Nuclear mRNA Quality Control and Cytoplasmic NMD Are Linked by the Guard Proteins Gbp2 and Hrb1
Abstract
:1. Introduction
2. Quality Control of Splicing in the Nucleus—Retention or Export of mRNA
3. Further Surveillance in the Cytoplasm—Detection of Errors via Nonsense-Mediated Decay
4. Gbp2 and Hrb1 in Nuclear Quality Control of Splicing—Decay or Export of mRNA
5. Gbp2 and Hrb1 in Nonsense-Mediated mRNA Decay—New Cytoplasmic Roles
6. Gbp2 and Hrb1 as Prototypes of Human Proteins
7. Closing Remarks
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Jacob, A.G.; Smith, C.W.J. Intron retention as a component of regulated gene expression programs. Hum. Genet. 2017, 136, 1043–1057. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kelemen, O.; Convertini, P.; Zhang, Z.; Wen, Y.; Shen, M.; Falaleeva, M.; Stamm, S. Function of alternative splicing. Gene 2013, 514, 1–30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, Y.; Rio, D.C. Mechanisms and Regulation of Alternative Pre-mRNA Splicing. Annu. Rev. Biochem. 2015, 84, 291–323. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Long, J.C.; Caceres, J.F. The SR protein family of splicing factors: Master regulators of gene expression. Biochem. J. 2009, 417, 15–27. [Google Scholar] [CrossRef] [Green Version]
- Zhou, Z.; Fu, X.D. Regulation of splicing by SR proteins and SR protein-specific kinases. Chromosoma 2013, 122, 191–207. [Google Scholar] [CrossRef]
- Wende, W.; Friedhoff, P.; Strasser, K. Mechanism and Regulation of Co-transcriptional mRNP Assembly and Nuclear mRNA Export. Adv. Exp. Med. Biol. 2019, 1203, 1–31. [Google Scholar] [CrossRef]
- De Almeida, S.F.; Garcia-Sacristan, A.; Custodio, N.; Carmo-Fonseca, M. A link between nuclear RNA surveillance, the human exosome and RNA polymerase II transcriptional termination. Nucleic Acids Res. 2010, 38, 8015–8026. [Google Scholar] [CrossRef] [Green Version]
- Martins, S.B.; Rino, J.; Carvalho, T.; Carvalho, C.; Yoshida, M.; Klose, J.M.; de Almeida, S.F.; Carmo-Fonseca, M. Spliceosome assembly is coupled to RNA polymerase II dynamics at the 3′ end of human genes. Nat. Struct. Mol. Biol. 2011, 18, 1115–1123. [Google Scholar] [CrossRef]
- Martinson, H.G. An active role for splicing in 3′-end formation. Wiley Interdiscip. Rev. RNA 2011, 2, 459–470. [Google Scholar] [CrossRef]
- Custodio, N.; Carmo-Fonseca, M.; Geraghty, F.; Pereira, H.S.; Grosveld, F.; Antoniou, M. Inefficient processing impairs release of RNA from the site of transcription. EMBO J. 1999, 18, 2855–2866. [Google Scholar] [CrossRef] [Green Version]
- Dower, K.; Kuperwasser, N.; Merrikh, H.; Rosbash, M. A synthetic A tail rescues yeast nuclear accumulation of a ribozyme-terminated transcript. RNA 2004, 10, 1888–1899. [Google Scholar] [CrossRef] [Green Version]
- Rigo, F.; Martinson, H.G. Polyadenylation releases mRNA from RNA polymerase II in a process that is licensed by splicing. RNA 2009, 15, 823–836. [Google Scholar] [CrossRef] [Green Version]
- Eberle, A.B.; Visa, N. Quality control of mRNP biogenesis: Networking at the transcription site. Semin. Cell Dev. Biol. 2014, 32, 37–46. [Google Scholar] [CrossRef]
- Schmid, M.; Jensen, T.H. Controlling nuclear RNA levels. Nat. Rev. Genet. 2018, 19, 518–529. [Google Scholar] [CrossRef]
- Davidson, L.; Kerr, A.; West, S. Co-transcriptional degradation of aberrant pre-mRNA by Xrn2. EMBO J. 2012, 31, 2566–2578. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carvalho, T.; Martins, S.; Rino, J.; Marinho, S.; Carmo-Fonseca, M. Pharmacological inhibition of the spliceosome subunit SF3b triggers exon junction complex-independent nonsense-mediated decay. J. Cell Sci. 2017, 130, 1519–1531. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Girard, C.; Will, C.L.; Peng, J.; Makarov, E.M.; Kastner, B.; Lemm, I.; Urlaub, H.; Hartmuth, K.; Luhrmann, R. Post-transcriptional spliceosomes are retained in nuclear speckles until splicing completion. Nat. Commun. 2012, 3, 994. [Google Scholar] [CrossRef] [PubMed]
- Hett, A.; West, S. Inhibition of U4 snRNA in human cells causes the stable retention of polyadenylated pre-mRNA in the nucleus. PLoS ONE 2014, 9, e96174. [Google Scholar] [CrossRef]
- Galganski, L.; Urbanek, M.O.; Krzyzosiak, W.J. Nuclear speckles: Molecular organization, biological function and role in disease. Nucleic Acids Res. 2017, 45, 10350–10368. [Google Scholar] [CrossRef] [Green Version]
