ncRNA BC1 influences translation in the oocyte

. 2021 Nov ; 18 (11) : 1893-1904. [epub] 20210208

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33491548

Grantová podpora
MR/N022556/1 Medical Research Council - United Kingdom

Regulation of translation is essential for the diverse biological processes involved in development. Particularly, mammalian oocyte development requires the precisely controlled translation of maternal transcripts to coordinate meiotic and early embryo progression while transcription is silent. It has been recently reported that key components of mRNA translation control are short and long noncoding RNAs (ncRNAs). We found that the ncRNABrain cytoplasmic 1 (BC1) has a role in the fully grown germinal vesicle (GV) mouse oocyte, where is highly expressed in the cytoplasm associated with polysomes. Overexpression of BC1 in GV oocyte leads to a minute decrease in global translation with a significant reduction of specific mRNA translation via interaction with the Fragile X Mental Retardation Protein (FMRP). BC1 performs a repressive role in translation only in the GV stage oocyte without forming FMRP or Poly(A) granules. In conclusion, BC1 acts as the translational repressor of specific mRNAs in the GV stage via its binding to a subset of mRNAs and physical interaction with FMRP. The results reported herein contribute to the understanding of the molecular mechanisms of developmental events connected with maternal mRNA translation.

Zobrazit více v PubMed

Kutter C, Watt S, Stefflova K, et al. Rapid turnover of long noncoding RNAs and the evolution of gene expression. PLoS Genet. 2012;8:e1002841. PubMed PMC

Ponting CP, Oliver PL, Reik W.. Evolution and functions of long noncoding RNAs. Cell. 2009;136:629–641. PubMed

Frankish A, Diekhans M, Ferreira AM, et al. GENCODE reference annotation for the human and mouse genomes. Nucleic Acids Res. 2019;47:766–773. PubMed PMC

Tiedge H, Fremeau RT, Weinstock PH, et al. Dendritic location of neural BC1 RNA. Proc Natl Acad Sci U S A. 1991;88:2093–2097. PubMed PMC

Taft RJ, Pheasant M, Mattick JS. The relationship between non-protein-coding DNA and eukaryotic complexity. BioEssays. 2007;29:288–299. PubMed

Rozhdestvensky TS, Kopylov AM, Brosius J, et al. Neuronal BC1 RNA structure: evolutionary conversion of a tRNAAla domain into an extended stem-loop structure. Rna. 2001;7:722–730. PubMed PMC

Lin D, Pestova TV, Hellen CUT, et al. Translational control by a small RNA: dendritic BC1 RNA targets the eukaryotic initiation factor 4A helicase mechanism. Mol Cell Biol. 2008;28:3008–3019. PubMed PMC

Eom T, Berardi V, Zhong J, et al. Dual nature of translational control by regulatory BC RNAs. Mol Cell Biol. 2011;31:4538–4549. PubMed PMC

Lee Y, Lee HS, Kim M, et al. Brain cytoplasmic RNAs in neurons: from biosynthesis to function. Biomolecules. 2020;10:11–15. PubMed PMC

Muddashetty RS, Khanam T, Kondrashov A, et al. Poly(A)-binding protein is associated with neuronal BC1 and BC200 ribonucleoprotein particles. J Mol Biol. 2002;321:433–445. PubMed

Wang H, Iacoangeli A, Popp S, et al. Dendritic BC1 RNA: functional role in regulation of translation initiation. J Neurosci. 2002;22:10232–10241. PubMed PMC

Briz V, Restivo L, Pasciuto E, et al. The non-coding RNA BC1 regulates experience-dependent structural plasticity and learning. Nat Commun. 2017;8:1–15. PubMed PMC

Lacoux C, Di Marino D, Boyl PP, et al. BC1-FMRP interaction is modulated by 2′-O-methylation: RNA-binding activity of the tudor domain and translational regulation at synapses. Nucleic Acids Res. 2012;40:4086–4096. PubMed PMC

de Rubeis S, Bagni C. Regulation of molecular pathways in the Fragile X Syndrome: insights into Autism Spectrum Disorders. J Neurodev Disord. 2011;3:257–269. PubMed PMC

Zalfa F, Giorgi M, Primerano B, et al. The Fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses. Cell. 2003;112:317–327. PubMed

Zalfa F, Adinolfi S, Napoli I, et al. FMRP binds specifically to the brain cytoplasmic RNAs BC1/BC200 via a novel RNA binding motif. J Biol Chem. 2005;280:33403–33410. PubMed

Zhang T, Pang P, Fang Z, et al. Expression of BC1 impairs spatial learning and memory in alzheimer’s disease via APP translation. Mol Neurobiol. 2018;55:6007–6020. PubMed

Eom T, Muslimov IA, Iacoangeli A, et al. Dendritic targeting and regulatory RNA control of local neuronal translation. Oxford Handb Neuronal Protein Synth. 2018;1–29.

