Transcriptional Adaptation in

Overview

Journal Elife

Specialty Biology

Date 2020 Jan 18

PMID 31951195

Citations 25

Authors

Vahan Serobyan

Zacharias Kontarakis

Mohamed A El-Brolosy

Jordan M Welker

Oleg Tolstenkov

Amr M Saadeldein

Nicholas Retzer

Alexander Gottschalk

Ann M Wehman

Didier Yr Stainier

Affiliations

Soon will be listed here.

Abstract

Transcriptional adaptation is a recently described phenomenon by which a mutation in one gene leads to the transcriptional modulation of related genes, termed adapting genes. At the molecular level, it has been proposed that the mutant mRNA, rather than the loss of protein function, activates this response. While several examples of transcriptional adaptation have been reported in zebrafish embryos and in mouse cell lines, it is not known whether this phenomenon is observed across metazoans. Here we report transcriptional adaptation in , and find that this process requires factors involved in mutant mRNA decay, as in zebrafish and mouse. We further uncover a requirement for Argonaute proteins and Dicer, factors involved in small RNA maturation and transport into the nucleus. Altogether, these results provide evidence for transcriptional adaptation in , a powerful model to further investigate underlying molecular mechanisms.

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References

Lindeboom R, Supek F, Lehner B . The rules and impact of nonsense-mediated mRNA decay in human cancers. Nat Genet. 2016; 48(10):1112-8. PMC: 5045715. DOI: 10.1038/ng.3664. View

Castel S, Cervera A, Mohammadi P, Aguet F, Reverter F, Wolman A . Modified penetrance of coding variants by cis-regulatory variation contributes to disease risk. Nat Genet. 2018; 50(9):1327-1334. PMC: 6119105. DOI: 10.1038/s41588-018-0192-y. View

Sztal T, McKaige E, Williams C, Ruparelia A, Bryson-Richardson R . Genetic compensation triggered by actin mutation prevents the muscle damage caused by loss of actin protein. PLoS Genet. 2018; 14(2):e1007212. PMC: 5821405. DOI: 10.1371/journal.pgen.1007212. View

Rechavi O, Lev I . Principles of Transgenerational Small RNA Inheritance in Caenorhabditis elegans. Curr Biol. 2017; 27(14):R720-R730. DOI: 10.1016/j.cub.2017.05.043. View

Kryuchkova-Mostacci N, Robinson-Rechavi M . Tissue-Specific Evolution of Protein Coding Genes in Human and Mouse. PLoS One. 2015; 10(6):e0131673. PMC: 4488272. DOI: 10.1371/journal.pone.0131673. View

Hutvagner G, Simard M . Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol. 2007; 9(1):22-32. DOI: 10.1038/nrm2321. View

Pavelec D, Lachowiec J, Duchaine T, Smith H, Kennedy S . Requirement for the ERI/DICER complex in endogenous RNA interference and sperm development in Caenorhabditis elegans. Genetics. 2009; 183(4):1283-95. PMC: 2787421. DOI: 10.1534/genetics.109.108134. View

Shirayama M, Seth M, Lee H, Gu W, Ishidate T, Conte Jr D . piRNAs initiate an epigenetic memory of nonself RNA in the C. elegans germline. Cell. 2012; 150(1):65-77. PMC: 3597741. DOI: 10.1016/j.cell.2012.06.015. View

Radomska K, Sager J, Farnsworth B, Tellgren-Roth A, Tuveri G, Peuckert C . Characterization and Expression of the Zebrafish qki Paralogs. PLoS One. 2016; 11(1):e0146155. PMC: 4699748. DOI: 10.1371/journal.pone.0146155. View

10.

Zhang Z, Krainer A . Involvement of SR proteins in mRNA surveillance. Mol Cell. 2004; 16(4):597-607. DOI: 10.1016/j.molcel.2004.10.031. View

11.

Ghanbarian H, Wagner N, Michiels J, Cuzin F, Wagner K, Rassoulzadegan M . Small RNA-directed epigenetic programming of embryonic stem cell cardiac differentiation. Sci Rep. 2017; 7:41799. PMC: 5292948. DOI: 10.1038/srep41799. View

12.

Singh G, Kucukural A, Cenik C, Leszyk J, Shaffer S, Weng Z . The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus. Cell. 2012; 151(4):750-764. PMC: 3522173. DOI: 10.1016/j.cell.2012.10.007. View

13.

Castel S, Martienssen R . RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat Rev Genet. 2013; 14(2):100-12. PMC: 4205957. DOI: 10.1038/nrg3355. View

14.

Vasale J, Gu W, Thivierge C, Batista P, Claycomb J, Youngman E . Sequential rounds of RNA-dependent RNA transcription drive endogenous small-RNA biogenesis in the ERGO-1/Argonaute pathway. Proc Natl Acad Sci U S A. 2010; 107(8):3582-7. PMC: 2840456. DOI: 10.1073/pnas.0911908107. View

15.

Huntzinger E, Kashima I, Fauser M, Sauliere J, Izaurralde E . SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA. 2008; 14(12):2609-17. PMC: 2590965. DOI: 10.1261/rna.1386208. View

16.

Conant G, Wagner A . Duplicate genes and robustness to transient gene knock-downs in Caenorhabditis elegans. Proc Biol Sci. 2004; 271(1534):89-96. PMC: 1691561. DOI: 10.1098/rspb.2003.2560. View

17.

Turunen M, Lehtola T, Heinonen S, Assefa G, Korpisalo P, Girnary R . Efficient regulation of VEGF expression by promoter-targeted lentiviral shRNAs based on epigenetic mechanism: a novel example of epigenetherapy. Circ Res. 2009; 105(6):604-9. DOI: 10.1161/CIRCRESAHA.109.200774. View

18.

Denli A, Tops B, Plasterk R, Ketting R, Hannon G . Processing of primary microRNAs by the Microprocessor complex. Nature. 2004; 432(7014):231-5. DOI: 10.1038/nature03049. View

19.

Zhuang J, Hunter C . Tissue specificity of Caenorhabditis elegans enhanced RNA interference mutants. Genetics. 2011; 188(1):235-7. PMC: 3120140. DOI: 10.1534/genetics.111.127209. View

20.

Fraser A, Kamath R, Zipperlen P, Martinez-Campos M, Sohrmann M, Ahringer J . Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature. 2000; 408(6810):325-30. DOI: 10.1038/35042517. View