- Wegener, M.; Muller-McNicoll, M. Nuclear retention of mRNAs—quality control, gene regulation and human disease. Semin. Cell Dev. Biol. 2018, 79, 131–142. [Google Scholar] [CrossRef]
- Dias, A.P.; Dufu, K.; Lei, H.; Reed, R. A role for TREX components in the release of spliced mRNA from nuclear speckle domains. Nat. Commun. 2010, 1, 97. [Google Scholar] [CrossRef] [Green Version]
- Ishihama, Y.; Tadakuma, H.; Tani, T.; Funatsu, T. The dynamics of pre-mRNAs and poly(A)+ RNA at speckles in living cells revealed by iFRAP studies. Exp. Cell Res. 2008, 314, 748–762. [Google Scholar] [CrossRef]
- Boothby, T.C.; Zipper, R.S.; van der Weele, C.M.; Wolniak, S.M. Removal of retained introns regulates translation in the rapidly developing gametophyte of Marsilea vestita. Dev. Cell 2013, 24, 517–529. [Google Scholar] [CrossRef] [Green Version]
- Majewska, K.; Wroblewska-Ankiewicz, P.; Rudzka, M.; Hyjek-Skladanowska, M.; Golebiewski, M.; Smolinski, D.J.; Kolowerzo-Lubnau, A. Different Patterns of mRNA Nuclear Retention during Meiotic Prophase in Larch Microsporocytes. Int. J. Mol. Sci. 2021, 22, 8501. [Google Scholar] [CrossRef] [PubMed]
- Naro, C.; Jolly, A.; Di Persio, S.; Bielli, P.; Setterblad, N.; Alberdi, A.J.; Vicini, E.; Geremia, R.; De la Grange, P.; Sette, C. An Orchestrated Intron Retention Program in Meiosis Controls Timely Usage of Transcripts during Germ Cell Differentiation. Dev. Cell 2017, 41, 82–93 e84. [Google Scholar] [CrossRef] [Green Version]
- Paci, G.; Caria, J.; Lemke, E.A. Cargo transport through the nuclear pore complex at a glance. J. Cell Sci. 2021, 134, jcs247874. [Google Scholar] [CrossRef] [PubMed]
- Soheilypour, M.; Mofrad, M.R.K. Quality control of mRNAs at the entry of the nuclear pore: Cooperation in a complex molecular system. Nucleus 2018, 9, 202–211. [Google Scholar] [CrossRef] [Green Version]
- Le Hir, H.; Izaurralde, E.; Maquat, L.E.; Moore, M.J. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 2000, 19, 6860–6869. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Singh, G.; Kucukural, A.; Cenik, C.; Leszyk, J.D.; Shaffer, S.A.; Weng, Z.; Moore, M.J. The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus. Cell 2012, 151, 750–764. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Botti, V.; McNicoll, F.; Steiner, M.C.; Richter, F.M.; Solovyeva, A.; Wegener, M.; Schwich, O.D.; Poser, I.; Zarnack, K.; Wittig, I.; et al. Cellular differentiation state modulates the mRNA export activity of SR proteins. J. Cell Biol. 2017, 216, 1993–2009. [Google Scholar] [CrossRef] [PubMed]
- Lai, M.C.; Tarn, W.Y. Hypophosphorylated ASF/SF2 binds TAP and is present in messenger ribonucleoproteins. J. Biol. Chem. 2004, 279, 31745–31749. [Google Scholar] [CrossRef] [Green Version]
- Müller-McNicoll, M.; Botti, V.; de Jesus Domingues, A.M.; Brandl, H.; Schwich, O.D.; Steiner, M.C.; Curk, T.; Poser, I.; Zarnack, K.; Neugebauer, K.M. SR proteins are NXF1 adaptors that link alternative RNA processing to mRNA export. Genes Dev. 2016, 30, 553–566. [Google Scholar] [CrossRef] [Green Version]
- Hackmann, A.; Wu, H.; Schneider, U.M.; Meyer, K.; Jung, K.; Krebber, H. Quality control of spliced mRNAs requires the shuttling SR proteins Gbp2 and Hrb1. Nat. Commun. 2014, 5, 3123. [Google Scholar] [CrossRef] [PubMed]
- Fasken, M.B.; Corbett, A.H. Links between mRNA Splicing, mRNA Quality Control, and Intellectual Disability. RNA Dis. 2016, 3. [Google Scholar] [CrossRef]
- Soucek, S.; Zeng, Y.; Bellur, D.L.; Bergkessel, M.; Morris, K.J.; Deng, Q.; Duong, D.; Seyfried, N.T.; Guthrie, C.; Staley, J.P.; et al. The Evolutionarily-conserved Polyadenosine RNA Binding Protein, Nab2, Cooperates with Splicing Machinery to Regulate the Fate of pre-mRNA. Mol. Cell. Biol. 2016, 36, 2697–2714. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Galy, V.; Gadal, O.; Fromont-Racine, M.; Romano, A.; Jacquier, A.; Nehrbass, U. Nuclear retention of unspliced mRNAs in yeast is mediated by perinuclear Mlp1. Cell 2004, 116, 63–73. [Google Scholar] [CrossRef] [Green Version]
- Coyle, J.H.; Bor, Y.C.; Rekosh, D.; Hammarskjold, M.L. The Tpr protein regulates export of mRNAs with retained introns that traffic through the Nxf1 pathway. RNA 2011, 17, 1344–1356. [Google Scholar] [CrossRef] [Green Version]
