Roles of Sumoylation in MRNA Processing and Metabolism

Overview

Journal Adv Exp Med Biol

Specialties Biology
General Medicine

Date 2017 Feb 16

PMID 28197904

Citations 18

Authors

Patricia Richard

Vasupradha Vethantham

James L Manley

Affiliations

Soon will be listed here.

Abstract

SUMO has gained prominence as a regulator in a number of cellular processes. The roles of sumoylation in RNA metabolism, however, while considerable, remain less well understood. In this chapter we have assembled data from proteomic analyses, localization studies and key functional studies to extend SUMO's role to the area of mRNA processing and metabolism. Proteomic analyses have identified multiple putative sumoylation targets in complexes functioning in almost all aspects of mRNA metabolism, including capping, splicing and polyadenylation of mRNA precursors. Possible regulatory roles for SUMO have emerged in pre-mRNA 3' processing, where SUMO influences the functions of polyadenylation factors and activity of the entire complex. SUMO is also involved in regulating RNA editing and RNA binding by hnRNP proteins, and recent reports have suggested the involvement of the SUMO pathway in mRNA export. Together, these reports suggest that SUMO is involved in regulation of many aspects of mRNA metabolism and hold the promise for exciting future studies.

Citing Articles

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References

Matunis M, Zhang X, Ellis N . SUMO: the glue that binds. Dev Cell. 2006; 11(5):596-7. DOI: 10.1016/j.devcel.2006.10.011. View

Denison C, Rudner A, Gerber S, Bakalarski C, Moazed D, Gygi S . A proteomic strategy for gaining insights into protein sumoylation in yeast. Mol Cell Proteomics. 2004; 4(3):246-54. DOI: 10.1074/mcp.M400154-MCP200. View

Shi Y, Di Giammartino D, Taylor D, Sarkeshik A, Rice W, Yates 3rd J . Molecular architecture of the human pre-mRNA 3' processing complex. Mol Cell. 2009; 33(3):365-76. PMC: 2946185. DOI: 10.1016/j.molcel.2008.12.028. View

Kashyap A, Schieltz D, Yates 3rd J, Kellogg D . Biochemical and genetic characterization of Yra1p in budding yeast. Yeast. 2004; 22(1):43-56. DOI: 10.1002/yea.1185. View

Wohlschlegel J, Johnson E, Reed S, Yates 3rd J . Global analysis of protein sumoylation in Saccharomyces cerevisiae. J Biol Chem. 2004; 279(44):45662-8. DOI: 10.1074/jbc.M409203200. View

Chan S, Huppertz I, Yao C, Weng L, Moresco J, Yates 3rd J . CPSF30 and Wdr33 directly bind to AAUAAA in mammalian mRNA 3' processing. Genes Dev. 2014; 28(21):2370-80. PMC: 4215182. DOI: 10.1101/gad.250993.114. View

Liu H, Banerjee T, Guan X, Freitas M, Parvin J . The chromatin scaffold protein SAFB1 localizes SUMO-1 to the promoters of ribosomal protein genes to facilitate transcription initiation and splicing. Nucleic Acids Res. 2015; 43(7):3605-13. PMC: 4402547. DOI: 10.1093/nar/gkv246. View

Geiss-Friedlander R, Melchior F . Concepts in sumoylation: a decade on. Nat Rev Mol Cell Biol. 2007; 8(12):947-56. DOI: 10.1038/nrm2293. View

Emili A, Shales M, McCracken S, Xie W, Tucker P, Kobayashi R . Splicing and transcription-associated proteins PSF and p54nrb/nonO bind to the RNA polymerase II CTD. RNA. 2002; 8(9):1102-11. PMC: 1370324. DOI: 10.1017/s1355838202025037. View

10.

Richard P, Manley J . Transcription termination by nuclear RNA polymerases. Genes Dev. 2009; 23(11):1247-69. PMC: 2763537. DOI: 10.1101/gad.1792809. View

11.

Xu X, Rose A, Muthuswamy S, Jeong S, Venkatakrishnan S, Zhao Q . NUCLEAR PORE ANCHOR, the Arabidopsis homolog of Tpr/Mlp1/Mlp2/megator, is involved in mRNA export and SUMO homeostasis and affects diverse aspects of plant development. Plant Cell. 2007; 19(5):1537-48. PMC: 1913724. DOI: 10.1105/tpc.106.049239. View

12.

Bretes H, Rouviere J, Leger T, Oeffinger M, Devaux F, Doye V . Sumoylation of the THO complex regulates the biogenesis of a subset of mRNPs. Nucleic Acids Res. 2014; 42(8):5043-58. PMC: 4005672. DOI: 10.1093/nar/gku124. View

13.

Schimmel J, Eifler K, Sigurdsson J, Cuijpers S, Hendriks I, Verlaan-de Vries M . Uncovering SUMOylation dynamics during cell-cycle progression reveals FoxM1 as a key mitotic SUMO target protein. Mol Cell. 2014; 53(6):1053-66. DOI: 10.1016/j.molcel.2014.02.001. View

14.

Ryan K . Pre-mRNA 3' cleavage is reversibly inhibited in vitro by cleavage factor dephosphorylation. RNA Biol. 2007; 4(1):26-33. PMC: 4851251. DOI: 10.4161/rna.4.1.4365. View

15.

Kim S, Yamamoto J, Chen Y, Aida M, Wada T, Handa H . Evidence that cleavage factor Im is a heterotetrameric protein complex controlling alternative polyadenylation. Genes Cells. 2010; 15(9):1003-13. DOI: 10.1111/j.1365-2443.2010.01436.x. View

16.

Cordin O, Banroques J, Tanner N, Linder P . The DEAD-box protein family of RNA helicases. Gene. 2005; 367:17-37. DOI: 10.1016/j.gene.2005.10.019. View

17.

Krecic A, Swanson M . hnRNP complexes: composition, structure, and function. Curr Opin Cell Biol. 1999; 11(3):363-71. DOI: 10.1016/S0955-0674(99)80051-9. View

18.

Liang S, Lutz C . p54nrb is a component of the snRNP-free U1A (SF-A) complex that promotes pre-mRNA cleavage during polyadenylation. RNA. 2005; 12(1):111-21. PMC: 1370891. DOI: 10.1261/rna.2213506. View

19.

Miller M, Barrett-Wilt G, Hua Z, Vierstra R . Proteomic analyses identify a diverse array of nuclear processes affected by small ubiquitin-like modifier conjugation in Arabidopsis. Proc Natl Acad Sci U S A. 2010; 107(38):16512-7. PMC: 2944710. DOI: 10.1073/pnas.1004181107. View

20.

Moreira M, Klur S, Watanabe M, Nemeth A, Le Ber I, Moniz J . Senataxin, the ortholog of a yeast RNA helicase, is mutant in ataxia-ocular apraxia 2. Nat Genet. 2004; 36(3):225-7. DOI: 10.1038/ng1303. View