Combinatorial interplay of RNA-binding proteins tunes levels of mitochondrial mRNA in trypanosomes
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
30120147
PubMed Central
PMC6191715
DOI
10.1261/rna.066233.118
PII: rna.066233.118
Knihovny.cz E-zdroje
- Klíčová slova
- RNA binding proteins, RNA editing, iCLIP, mitochondrion, ribonuclear protein, trypanosome,
- MeSH
- editace RNA MeSH
- messenger RNA genetika metabolismus MeSH
- mitochondrie genetika metabolismus MeSH
- proteiny vázající RNA metabolismus MeSH
- protozoální proteiny genetika metabolismus MeSH
- RNA mitochondriální genetika metabolismus MeSH
- Trypanosoma genetika metabolismus MeSH
- vazba proteinů MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- gBP21 protein, Trypanosoma brucei MeSH Prohlížeč
- messenger RNA MeSH
- mitochondrial messenger RNA MeSH Prohlížeč
- proteiny vázající RNA MeSH
- protozoální proteiny MeSH
- RNA mitochondriální MeSH
MRP1/2 is a heteromeric protein complex that functions in the trypanosomatid mitochondrion as part of the RNA editing machinery, which facilitates multiple targeted insertions and deletions of uridines. MRP1/2 was shown to interact with MRB8170, which initiates RNA editing by marking pre-edited mRNAs, while TbRGG2 is required for its efficient progression on pan-edited mRNAs. Both MRP1/2 and TbRGG2 are capable of modulating RNA-RNA interactions in vitro. As determined by using iCLIP and RIP-qPCR, RNAs bound to MRP1/2 are characterized and compared with those associated with MRB8170 and TbRGG2. We provide evidence that MRP1 and MRB8170 have correlated binding and similar RNA crosslinking peak profiles over minimally and never-edited mRNAs. Our results suggest that MRP1 assists MRB8170 in RNA editing on minimally edited mRNAs.
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Acestor N, Panigrahi AK, Carnes J, Zíková A, Stuart KD. 2009. The MRB1 complex functions in kinetoplastid RNA processing. RNA 15: 277–286. PubMed PMC
Allen TE, Heidmann S, Reed R, Myler PJ, Göringer HU, Stuart KD. 1998. Association of guide RNA binding protein gBP21 with active RNA editing complexes in Trypanosoma brucei. Mol Cell Biol 18: 6014–6022. PubMed PMC
Ammerman ML, Presnyak V, Fisk JC, Foda BM, Read LK. 2010. TbRGG2 facilitates kinetoplastid RNA editing initiation and progression past intrinsic pause sites. RNA 16: 2239–2251. PubMed PMC
Aphasizhev R, Aphasizheva I. 2011. Uridine insertion/deletion editing in trypanosomes: a playground for RNA-guided information transfer. Wiley Interdiscip Rev RNA 2: 669–685. PubMed PMC
Aphasizhev R, Aphasizheva I, Nelson RE, Simpson L. 2003. A 100-kD complex of two RNA-binding proteins from mitochondria of Leishmania tarentolae catalyzes RNA annealing and interacts with several RNA editing components. RNA 9: 62–76. PubMed PMC
Aphasizheva I, Aphasizhev R. 2016. U-insertion/deletion mRNA-editing holoenzyme: definition in sight. Trends Parasitol 32: 144–156. PubMed PMC
Aphasizheva I, Zhang L, Wang X, Kaake RM, Huang L, Monti S, Aphasizhev R. 2014. RNA binding and core complexes constitute the U-insertion/deletion editosome. Mol Cell Biol 34: 4329–4342. PubMed PMC
Carnes J, Trotter JR, Ernst NL, Steinberg A, Stuart K. 2005. An essential RNase III insertion editing endonuclease in Trypanosoma brucei. Proc Natl Acad Sci 102: 16614–16619. PubMed PMC