- Rajanala, K.; Nandicoori, V.K. Localization of nucleoporin Tpr to the nuclear pore complex is essential for Tpr mediated regulation of the export of unspliced RNA. PLoS ONE 2012, 7, e29921. [Google Scholar] [CrossRef]
- Green, D.M.; Johnson, C.P.; Hagan, H.; Corbett, A.H. The C-terminal domain of myosin-like protein 1 (Mlp1p) is a docking site for heterogeneous nuclear ribonucleoproteins that are required for mRNA export. Proc. Natl. Acad. Sci. USA 2003, 100, 1010–1015. [Google Scholar] [CrossRef] [Green Version]
- Vinciguerra, P.; Iglesias, N.; Camblong, J.; Zenklusen, D.; Stutz, F. Perinuclear Mlp proteins downregulate gene expression in response to a defect in mRNA export. EMBO J. 2005, 24, 813–823. [Google Scholar] [CrossRef]
- Fasken, M.B.; Corbett, A.H. Mechanisms of nuclear mRNA quality control. RNA Biol. 2009, 6, 237–241. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Skruzny, M.; Schneider, C.; Racz, A.; Weng, J.; Tollervey, D.; Hurt, E. An endoribonuclease functionally linked to perinuclear mRNP quality control associates with the nuclear pore complexes. PLoS Biol. 2009, 7, e8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sayani, S.; Janis, M.; Lee, C.Y.; Toesca, I.; Chanfreau, G.F. Widespread impact of nonsense-mediated mRNA decay on the yeast intronome. Mol. Cell 2008, 31, 360–370. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zander, G.; Hackmann, A.; Bender, L.; Becker, D.; Lingner, T.; Salinas, G.; Krebber, H. mRNA quality control is bypassed for immediate export of stress-responsive transcripts. Nature 2016, 540, 593–596. [Google Scholar] [CrossRef] [PubMed]
- Karousis, E.D.; Muhlemann, O. Nonsense-Mediated mRNA Decay Begins Where Translation Ends. Cold Spring Harb. Perspect. Biol. 2019, 11, a032862. [Google Scholar] [CrossRef]
- Kurosaki, T.; Popp, M.W.; Maquat, L.E. Quality and quantity control of gene expression by nonsense-mediated mRNA decay. Nat. Rev. 2019, 20, 406–420. [Google Scholar] [CrossRef]
- Celik, A.; Baker, R.; He, F.; Jacobson, A. High-resolution profiling of NMD targets in yeast reveals translational fidelity as a basis for substrate selection. RNA 2017, 23, 735–748. [Google Scholar] [CrossRef] [Green Version]
- He, F.; Peltz, S.W.; Donahue, J.L.; Rosbash, M.; Jacobson, A. Stabilization and ribosome association of unspliced pre-mRNAs in a yeast upf1- mutant. Proc. Natl. Acad. Sci. USA 1993, 90, 7034–7038. [Google Scholar] [CrossRef] [Green Version]
- Jaillon, O.; Bouhouche, K.; Gout, J.F.; Aury, J.M.; Noel, B.; Saudemont, B.; Nowacki, M.; Serrano, V.; Porcel, B.M.; Segurens, B.; et al. Translational control of intron splicing in eukaryotes. Nature 2008, 451, 359–362. [Google Scholar] [CrossRef] [Green Version]
- Green, R.E.; Lewis, B.P.; Hillman, R.T.; Blanchette, M.; Lareau, L.F.; Garnett, A.T.; Rio, D.C.; Brenner, S.E. Widespread predicted nonsense-mediated mRNA decay of alternatively-spliced transcripts of human normal and disease genes. Bioinformatics 2003, 19 (Suppl. 1), i118–i121. [Google Scholar] [CrossRef] [Green Version]
- Lewis, B.P.; Green, R.E.; Brenner, S.E. Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc. Natl. Acad. Sci. USA 2003, 100, 189–192. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barberan-Soler, S.; Lambert, N.J.; Zahler, A.M. Global analysis of alternative splicing uncovers developmental regulation of nonsense-mediated decay in C. elegans. RNA 2009, 15, 1652–1660. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hansen, K.D.; Lareau, L.F.; Blanchette, M.; Green, R.E.; Meng, Q.; Rehwinkel, J.; Gallusser, F.L.; Izaurralde, E.; Rio, D.C.; Dudoit, S.; et al. Genome-wide identification of alternative splice forms down-regulated by nonsense-mediated mRNA decay in Drosophila. PLoS Genet. 2009, 5, e1000525. [Google Scholar] [CrossRef] [PubMed]
- McIlwain, D.R.; Pan, Q.; Reilly, P.T.; Elia, A.J.; McCracken, S.; Wakeham, A.C.; Itie-Youten, A.; Blencowe, B.J.; Mak, T.W. Smg1 is required for embryogenesis and regulates diverse genes via alternative splicing coupled to nonsense-mediated mRNA decay. Proc. Natl. Acad. Sci. USA 2010, 107, 12186–12191. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Garcia-Moreno, J.F.; Romao, L. Perspective in Alternative Splicing Coupled to Nonsense-Mediated mRNA Decay. Int. J. Mol. Sci. 2020, 21, 9424. [Google Scholar] [CrossRef]
