832 | PSMD10 | Stress Development | 2 | RUVBL1 / RUVBL2 | 8 | 1 | 3 | 0 |
O00231 | PSMD11 | Stress Development | 2 | RUVBL1 / RUVBL2 | 8 | 6 | 13 | 0 |
O00232 | PSMD12 | Stress Development | 3 | UPF1 / RUVBL1 / RUVBL2 | 1 | 1 | 11 | 1 |
Q9UNM6 | PSMD13 | Stress Development | 2 | RUVBL1 / RUVBL2 | 8 | 1 | 3 | 1 |
O00487 | PSMD14 | Stress Development | 5 | UPF1 / SEC13 / GNL2 / RUVBL1 / RUVBL2 | 10 | 0 | 9 | 0 |
Q13200 | PSMD2 | Stress Development | 4 | GNL2 / MOV10 / RUVBL1 / RUVBL2 | 6 | 3 | 15 | 1 |
O43242 | PSMD3 | Stress Development | 3 | MOV10 / RUVBL1 / RUVBL2 | 5 | 1 | 21 | 1 |
Q15008 | PSMD6 | Stress Development | 2 | RUVBL1 / RUVBL2 | 3 | 1 | 9 | 1 |
P51665 | PSMD7 | Stress Development | 2 | RUVBL1 / RUVBL2 | 10 | 2 | 12 | 1 |
P48556 | PSMD8 | Stress Development | 2 | GNL2 / RUVBL2 | 5 | 2 | 11 | 1 |
P61289 | PSME3 | Stress Development | 2 | RNPS1 / MOV10 | 8 | 5 | 10 | 1 |
Q15185 | PTGES3 | Stress | 2 | SMG5 / SMG6 | 9 | 1 | 22 | 0 |
P78406 | RAE1 | Stress | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / SEC13 | 9 | 1 | 12 | 1 |
P49792 | RANBP2 | Cancer Stress | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / SEC13 | 2 | 1 | 15 | 0 |
Q96S59 | RANBP9 | Development | 1 | RNPS1 | 2 | 0 | 7 | 0 |
P52306 | RAP1GDS1 | Cancer | 1 | MOV10 | 3 | 0 | 4 | 0 |
P10276 | RARA | Cancer Development | 2 | RUVBL1 / PNRC2 | 2 | 2 | 5 | 1 |
P13631 | RARG | Development | 1 | PNRC2 | 1 | 0 | 0 | 1 |
Q09028 | RBBP4 | Development | 2 | RUVBL1 / RUVBL2 | 10 | 1 | 19 | 0 |
Q16576 | RBBP7 | Development | 2 | RUVBL1 / RUVBL2 | 3 | 2 | 3 | 1 |
P98175 | RBM10 | Cancer | 5 | MAGOH / EIF4A3 / MOV10 / RUVBL1 / RUVBL2 | 8 | 3 | 3 | 1 |
Q96T37 | RBM15 | Cancer | 1 | UPF1 | 8 | 0 | 16 | 1 |
Q04864 | REL | Cancer | 3 | SMG9 / MAGOHB / EIF4A3 | 3 | 2 | 7 | 1 |
Q04206 | RELA | Development | 2 | RUVBL1 / RUVBL2 | 3 | 1 | 14 | 0 |
Q6PCD5 | RFWD3 | Cancer | 1 | MOV10 | 12 | 2 | 7 | 0 |
A6NKT7 | RGPD3 | Cancer | 1 | SEC13 | 2 | 0 | 0 | 0 |
P62745 | RHOB | Development | 1 | SEC13 | 0 | 1 | 9 | 0 |
P08134 | RHOC | Development | 1 | SEC13 | 1 | 1 | 4 | 1 |
P27694 | RPA1 | Stress | 3 | MOV10 / RUVBL1 / RUVBL2 | 5 | 1 | 8 | 0 |
P15927 | RPA2 | Stress | 2 | MOV10 / RUVBL2 | 4 | 2 | 16 | 0 |
P35244 | RPA3 | Stress | 2 | MOV10 / RUVBL2 | 9 | 2 | 6 | 0 |
P04843 | RPN1 | Cancer | 2 | SEC13 / RUVBL1 | 7 | 1 | 4 | 1 |
Q9UK32 | RPS6KA6 | Development | 1 | DHX34 | 0 | 1 | 1 | 1 |