David V, Flegontov P, Gerasimov E, Tanifuji G, Hashimi H, Logacheva MD, Maruyama S, Onodera NT, Gray MW, Archibald JM, et al. 2015. Gene loss and error-prone RNA editing in the mitochondrion of Perkinsela, an endosymbiotic kinetoplastid. mBio 6: e01498-15. PubMed PMC
Dixit S, Müller-Mcnicoll M, David V, Zarnack K, Ule J, Hashimi H, Lukeš J. 2017. Differential binding of mitochondrial transcripts by MRB8170 and MRB4160 regulates distinct editing fates of mitochondrial MRNA in trypanosomes. mBio 8: e02288-16. PubMed PMC
Fisk JC, Ammerman ML, Presnyak V, Read LK. 2008. TbRGG2, an essential RNA editing accessory factor in two trypanosoma brucei life cycle stages. J Biol Chem 283: 23016–23025. PubMed PMC
Fisk JC, Presnyak V, Ammerman ML, Read LK. 2009. Distinct and overlapping functions of MRP1/2 and RBP16 in mitochondrial RNA metabolism. Mol Cell Biol 29: 5214–5225. PubMed PMC
Foda BM, Downey KM, Fisk JC, Read LK. 2012. Multifunctional G-rich and RRM-containing domains of TbRGG2 perform separate yet essential functions in trypanosome RNA editing. Eukaryot Cell 11: 1119–1131. PubMed PMC
Gerasimov ES, Gasparyan AA, Kaurov I, Tichý B, Logacheva MD, Kolesnikov AA, Lukeš J, Yurchenko V, Zimmer SL, Flegontov P. 2018. Trypanosomatid mitochondrial RNA editing: dramatically complex transcript repertoires revealed with a dedicated mapping tool. Nucleic Acids Res 46: 765–781. PubMed PMC
Hashimi H, Zimmer SL, Ammerman ML, Read LK, Lukeš J. 2013. Dual core processing: MRB1 is an emerging kinetoplast RNA editing complex. Trends Parasitol 29: 91–99. PubMed PMC
Hayman ML, Read LK. 1999. Trypanosoma brucei RBP16 is a mitochondrial Y-box family protein with guide RNA binding activity. J Biol Chem 274: 12067–12074. PubMed
Horáková E, Changmai P, Paris Z, Salmon D, Lukeš J. 2015. Simultaneous depletion of Atm and Mdl rebalances cytosolic Fe-S cluster assembly but not heme import into the mitochondrion of Trypanosoma brucei. FEBS J 282: 4157–4175. PubMed
Huppertz I, Attig J, D'Ambrogio A, Easton LE, Sibley CR, Sugimoto Y, Tajnik M, König J, Ule J. 2014. iCLIP: protein–RNA interactions at nucleotide resolution. Methods 65: 274–287. PubMed PMC
Jensen RE, Englund PT. 2012. Network news: the replication of kinetoplast DNA. Annu Rev Microbiol 66: 473–491. PubMed
Kafková L, Ammerman ML, Faktorová D, Fisk JC, Zimmer SL, Sobotka R, Read LK, Lukeš J, Hashimi H. 2012. Functional characterization of two paralogs that are novel RNA binding proteins influencing mitochondrial transcripts of Trypanosoma brucei. RNA 18: 1846–1861. PubMed PMC
Langmead B, Trapnell C, Pop M, Salzberg SL, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, et al. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25. PubMed PMC
Li F, Ge P, Hui WH, Atanasov I, Rogers K, Guo Q, Osato D, Falick AM, Zhou ZH, Simpson L. 2009. Structure of the core editing complex (L-complex) involved in uridine insertion/deletion RNA editing in trypanosomatid mitochondria. Proc Natl Acad Sci 106: 12306–12310. PubMed PMC
Lott K, Mukhopadhyay S, Li J, Wang J, Yao J, Sun Y, Qu J, Read LK. 2015. Arginine methylation of DRBD18 differentially impacts its opposing effects on the trypanosome transcriptome. Nucleic Acids Res 43: 5501–5523. PubMed PMC
Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15: 550. PubMed PMC
Miller MM, Halbig K, Cruz-Reyes J, Read LK. 2006. RBP16 stimulates trypanosome RNA editing in vitro at an early step in the editing reaction. RNA 12: 1292–1303. PubMed PMC