- Andjus, S.; Morillon, A.; Wery, M. From Yeast to Mammals, the Nonsense-Mediated mRNA Decay as a Master Regulator of Long Non-Coding RNAs Functional Trajectory. Non-Coding RNA 2021, 7, 44. [Google Scholar] [CrossRef] [PubMed]
- Nasif, S.; Contu, L.; Muhlemann, O. Beyond quality control: The role of nonsense-mediated mRNA decay (NMD) in regulating gene expression. Semin. Cell Dev. Biol. 2018, 75, 78–87. [Google Scholar] [CrossRef]
- Nickless, A.; Bailis, J.M.; You, Z. Control of gene expression through the nonsense-mediated RNA decay pathway. Cell Biosci. 2017, 7, 26. [Google Scholar] [CrossRef]
- Gupta, P.; Li, Y.R. Upf proteins: Highly conserved factors involved in nonsense mRNA mediated decay. Mol. Biol. Rep. 2018, 45, 39–55. [Google Scholar] [CrossRef]
- Czaplinski, K.; Ruiz-Echevarria, M.J.; Paushkin, S.V.; Han, X.; Weng, Y.; Perlick, H.A.; Dietz, H.C.; Ter-Avanesyan, M.D.; Peltz, S.W. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev. 1998, 12, 1665–1677. [Google Scholar] [CrossRef] [Green Version]
- Ivanov, P.V.; Gehring, N.H.; Kunz, J.B.; Hentze, M.W.; Kulozik, A.E. Interactions between UPF1, eRFs, PABP and the exon junction complex suggest an integrated model for mammalian NMD pathways. EMBO J. 2008, 27, 736–747. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Czaplinski, K.; Weng, Y.; Hagan, K.W.; Peltz, S.W. Purification and characterization of the Upf1 protein: A factor involved in translation and mRNA degradation. RNA 1995, 1, 610–623. [Google Scholar] [PubMed]
- Fiorini, F.; Bagchi, D.; Le Hir, H.; Croquette, V. Human Upf1 is a highly processive RNA helicase and translocase with RNP remodelling activities. Nat. Commun. 2015, 6, 7581. [Google Scholar] [CrossRef] [Green Version]
- Franks, T.M.; Singh, G.; Lykke-Andersen, J. Upf1 ATPase-dependent mRNP disassembly is required for completion of nonsense- mediated mRNA decay. Cell 2010, 143, 938–950. [Google Scholar] [CrossRef] [Green Version]
- Serdar, L.D.; Whiteside, D.L.; Baker, K.E. ATP hydrolysis by UPF1 is required for efficient translation termination at premature stop codons. Nat. Commun. 2016, 7, 14021. [Google Scholar] [CrossRef]
- Serdar, L.D.; Whiteside, D.L.; Nock, S.L.; McGrath, D.; Baker, K.E. Inhibition of post-termination ribosome recycling at premature termination codons in UPF1 ATPase mutants. eLife 2020, 9, e57834. [Google Scholar] [CrossRef]
- Colombo, M.; Karousis, E.D.; Bourquin, J.; Bruggmann, R.; Mühlemann, O. Transcriptome-wide identification of NMD-targeted human mRNAs reveals extensive redundancy between SMG6- and SMG7-mediated degradation pathways. RNA 2017, 23, 189–201. [Google Scholar] [CrossRef] [Green Version]
- Nagy, E.; Maquat, L.E. A rule for termination-codon position within intron-containing genes: When nonsense affects RNA abundance. Trends Biochem. Sci. 1998, 23, 198–199. [Google Scholar] [CrossRef]
- Schlautmann, L.P.; Gehring, N.H. A Day in the Life of the Exon Junction Complex. Biomolecules 2020, 10, 866. [Google Scholar] [CrossRef] [PubMed]
- Woodward, L.A.; Mabin, J.W.; Gangras, P.; Singh, G. The exon junction complex: A lifelong guardian of mRNA fate. Wiley Interdiscip. Rev. RNA 2017, 8, e1411. [Google Scholar] [CrossRef]
- Lejeune, F.; Ishigaki, Y.; Li, X.; Maquat, L.E. The exon junction complex is detected on CBP80-bound but not eIF4E-bound mRNA in mammalian cells: Dynamics of mRNP remodeling. EMBO J. 2002, 21, 3536–3545. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- 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. USA 2010, 107, 10050–10055. [Google Scholar] [CrossRef] [Green Version]
- Gehring, N.H.; Neu-Yilik, G.; Schell, T.; Hentze, M.W.; Kulozik, A.E. Y14 and hUpf3b form an NMD-activating complex. Mol. Cell 2003, 11, 939–949. [Google Scholar] [CrossRef]
- Wen, J.; He, M.; Petrj, M.; Marzi, L.; Wang, J.; Piechocki, K.; McLeod, T.; Singh, A.K.; Dwivedi, V.; Brogna, S. An intron proximal to a PTC enhances NMD in Saccharomyces cerevisiae. bioRxiv 2020, 149245. [Google Scholar] [CrossRef] [Green Version]
- Cao, D.; Parker, R. Computational modeling and experimental analysis of nonsense-mediated decay in yeast. Cell 2003, 113, 533–545. [Google Scholar] [CrossRef] [Green Version]
- Hagan, K.W.; Ruiz-Echevarria, M.J.; Quan, Y.; Peltz, S.W. Characterization of cis-acting sequences and decay intermediates involved in nonsense-mediated mRNA turnover. Mol. Cell. Biol. 1995, 15, 809–823. [Google Scholar] [CrossRef] [Green Version]