Q8N122 | RPTOR | Stress | 3 | MOV10 / RUVBL1 / RUVBL2 | 9 | 0 | 9 | 1 |
P19793 | RXRA | Development | 1 | PNRC2 | 2 | 0 | 0 | 1 |
Q9NSC2 | SALL1 | Development | 1 | RUVBL2 | 0 | 2 | 1 | 1 |
Q9UJQ4 | SALL4 | Cancer Development | 1 | RUVBL2 | 3 | 0 | 3 | 0 |
P21912 | SDHB | Cancer | 1 | RUVBL2 | 5 | 1 | 2 | 1 |
Q99643 | SDHC | Cancer | 1 | UPF1 | 2 | 2 | 5 | 0 |
O94979 | SEC31A | Stress | 2 | SEC13 / MOV10 | 5 | 2 | 14 | 1 |
P61619 | SEC61A1 | Stress | 2 | UPF3B / MOV10 | 4 | 3 | 13 | 1 |
Q96EE3 | SEH1L | Stress | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / SEC13 | 12 | 1 | 18 | 1 |
Q99719 | SEPT5 | Cancer | 1 | RUVBL2 | 0 | 0 | 12 | 0 |
Q14141 | SEPT6 | Cancer | 1 | DHX34 | 1 | 0 | 2 | 0 |
O75533 | SF3B1 | Cancer | 8 | UPF1 / UPF3B / RNPS1 / RBM8A / MAGOH / EIF4A3 / MOV10 / RUVBL2 | 8 | 2 | 12 | 0 |
P23246 | SFPQ | Cancer | 2 | RNPS1 / MOV10 | 9 | 4 | 10 | 1 |
Q96B97 | SH3KBP1 | Development | 1 | MOV10 | 0 | 0 | 1 | 1 |
P29353 | SHC1 | Stress Development | 3 | MOV10 / RUVBL1 / RUVBL2 | 2 | 0 | 13 | 0 |
Q12824 | SMARCB1 | Cancer | 2 | EIF4A3 / RUVBL1 | 10 | 1 | 7 | 1 |
Q96GM5 | SMARCD1 | Cancer | 2 | UPF2 / RUVBL1 | 8 | 1 | 5 | 1 |
Q6STE5 | SMARCD3 | Development | 2 | UPF2 / RUVBL1 | 0 | 0 | 2 | 1 |
Q969G3 | SMARCE1 | Cancer | 1 | MOV10 | 6 | 1 | 10 | 0 |
Q14683 | SMC1A | Cancer | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / RUVBL2 | 10 | 3 | 11 | 0 |
Q8TEQ0 | SNX29 | Cancer | 1 | MAGOH | 1 | 0 | 5 | 1 |
P04179 | SOD2 | Stress | 2 | GNL2 / RUVBL2 | 0 | 3 | 14 | 0 |
P48431 | SOX2 | Cancer Development | 3 | SMG6 / RUVBL1 / RUVBL2 | 2 | 0 | 2 | 0 |
O60271 | SPAG9 | Development | 1 | PNRC2 | 5 | 3 | 9 | 1 |
Q13813 | SPTAN1 | Development | 2 | MAGOH / EIF4A3 | 1 | 1 | 5 | 1 |
Q01082 | SPTBN1 | Development | 3 | RBM8A / MAGOH / EIF4A3 | 0 | 4 | 9 | 0 |
P36956 | SREBF1 | Development | 2 | SEC13 / RUVBL2 | 2 | 1 | 1 | 1 |
Q12772 | SREBF2 | Development | 1 | SEC13 | 5 | 3 | 19 | 1 |
Q01130 | SRSF2 | Cancer | 6 | UPF3B / RNPS1 / RBM8A / MAGOH / EIF4A3 / RUVBL1 | 11 | 2 | 16 | 0 |
P84103 | SRSF3 | Cancer | 5 | UPF3B / RNPS1 / RBM8A / MAGOH / EIF4A3 | 12 | 1 | 19 | 1 |
P43307 | SSR1 | Stress | 1 | RUVBL2 | 3 | 3 | 11 | 0 |
P40763 | STAT3 | Cancer Development | 2 | RBM8A / MOV10 | 2 | 3 | 16 | 1 |
Q15468 | STIL | Cancer | 3 | UPF1 / SMG7 / SMG9 | 9 | 1 | 9 | 0 |
Q16623 | STX1A | Development | 1 | SEC13 | 0 | 1 | 0 | 1 |
P61266 | STX1B | Development | 1 | SEC13 | 0 | 0 | 0 | 1 |