Müller UF, Göringer HU. 2002. Mechanism of the gBP21-mediated RNA/RNA annealing reaction: matchmaking and charge reduction. Nucleic Acids Res 30: 447–455. PubMed PMC
Müller UF, Lambert L, Göringer HU. 2001. Annealing of RNA editing substrates facilitated by guide RNA-binding protein gBP21. EMBO J 20: 1394–1404. PubMed PMC
Pelletier M, Read LK. 2003. RBP16 is a multifunctional gene regulatory protein involved in editing and stabilization of specific mitochondrial mRNAs in Trypanosoma brucei. RNA 9: 457–468. PubMed PMC
Read LK, Lukeš J, Hashimi H. 2016. Trypanosome RNA editing: the complexity of getting U in and taking U out. Wiley Interdiscip Rev RNA 7: 33–51. PubMed PMC
Rusché LN, Cruz-Reyes J, Piller KJ, Sollner-Webb B. 1997. Purification of a functional enzymatic editing complex from Trypanosoma brucei mitochondria. EMBO J 16: 4069–4081. PubMed PMC
Schnaufer A, Panigrahi AK, Panicucci B, Igo RP, Salavati R, Stuart K. 2001. An RNA ligase essential for RNA editing and survival of the bloodstream form of Trypanosoma brucei. Science 291: 2159–2162. PubMed
Schnaufer A, Ernst NL, Palazzo SS, O'Rear J, Salavati R, Stuart K. 2003. Separate insertion and deletion subcomplexes of the Trypanosoma brucei RNA editing complex. Mol Cell 12: 307–319. PubMed
Schumacher MA, Karamooz E, Zíková A, Trantírek L, Lukeš J. 2006. Crystal structures of T. brucei MRP1/MRP2 guide-RNA binding complex reveal RNA matchmaking mechanism. Cell 126: 701–711. PubMed
Simpson RM, Bruno AE, Bard JE, Buck MJ, Read LK. 2016. High-throughput sequencing of partially edited trypanosome mRNAs reveals barriers to editing progression and evidence for alternative editing. RNA 22: 677–695. PubMed PMC
Simpson RM, Bruno AE, Chen R, Lott K, Tylec BL, Bard JE, Sun Y, Buck MJ, Read LK. 2017. Trypanosome RNA editing mediator complex proteins have distinct functions in gRNA utilization. Nucleic Acids Res 45: 7965–7983. PubMed PMC
Suematsu T, Zhang L, Aphasizheva I, Monti S, Huang L, Wang Q, Costello CE, Aphasizhev R. 2016. Antisense transcripts delimit exonucleolytic activity of the mitochondrial 3′ processome to generate guide RNAs. Mol Cell 61: 364–378. PubMed PMC
Thorvaldsdottir H, Robinson JT, Mesirov JP. 2013. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14: 178–192. PubMed PMC
Verner Z, Basu S, Benz C, Dixit S, Dobáková E, Faktorová D, Hashimi H, Horáková E, Huang Z, Paris Z, et al. 2015. Malleable mitochondrion of Trypanosoma brucei. Int Rev Cell Mol Biol 315: 73–151. PubMed
Vondrušková E, van den Burg J, Zíková A, Ernst NL, Stuart K, Benne R, Lukeš J. 2005. RNA interference analyses suggest a transcript-specific regulatory role for mitochondrial RNA-binding proteins MRP1 and MRP2 in RNA editing and other RNA processing in Trypanosoma brucei. J Biol Chem 280: 2429–2438. PubMed
Weng J, Aphasizheva I, Etheridge RD, Huang L, Wang X, Falick AM, Aphasizhev R. 2008. Guide RNA-binding complex from mitochondria of trypanosomatids. Mol Cell 32: 198–209. PubMed PMC
Zíková A, Kopečná J, Schumacher MA, Stuart K, Trantírek L, Lukeš J. 2008. Structure and function of the native and recombinant mitochondrial MRP1/MRP2 complex from Trypanosoma brucei. Int J Parasitol 38: 901–912. PubMed PMC
Zimmer SL, Simpson RM, Read LK. 2018. High throughput sequencing revolution reveals conserved fundamentals of U-indel editing. WIREs RNA 10.1002/wrna.1487. PubMed DOI PMC
Lexis and Grammar of Mitochondrial RNA Processing in Trypanosomes