- 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. [Google Scholar] [CrossRef]
- Muhlrad, D.; Parker, R. Premature translational termination triggers mRNA decapping. Nature 1994, 370, 578–581. [Google Scholar] [CrossRef]
- Nissan, T.; Rajyaguru, P.; She, M.; Song, H.; Parker, R. Decapping activators in Saccharomyces cerevisiae act by multiple mechanisms. Mol. Cell 2010, 39, 773–783. [Google Scholar] [CrossRef] [Green Version]
- Mitchell, P.; Tollervey, D. An NMD pathway in yeast involving accelerated deadenylation and exosome-mediated 3′-->5′ degradation. Mol. Cell 2003, 11, 1405–1413. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Eberle, A.B.; Lykke-Andersen, S.; Mühlemann, O.; Jensen, T.H. SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat. Struct. Mol. Biol. 2009, 16, 49–55. [Google Scholar] [CrossRef]
- Gatfield, D.; Izaurralde, E. Nonsense-mediated messenger RNA decay is initiated by endonucleolytic cleavage in Drosophila. Nature 2004, 429, 575–578. [Google Scholar] [CrossRef]
- Huntzinger, E.; Kashima, I.; Fauser, M.; Saulière, J.; Izaurralde, E. SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA 2008, 14, 2609–2617. [Google Scholar] [CrossRef] [Green Version]
- Ohnishi, T.; Yamashita, A.; Kashima, I.; Schell, T.; Anders, K.R.; Grimson, A.; Hachiya, T.; Hentze, M.W.; 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. [Google Scholar] [CrossRef]
- Okada-Katsuhata, Y.; Yamashita, A.; Kutsuzawa, K.; Izumi, N.; Hirahara, F.; Ohno, S. N- and C-terminal Upf1 phosphorylations create binding platforms for SMG-6 and SMG-5:SMG-7 during NMD. Nucleic Acids Res. 2012, 40, 1251–1266. [Google Scholar] [CrossRef] [Green Version]
- Loh, B.; Jonas, S.; Izaurralde, E. The SMG5-SMG7 heterodimer directly recruits the CCR4-NOT deadenylase complex to mRNAs containing nonsense codons via interaction with POP2. Genes Dev. 2013, 27, 2125–2138. [Google Scholar] [CrossRef] [Green Version]
- Muhlrad, D.; Parker, R. Recognition of yeast mRNAs as “nonsense containing” leads to both inhibition of mRNA translation and mRNA degradation: Implications for the control of mRNA decapping. Mol. Biol. Cell 1999, 10, 3971–3978. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Isken, O.; Kim, Y.K.; Hosoda, N.; Mayeur, G.L.; Hershey, J.W.; Maquat, L.E. Upf1 phosphorylation triggers translational repression during nonsense-mediated mRNA decay. Cell 2008, 133, 314–327. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Egecioglu, D.E.; Chanfreau, G. Proofreading and spellchecking: A two-tier strategy for pre-mRNA splicing quality control. RNA 2011, 17, 383–389. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sayani, S.; Chanfreau, G.F. Sequential RNA degradation pathways provide a fail-safe mechanism to limit the accumulation of unspliced transcripts in Saccharomyces cerevisiae. RNA 2012, 18, 1563–1572. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hacker, S.; Krebber, H. Differential Export Requirements for Shuttling Serine/Arginine-type mRNA-binding Proteins. J. Biol. Chem. 2004, 279, 5049–5052. [Google Scholar] [CrossRef] [Green Version]
- Windgassen, M.; Krebber, H. Identification of Gbp2 as a novel poly(A)+ RNA-binding protein involved in the cytoplasmic delivery of messenger RNAs in yeast. EMBO Rep. 2003, 4, 278–283. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bossie, M.A.; Silver, P.A. Movement of macromolecules between the cytoplasm and the nucleus in yeast. Curr. Opin. Genet. Dev. 1992, 2, 768–774. [Google Scholar] [CrossRef]
- Birney, E.; Kumar, S.; Krainer, A.R. Analysis of the RNA-recognition motif and RS and RGG domains: Conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res. 1993, 21, 5803–5816. [Google Scholar] [CrossRef] [Green Version]
- Wegener, M.; Muller-McNicoll, M. View from an mRNP: The Roles of SR Proteins in Assembly, Maturation and Turnover. Adv. Exp. Med. Biol 2019, 1203, 83–112. [Google Scholar] [CrossRef] [PubMed]
- Baierlein, C.; Hackmann, A.; Gross, T.; Henker, L.; Hinz, F.; Krebber, H. Monosome formation during translation initiation requires the serine/arginine-rich protein Npl3. Mol. Cell. Biol. 2013, 33, 4811–4823. [Google Scholar] [CrossRef] [Green Version]
- Bucheli, M.E.; Buratowski, S. Npl3 is an antagonist of mRNA 3′ end formation by RNA polymerase II. EMBO J. 2005, 24, 2150–2160. [Google Scholar] [CrossRef]