Q15022 | SUZ12 | Cancer Development | 6 | UPF1 / RNPS1 / RBM8A / MAGOH / EIF4A3 / RUVBL2 | 9 | 0 | 7 | 0 |
Q93075 | TATDN2 | Stress | 1 | MOV10 | 5 | 2 | 11 | 1 |
Q9BZK7 | TBL1XR1 | Cancer Development | 1 | RUVBL2 | 5 | 2 | 8 | 0 |
Q99081 | TCF12 | Cancer Development | 2 | RBM8A / MOV10 | 1 | 1 | 19 | 0 |
P15923 | TCF3 | Cancer Development | 2 | RUVBL1 / RUVBL2 | 6 | 2 | 6 | 0 |
P15884 | TCF4 | Development | 1 | MAGOHB | 0 | 1 | 8 | 1 |
Q9NQB0 | TCF7L2 | Cancer | 2 | MAGOHB / RUVBL1 | 4 | 2 | 4 | 1 |
O14746 | TERT | Cancer | 5 | UPF1 / SMG5 / SMG6 / RUVBL1 / RUVBL2 | 0 | 1 | 7 | 1 |
Q92734 | TFG | Cancer | 1 | SEC13 | 3 | 3 | 9 | 1 |
P0C1Z6 | TFPT | Cancer | 2 | RUVBL1 / RUVBL2 | 4 | 1 | 15 | 1 |
Q96RS0 | TGS1 | Development | 1 | MAGOH | 7 | 0 | 19 | 0 |
Q9Y2W1 | THRAP3 | Cancer Development | 6 | UPF3B / RNPS1 / RBM8A / MAGOH / CASC3 / EIF4A3 | 8 | 4 | 21 | 1 |
Q92956 | TNFRSF14 | Cancer | 1 | RUVBL2 | 2 | 0 | 7 | 1 |
P04637 | TP53 | Cancer | 4 | SMG1 / SMG5 / SMG7 / MOV10 | 4 | 2 | 20 | 1 |
Q9H3D4 | TP63 | Cancer | 1 | UPF2 | 0 | 1 | 3 | 0 |
P06753 | TPM3 | Cancer | 1 | MOV10 | 3 | 4 | 12 | 1 |
P12270 | TPR | Cancer Stress | 8 | UPF1 / UPF3B / RNPS1 / RBM8A / MAGOH / SEC13 / GNL2 / RUVBL2 | 8 | 1 | 19 | 1 |
P14373 | TRIM27 | Cancer | 3 | SMG9 / MAGOHB / EIF4A3 | 13 | 0 | 1 | 1 |
Q9UPN9 | TRIM33 | Cancer | 1 | RUVBL1 | 3 | 0 | 15 | 0 |
Q9Y4A5 | TRRAP | Cancer | 3 | SMG1 / RUVBL1 / RUVBL2 | 11 | 1 | 10 | 0 |
Q92574 | TSC1 | Cancer | 1 | MOV10 | 2 | 2 | 7 | 1 |
Q71U36 | TUBA1A | Development | 5 | SMG1 / SEC13 / GNL2 / RUVBL1 / RUVBL2 | 0 | 3 | 2 | 1 |
P68363 | TUBA1B | Development | 5 | MAGOH / SEC13 / GNL2 / RUVBL1 / RUVBL2 | 2 | 6 | 9 | 1 |
Q13748 | TUBA3C | Development | 4 | SEC13 / GNL2 / RUVBL1 / RUVBL2 | 1 | 0 | 0 | 1 |
Q6PEY2 | TUBA3E | Development | 4 | SEC13 / GNL2 / RUVBL1 / RUVBL2 | 0 | 0 | 0 | 1 |
P68366 | TUBA4A | Development | 6 | RNPS1 / SEC13 / GNL2 / MOV10 / RUVBL1 / RUVBL2 | 0 | 0 | 2 | 1 |
Q9NY65 | TUBA8 | Development | 4 | SEC13 / GNL2 / RUVBL1 / RUVBL2 | 1 | 0 | 1 | 1 |
A6NHL2 | TUBAL3 | Development | 3 | GNL2 / RUVBL1 / RUVBL2 | 1 | 0 | 0 | 1 |
Q9H4B7 | TUBB1 | Development | 4 | EIF4A3 / GNL2 / RUVBL1 / RUVBL2 | 3 | 0 | 1 | 1 |
Q13885 | TUBB2A | Development | 5 | UPF2 / EIF4A3 / GNL2 / RUVBL1 / RUVBL2 | 0 | 3 | 2 | 1 |
Q9BVA1 | TUBB2B | Development | 4 | EIF4A3 / GNL2 / RUVBL1 / RUVBL2 | 1 | 3 | 1 | 1 |
