Nuclear mRNA decay: regulatory networks that control gene expression

Maniatis, T. & Reed, R. An extensive network of coupling among gene expression machines. Nature 416, 499–506 (2002).

Article  CAS  PubMed  Google Scholar 

Rambout, X., Dequiedt, F. & Maquat, L. E. Beyond transcription: roles of transcription factors in pre-mRNA splicing. Chem. Rev. 118, 4339–4364 (2018).

Article  CAS  PubMed  Google Scholar 

Mitschka, S. & Mayr, C. Context-specific regulation and function of mRNA alternative polyadenylation. Nat. Rev. Mol. Cell Biol. 23, 779–796 (2022).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Wolin, S. L. & Maquat, L. E. Cellular RNA surveillance in health and disease. Science 366, 822–827 (2019).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Kilchert, C. RNA exosomes and their cofactors. Methods Mol. Biol. 2062, 215–235 (2020).

Article  CAS  PubMed  Google Scholar 

Schmid, M. & Jensen, T. H. Controlling nuclear RNA levels. Nat. Rev. Genet. 19, 518–529 (2018).

Article  CAS  PubMed  Google Scholar 

Kilchert, C., Wittmann, S. & Vasiljeva, L. The regulation and functions of the nuclear RNA exosome complex. Nat. Rev. Mol. Cell Biol. 17, 227–239 (2016).

Article  CAS  PubMed  Google Scholar 

Agostini, F., Zagalak, J., Attig, J., Ule, J. & Luscombe, N. M. Intergenic RNA mainly derives from nascent transcripts of known genes. Genome Biol. 22, 136 (2021).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Collins, J. W. et al. ZCCHC8 is required for the degradation of pervasive transcripts originating from multiple genomic regulatory features. Preprint at bioRxiv https://doi.org/10.1101/2021.01.29.428898 (2021).

Wu, G. et al. A two-layered targeting mechanism underlies nuclear RNA sorting by the human exosome. Cell Rep. 30, 2387–2401.e5 (2020).

Article  CAS  PubMed  Google Scholar 

Wu, M. et al. The RNA exosome shapes the expression of key protein-coding genes. Nucleic Acids Res. 48, 8509–8528 (2020).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Villa, T. & Porrua, O. Pervasive transcription: a controlled risk. FEBS J. 290, 3723–3736 (2022).

Article  PubMed  Google Scholar 

Eaton, J. D. & West, S. Termination of transcription by RNA polymerase II: BOOM! Trends Genet. 36, 664–675 (2020).

Article  CAS  PubMed  Google Scholar 

Zhou, H. et al. Rixosomal RNA degradation contributes to silencing of Polycomb target genes. Nature 604, 167–174 (2022).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Andersen, P. R. et al. The human cap-binding complex is functionally connected to the nuclear RNA exosome. Nat. Struct. Mol. Biol. 20, 1367–1376 (2013).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Meola, N. et al. Identification of a nuclear exosome decay pathway for processed transcripts. Mol. Cell 64, 520–533 (2016). This study identifies the core constituents and the canonical RNA targets of the RNA exosome adaptor PAXT in human cells.

Article  CAS  PubMed  Google Scholar 

Winczura, K. et al. Characterizing ZC3H18, a multi-domain protein at the interface of RNA production and destruction decisions. Cell Rep. 22, 44–58 (2018).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Rouvière, J. O. et al. ARS2 instructs early transcription termination-coupled RNA decay by recruiting ZC3H4 to nascent transcripts. Mol. Cell 22, 2240–2257.e6 (2023).

Article  Google Scholar 

Foucher, A. E. et al. Structural analysis of Red1 as a conserved scaffold of the RNA-targeting MTREC/PAXT complex. Nat. Commun. 13, 4969 (2022).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Polák, P. et al. Dual agonistic and antagonistic roles of ZC3H18 provide for co-activation of distinct nuclear RNA decay pathways. Cell Rep. 42, 113325 (2023).