- Dermody, J.L.; Dreyfuss, J.M.; Villén, J.; Ogundipe, B.; Gygi, S.P.; Park, P.J.; Ponticelli, A.S.; Moore, C.L.; Buratowski, S.; Bucheli, M.E. Unphosphorylated SR-like protein Npl3 stimulates RNA polymerase II elongation. PLoS ONE 2008, 3, e3273. [Google Scholar] [CrossRef] [Green Version]
- Estrella, L.A.; Wilkinson, M.F.; Gonzalez, C.I. The Shuttling Protein Npl3 Promotes Translation Termination Accuracy in Saccharomyces cerevisiae. J. Mol. Biol. 2009. [Google Scholar] [CrossRef] [Green Version]
- Kress, T.L.; Krogan, N.J.; Guthrie, C. A single SR-like protein, Npl3, promotes pre-mRNA splicing in budding yeast. Mol. Cell 2008, 32, 727–734. [Google Scholar] [CrossRef] [Green Version]
- Lee, M.S.; Henry, M.; Pamela, A. A protein that shuttles between the nucleus and the cvtoplasm is an important mediator of RNA export. Genes Dev. 1996, 10, 1233–1246. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rajyaguru, P.; She, M.; Parker, R. Scd6 targets eIF4G to repress translation: RGG motif proteins as a class of eIF4G-binding proteins. Mol. Cell 2012, 45, 244–254. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Windgassen, M.; Sturm, D.; Cajigas, I.J.; Gonzalez, C.I.; Seedorf, M.; Bastians, H.; Krebber, H. Yeast shuttling SR proteins Npl3p, Gbp2p, and Hrb1p are part of the translating mRNPs, and Npl3p can function as a translational repressor. Mol. Cell. Biol. 2004, 24, 10479–10491. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Caceres, J.F.; Screaton, G.R.; Krainer, A.R. A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes Dev. 1998, 12, 55–66. [Google Scholar] [CrossRef] [Green Version]
- Huang, Y.; Steitz, J.A. SRprises along a messenger’s journey. Mol. Cell 2005, 17, 613–615. [Google Scholar] [CrossRef] [PubMed]
- Hurt, E.; Luo, M.-J.; Röther, S.; Reed, R.; Strässer, K. Cotranscriptional recruitment of the serine-arginine-rich (SR)-like proteins Gbp2 and Hrb1 to nascent mRNA via the TREX complex. Proc. Natl. Acad. Sci. USA 2004, 101, 1858–1862. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Meinel, D.M.; Burkert-Kautzsch, C.; Kieser, A.; O’Duibhir, E.; Siebert, M.; Mayer, A.; Cramer, P.; Söding, J.; Holstege, F.C.P.; Sträßer, K. Recruitment of TREX to the Transcription Machinery by Its Direct Binding to the Phospho-CTD of RNA Polymerase II. PLoS Genet. 2013, 9, e1003914. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Meinel, D.M.; Sträßer, K. Co-transcriptional mRNP formation is coordinated within a molecular mRNP packaging station in S. cerevisiae. BioEssays 2015, 37, 666–677. [Google Scholar] [CrossRef]
- Abruzzi, K.C.; Lacadie, S.; Rosbash, M. Biochemical analysis of TREX complex recruitment to intronless and intron-containing yeast genes. EMBO J. 2004, 23, 2620–2631. [Google Scholar] [CrossRef] [Green Version]
- Chanarat, S.; Seizl, M.; Strasser, K. The Prp19 complex is a novel transcription elongation factor required for TREX occupancy at transcribed genes. Genes Dev. 2011, 25, 1147–1158. [Google Scholar] [CrossRef] [Green Version]
- Gromadzka, A.M.; Steckelberg, A.L.; Singh, K.K.; Hofmann, K.; Gehring, N.H. A short conserved motif in ALYREF directs cap- and EJC-dependent assembly of export complexes on spliced mRNAs. Nucleic Acids Res. 2016, 44, 2348–2361. [Google Scholar] [CrossRef] [PubMed]
- Lardelli, R.M.; Thompson, J.X.; Yates, J.R., 3rd; Stevens, S.W. Release of SF3 from the intron branchpoint activates the first step of pre-mRNA splicing. RNA 2010, 16, 516–528. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Masuda, S.; Das, R.; Cheng, H.; Hurt, E.; Dorman, N.; Reed, R. Recruitment of the human TREX complex to mRNA during splicing. Genes Dev. 2005, 19, 1512–1517. [Google Scholar] [CrossRef] [Green Version]
- Warkocki, Z.; Odenwalder, P.; Schmitzova, J.; Platzmann, F.; Stark, H.; Urlaub, H.; Ficner, R.; Fabrizio, P.; Luhrmann, R. Reconstitution of both steps of Saccharomyces cerevisiae splicing with purified spliceosomal components. Nat. Struct. Mol. Biol. 2009, 16, 1237–1243. [Google Scholar] [CrossRef]
- Tuck, A.C.; Tollervey, D. A Transcriptome-wide Atlas of RNP Composition Reveals Diverse Classes of mRNAs and lncRNAs. Cell 2013, 154, 996–1009. [Google Scholar] [CrossRef] [Green Version]
- Mourier, T.; Jeffares, D.C. Eukaryotic intron loss. Science 2003, 300, 1393. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Neuveglise, C.; Marck, C.; Gaillardin, C. The intronome of budding yeasts. Comptes Rendus Biol. 2011, 334, 662–670. [Google Scholar] [CrossRef]