Q13509 | TUBB3 | Development | 4 | EIF4A3 / GNL2 / RUVBL1 / RUVBL2 | 0 | 3 | 0 | 1 |
P04350 | TUBB4A | Development | 4 | EIF4A3 / GNL2 / RUVBL1 / RUVBL2 | 0 | 0 | 0 | 1 |
P68371 | TUBB4B | Development | 4 | EIF4A3 / GNL2 / RUVBL1 / RUVBL2 | 8 | 3 | 5 | 1 |
Q9BUF5 | TUBB6 | Development | 5 | EIF4A3 / GNL2 / MOV10 / RUVBL1 / RUVBL2 | 1 | 0 | 6 | 1 |
Q3ZCM7 | TUBB8 | Development | 4 | EIF4A3 / GNL2 / RUVBL1 / RUVBL2 | 0 | 0 | 0 | 1 |
Q99757 | TXN2 | Stress | 1 | MOV10 | 4 | 2 | 7 | 1 |
Q01081 | U2AF1 | Cancer | 4 | UPF3B / RNPS1 / RBM8A / MAGOH | 9 | 0 | 14 | 1 |
P62987 | UBA52 | Stress Development | 18 | UPF1 / UPF2 / UPF3A / UPF3B / SMG1 / SMG5 / SMG6 / SMG7 / SMG8 / SMG9 / RNPS1 / RBM8A / MAGOH / CASC3 / EIF4A3 / MOV10 / RUVBL1 / RUVBL2 | 2 | 2 | 20 | 1 |
P0CG48 | UBC | Stress Development | 23 | UPF1 / UPF2 / UPF3B / SMG1 / SMG5 / SMG6 / SMG7 / SMG8 / SMG9 / RNPS1 / RBM8A / MAGOH / MAGOHB / CASC3 / EIF4A3 / DHX34 / SEC13 / GNL2 / NBAS / MOV10 / RUVBL1 / RUVBL2 / PNRC2 | 0 | 3 | 13 | 1 |
P35125 | USP6 | Cancer | 1 | RUVBL1 | 2 | 1 | 0 | 0 |
P50552 | VASP | Development | 1 | MOV10 | 2 | 1 | 8 | 1 |
P55072 | VCP | Stress | 4 | SEC13 / GNL2 / RUVBL1 / RUVBL2 | 6 | 2 | 13 | 1 |
Q96AJ9 | VTI1A | Cancer | 1 | SEC13 | 8 | 1 | 9 | 1 |
O00401 | WASL | Development | 1 | RUVBL2 | 0 | 4 | 23 | 0 |
Q9H6R7 | WDCP | Cancer | 2 | RUVBL1 / RUVBL2 | 8 | 0 | 0 | 0 |
P61964 | WDR5 | Development | 2 | RUVBL1 / RUVBL2 | 14 | 2 | 5 | 1 |
O14980 | XPO1 | Cancer | 12 | UPF1 / UPF2 / UPF3A / UPF3B / SMG7 / RNPS1 / CASC3 / EIF4A3 / SEC13 / GNL2 / RUVBL1 / RUVBL2 | 14 | 3 | 12 | 0 |
P62258 | YWHAE | Cancer Stress | 5 | UPF1 / SEC13 / GNL2 / RUVBL1 / RUVBL2 | 6 | 3 | 10 | 1 |
P25490 | YY1 | Development | 2 | RUVBL1 / RUVBL2 | 7 | 5 | 7 | 0 |
Q05516 | ZBTB16 | Cancer | 1 | PNRC2 | 0 | 1 | 10 | 0 |
Q14202 | ZMYM3 | Cancer | 1 | MOV10 | 8 | 0 | 3 | 1 |
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Fernandes, R., Nogueira, G., da Costa, P.J., Pinto, F., Romão, L. (2019). Nonsense-Mediated mRNA Decay in Development, Stress and Cancer. In: Romão, L. (eds) The mRNA Metabolism in Human Disease. Advances in Experimental Medicine and Biology, vol 1157. Springer, Cham. https://doi.org/10.1007/978-3-030-19966-1_3
Download citation
DOI: https://doi.org/10.1007/978-3-030-19966-1_3
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-19965-4
Online ISBN: 978-3-030-19966-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)