Article  PubMed  PubMed Central  Google Scholar 

Dubiez, E. et al. Structural basis for competitive binding of productive and degradative co-transcriptional effectors to the nuclear cap-binding complex. Cell Rep. 43, 113639 (2024).

Article  CAS  PubMed  Google Scholar 

Lubas, M. et al. Interaction profiling identifies the human nuclear exosome targeting complex. Mol. Cell 43, 624–637 (2011). This study defines the constituents and the canonical RNA targets of the RNA exosome adaptors NEXT and mTRAMP in human cells.

Article  CAS  PubMed  Google Scholar 

Lubas, M. et al. The human nuclear exosome targeting complex is loaded onto newly synthesized RNA to direct early ribonucleolysis. Cell Rep. 10, 178–192 (2015).

Article  CAS  PubMed  Google Scholar 

Lykke-Andersen, S. et al. Integrator is a genome-wide attenuator of non-productive transcription. Mol. Cell 81, 514–529.e6 (2021).

Article  CAS  PubMed  Google Scholar 

Ogami, K. et al. An Mtr4/ZFC3H1 complex facilitates turnover of unstable nuclear RNAs to prevent their cytoplasmic transport and global translational repression. Genes Dev. 31, 1257–1271 (2017).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Insco, M. L. et al. Oncogenic CDK13 mutations impede nuclear RNA surveillance. Science 380, eabn7625 (2023).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Bresson, S. M., Hunter, O. V., Hunter, A. C. & Conrad, N. K. Canonical poly(A) polymerase activity promotes the decay of a wide variety of mammalian nuclear RNAs. PLoS Genet. 11, e1005610 (2015). This study uses human cells to identify those nuclear RNAs that are degraded by the PPD pathway and how they are degraded.

Article  PubMed  PubMed Central  Google Scholar 

Beaulieu, Y. B., Kleinman, C. L., Landry-Voyer, A. M., Majewski, J. & Bachand, F. Polyadenylation-dependent control of long noncoding RNA expression by the poly(A)-binding protein nuclear 1. PLoS Genet. 8, e1003078 (2012).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Silla, T. et al. The human ZC3H3 and RBM26/27 proteins are critical for PAXT-mediated nuclear RNA decay. Nucleic Acids Res. 48, 2518–2530 (2020).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Hurt, J. A. et al. A conserved CCCH-type zinc finger protein regulates mRNA nuclear adenylation and export. J. Cell Biol. 185, 265–277 (2009).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Wagner, E. J., Tong, L. & Adelman, K. Integrator is a global promoter-proximal termination complex. Mol. Cell 83, 416–427 (2023).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Estell, C. et al. A restrictor complex of ZC3H4, WDR82, and ARS2 integrates with PNUTS to control unproductive transcription. Mol. Cell 83, 2222–2239.e5 (2023).

Article  CAS  PubMed  Google Scholar 

Rambout, X. & Maquat, L. E. The nuclear cap-binding complex as choreographer of gene transcription and pre-mRNA processing. Genes Dev. 34, 1113–1127 (2020).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Rambout, X. et al. PGC-1α senses the CBC of pre-mRNA to dictate the fate of promoter-proximally paused RNAPII. Mol. Cell 83, 186–202.e11 (2023).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Rambout, X. & Maquat, L. E. NCBP3: a multifaceted adaptive regulator of gene expression. Trends Biochem. Sci. 46, 87–96 (2021).

Article  CAS  PubMed  Google Scholar 

Klama, S. et al. A guard protein mediated quality control mechanism monitors 5′-capping of pre-mRNAs. Nucleic Acids Res. 50, 11301–11314 (2022).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Jiao, X., Chang, J. H., Kilic, T., Tong, L. & Kiledjian, M. A mammalian pre-mRNA 5′ end capping quality control mechanism and an unexpected link of capping to pre-mRNA processing. Mol. Cell 50, 104–115 (2013).

Article  CAS  PubMed 

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