- Baejen, C.; Torkler, P.; Gressel, S.; Essig, K.; Söding, J.; Cramer, P. Transcriptome Maps of mRNP Biogenesis Factors Define Pre-mRNA Recognition. Mol. Cell 2014, 55, 745–757. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bretes, H.; Rouviere, J.O.; Leger, T.; Oeffinger, M.; Devaux, F.; Doye, V.; Palancade, B. Sumoylation of the THO complex regulates the biogenesis of a subset of mRNPs. Nucleic Acids Res. 2014, 42, 5043–5058. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hackmann, A.; Gross, T.; Baierlein, C.; Krebber, H. The mRNA export factor Npl3 mediates the nuclear export of large ribosomal subunits. EMBO Rep. 2011, 12, 1024–1031. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kong, K.Y.E.; Tang, H.M.V.; Pan, K.; Huang, Z.; Lee, T.H.J.; Hinnebusch, A.G.; Jin, D.Y.; Wong, C.M. Cotranscriptional recruitment of yeast TRAMP complex to intronic sequences promotes optimal pre-mRNA splicing. Nucleic Acids Res. 2014, 42, 643–660. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bresson, S.; Tollervey, D. Surveillance-ready transcription: Nuclear RNA decay as a default fate. Open Biol. 2018, 8, 170270. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jensen, T.H.; Dower, K.; Libri, D.; Rosbash, M. Early formation of mRNP: License for export or quality control? Mol. Cell 2003, 11, 1129–1138. [Google Scholar] [CrossRef]
- Saguez, C.; Olesen, J.R.; Jensen, T.H. Formation of export-competent mRNP: Escaping nuclear destruction. Curr. Opin. Cell Biol. 2005, 17, 287–293. [Google Scholar] [CrossRef]
- Stewart, M. Nuclear export of mRNA. Trends Biochem. Sci. 2010, 35, 609–617. [Google Scholar] [CrossRef]
- Merrick, W.C.; Pavitt, G.D. Protein Synthesis Initiation in Eukaryotic Cells. Cold Spring Harb. Perspect. Biol. 2018, 10, a033092. [Google Scholar] [CrossRef]
- Lund, M.K.; Guthrie, C. The DEAD-box protein Dbp5p is required to dissociate Mex67p from exported mRNPs at the nuclear rim. Mol. Cell 2005, 20, 645–651. [Google Scholar] [CrossRef]
- Tieg, B.; Krebber, H. Dbp5—From nuclear export to translation. Biochim. Biophys. Acta 2013, 1829, 791–798. [Google Scholar] [CrossRef]
- Tran, E.J.; Zhou, Y.; Corbett, A.H.; Wente, S.R. The DEAD-box protein Dbp5 controls mRNA export by triggering specific RNA:protein remodeling events. Mol. Cell 2007, 28, 850–859. [Google Scholar] [CrossRef] [PubMed]
- Grosse, S.; Lu, Y.Y.; Coban, I.; Neumann, B.; Krebber, H. Nuclear SR-protein mediated mRNA quality control is continued in cytoplasmic nonsense-mediated decay. RNA Biol. 2021, 18, 1390–1407. [Google Scholar] [CrossRef]
- Johnson, S.J.; Jackson, R.N. Ski2-like RNA helicase structures: Common themes and complex assemblies. RNA Biol. 2013, 10, 33–43. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Poornima, G.; Srivastava, G.; Roy, B.; Kuttanda, I.A.; Kurbah, I.; Rajyaguru, P.I. RGG-motif containing mRNA export factor Gbp2 acts as a translation repressor. RNA Biol. 2021, 1–12. [Google Scholar] [CrossRef]
- He, F.; Jacobson, A. Nonsense-Mediated mRNA Decay: Degradation of Defective Transcripts Is Only Part of the Story. Annu Rev. Genet. 2015, 49, 339–366. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, Z.; Krainer, A.R. Involvement of SR proteins in mRNA surveillance. Mol. Cell 2004, 16, 597–607. [Google Scholar] [CrossRef]
- Aznarez, I.; Nomakuchi, T.T.; Tetenbaum-Novatt, J.; Rahman, M.A.; Fregoso, O.; Rees, H.; Krainer, A.R. Mechanism of Nonsense-Mediated mRNA Decay Stimulation by Splicing Factor SRSF1. Cell Rep. 2018, 23, 2186–2198. [Google Scholar] [CrossRef] [Green Version]
- Rahman, M.A.; Lin, K.T.; Bradley, R.K.; Abdel-Wahab, O.; Krainer, A.R. Recurrent SRSF2 mutations in MDS affect both splicing and NMD. Genes Dev. 2020, 34, 413–427. [Google Scholar] [CrossRef]
- Kim, J.; Park, R.Y.; Chen, J.K.; Kim, J.; Jeong, S.; Ohn, T. Splicing factor SRSF3 represses the translation of programmed cell death 4 mRNA by associating with the 5′-UTR region. Cell Death Differ. 2014, 21, 481–490. [Google Scholar] [CrossRef]
- Swartz, J.E.; Bor, Y.C.; Misawa, Y.; Rekosh, D.; Hammarskjold, M.L. The shuttling SR protein 9G8 plays a role in translation of unspliced mRNA containing a constitutive transport element. J. Biol. Chem. 2007, 282, 19844–19853. [Google Scholar] [CrossRef] [Green Version]
- Siebel, C.W.; Feng, L.; Guthrie, C.; Fu, X.D. Conservation in budding yeast of a kinase specific for SR splicing factors. Proc. Natl. Acad. Sci. USA 1999, 96, 5440–5445. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kataoka, N.; Bachorik, J.L.; Dreyfuss, G. Transportin-SR, a nuclear import receptor for SR proteins. J. Cell Biol. 1999, 145, 1145–1152. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Saudemont, B.; Popa, A.; Parmley, J.L.; Rocher, V.; Blugeon, C.; Necsulea, A.; Meyer, E.; Duret, L. The fitness cost of mis-splicing is the main determinant of alternative splicing patterns. Genome Biol. 2017, 18, 208. [Google Scholar] [CrossRef] [PubMed]
- Anna, A.; Monika, G. Splicing mutations in human genetic disorders: Examples, detection, and confirmation. J. Appl. Genet. 2018, 59, 253–268. [Google Scholar] [CrossRef] [Green Version]
- Scotti, M.M.; Swanson, M.S. RNA mis-splicing in disease. Nat. Rev. Genet. 2016, 17, 19–32. [Google Scholar] [CrossRef] [PubMed]
- Urbanski, L.M.; Leclair, N.; Anczukow, O. Alternative-splicing defects in cancer: Splicing regulators and their downstream targets, guiding the way to novel cancer therapeutics. Wiley Interdiscip. Rev. RNA 2018, 9, e1476. [Google Scholar] [CrossRef]
- Bhadra, M.; Howell, P.; Dutta, S.; Heintz, C.; Mair, W.B. Alternative splicing in aging and longevity. Hum. Genet. 2020, 139, 357–369. [Google Scholar] [CrossRef]
- Buchan, J.R.; Muhlrad, D.; Parker, R. P bodies promote stress granule assembly in Saccharomyces cerevisiae. J. Cell Biol. 2008, 183, 441–455. [Google Scholar] [CrossRef]
- Twyffels, L.; Gueydan, C.; Kruys, V. Shuttling SR proteins: More than splicing factors. FEBS J. 2011, 278, 3246–3255. [Google Scholar] [CrossRef]
- Cai, B.; Li, Z.; Ma, M.; Zhang, J.; Kong, S.; Abdalla, B.A.; Xu, H.; Jebessa, E.; Zhang, X.; Lawal, R.A.; et al. Long noncoding RNA SMUL suppresses SMURF2 production-mediated muscle atrophy via nonsense-mediated mRNA decay. Mol. Nucleic Acids 2021, 23, 512–526. [Google Scholar] [CrossRef]
- Wery, M.; Descrimes, M.; Vogt, N.; Dallongeville, A.S.; Gautheret, D.; Morillon, A. Nonsense-Mediated Decay Restricts LncRNA Levels in Yeast Unless Blocked by Double-Stranded RNA Structure. Mol. Cell 2016, 61, 379–392. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ajiro, M.; Jia, R.; Yang, Y.; Zhu, J.; Zheng, Z.M. A genome landscape of SRSF3-regulated splicing events and gene expression in human osteosarcoma U2OS cells. Nucleic Acids Res. 2016, 44, 1854–1870. [Google Scholar] [CrossRef]
- Li, H.; Guo, S.; Zhang, M.; Li, L.; Wang, F.; Song, B. Long non-coding RNA AGAP2-AS1 accelerates cell proliferation, migration, invasion and the EMT process in colorectal cancer via regulating the miR-4,668-3p/SRSF1 axis. J. Gene Med. 2020, 22, e3250. [Google Scholar] [CrossRef] [PubMed]
- Paz, S.; Ritchie, A.; Mauer, C.; Caputi, M. The RNA binding protein SRSF1 is a master switch of gene expression and regulation in the immune system. Cytokine Growth Factor Rev. 2021, 57, 19–26. [Google Scholar] [CrossRef]
- Sokol, E.; Kedzierska, H.; Czubaty, A.; Rybicka, B.; Rodzik, K.; Tanski, Z.; Boguslawska, J.; Piekielko-Witkowska, A. microRNA-mediated regulation of splicing factors SRSF1, SRSF2 and hnRNP A1 in context of their alternatively spliced 3′UTRs. Exp. Cell Res. 2018, 363, 208–217. [Google Scholar] [CrossRef] [PubMed]
- Xu, Y.F.; Xu, X.; Gin, A.; Nshimiyimana, J.D.; Mooers, B.H.M.; Caputi, M.; Hannafon, B.N.; Ding, W.Q. SRSF1 regulates exosome microRNA enrichment in human cancer cells. Cell Commun. Signal. 2020, 18, 130. [Google Scholar] [CrossRef]
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Lu, Y.-Y.; Krebber, H. Nuclear mRNA Quality Control and Cytoplasmic NMD Are Linked by the Guard Proteins Gbp2 and Hrb1. Int. J. Mol. Sci. 2021, 22, 11275. https://doi.org/10.3390/ijms222011275
Lu Y-Y, Krebber H. Nuclear mRNA Quality Control and Cytoplasmic NMD Are Linked by the Guard Proteins Gbp2 and Hrb1. International Journal of Molecular Sciences. 2021; 22(20):11275. https://doi.org/10.3390/ijms222011275
Chicago/Turabian StyleLu, Yen-Yun, and Heike Krebber. 2021. "Nuclear mRNA Quality Control and Cytoplasmic NMD Are Linked by the Guard Proteins Gbp2 and Hrb1" International Journal of Molecular Sciences 22, no. 20: 11275. https://doi.org/10.3390/ijms222011275