Iacoangeli A, Rozhdestvensky TS, Dolzhanskaya N, et al. On BC1 RNA and the fragile X mental retardation protein. Proc Natl Acad Sci U S A. 2008;105:734–739. PubMed PMC

Zhong J, Chuang SC, Bianchi R, et al. Regulatory BC1 RNA and the fragile X mental retardation protein: convergent functionality in brain. PLoS One. 2010;5:e15509. PubMed PMC

Darnell JC, Van Driesche SJ, Zhang C, et al. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell. 2011;146:247–261. PubMed PMC

Iacoangeli A, Tiedge H. Translational control at the synapse: role of RNA regulators. Trends Biochem Sci. 2013;38:47–55. PubMed PMC

Battaglia R, Vento ME, Borzì P, et al. Non-coding RNAs in the ovarian follicle. Front Genet. 2017;8:57. PubMed PMC

Ganesh S, Horvat F, Drutovic D, et al. The most abundant maternal lncRNA Sirena1 acts post-transcriptionally and impacts mitochondrial distribution. Nucleic Acids Res. 2020;48:3211–3227. PubMed PMC

Karlic R, Ganesh S, Franke V, et al. Long non-coding RNA exchange during the oocyte-to-embryo transition in mice. DNA Res. 2017;24:129–141. PubMed PMC

Kataruka S, Modrak M, Kinterova V, et al. MicroRNA dilution during oocyte growth disables the microRNA pathway in mammalian oocytes. Nucleic Acids Res. 2020;48:8050–8062. PubMed PMC

De La Fuente R, Viveiros MM, Burns KH, et al. Major chromatin remodeling in the germinal vesicle (GV) of mammalian oocytes is dispensable for global transcriptional silencing but required for centromeric heterochromatin function. Dev Biol. 2004;275:447–458. PubMed

Susor A, Kubelka M. Translational regulation in the mammalian oocyte. In: Results and problems in cell differentiation. Results. 2017;63:257-295. Springer Verlag PubMed

Carrieri C, Cimatti L, Biagioli M, et al. Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature. 2012;491:454–457. PubMed

Hutchinson JN, Ensminger AW, Clemson CM, et al. A screen for nuclear transcripts identifies two linked noncoding RNAs associated with SC35 splicing domains. BMC Genomics. 2007;8:1–16. PubMed PMC

Tetkova A, Jansova D, Susor A. Spatio-temporal expression of ANK2 promotes cytokinesis in oocytes. Sci Rep. 2019;9:1–13. PubMed PMC

Wang H, Iacoangeli A, Lin D, et al. Dendritic BC1 RNA in translational control mechanisms. J Cell Biol. 2005;171:811–821. PubMed PMC

Masek T, Del Llano E, Gahurova L, et al. Identifying the translatome of mouse NEBD-stage oocytes via SSP-profiling; a novel polysome fractionation method. Int J Mol Sci. 2020;21:1254. PubMed PMC

Skryabin BV, Sukonina V, Jordan U, et al. Neuronal untranslated BC1 RNA: targeted gene elimination in mice. Mol Cell Biol. 2003;23:6435–6441. PubMed PMC

Dever TE. Gene-specific regulation by general translation factors. Cell. 2002;108:545–556. PubMed

England CG, Ehlerding EB, Cai W. NanoLuc: a small luciferase is brightening up the field of bioluminescence. Bioconjug Chem. 2016;27:1175–1187. PubMed PMC

Gandin V, Masvidal L, Hulea L, et al. NanoCAGE reveals 5ʹ UTR features that define specific modes of translation of functionally related MTOR-sensitive mRNAs. Genome Res. 2016;26:636–648. PubMed PMC

Mayr C. What are 3′ UTRs doing? Cold Spring Harb. Perspect Biol. 2019;11(10):a034728. PubMed PMC

Mann M, Wright PR, Backofen R. IntaRNA 2.0: enhanced and customizable prediction of RNA-RNA interactions. Nucleic Acids Res. 2017;45:435–439. PubMed PMC

Barbagallo C, Brex D, Caponnetto A, et al. LncRNA UCA1, upregulated in CRC biopsies and downregulated in serum exosomes, controls mRNA expression by RNA-RNA interactions. Mol Ther Nucleic Acids. 2018;12:229–241. PubMed PMC

Torres M, Becquet D, Guillen S, et al. RNA pull-down procedure to identify RNA targets of a long non-coding RNA. J Vis Exp. 2018;2018:e57379. PubMed PMC

Chen E, Joseph S. Fragile X mental retardation protein: a paradigm for translational control by RNA-binding proteins. Biochimie. 2015;114:147–154. PubMed PMC

Jansova D, Tetkova A, Koncicka M, et al. Localization of RNA and translation in the mammalian oocyte and embryo. PLoS One. 2018;13:1–25. PubMed PMC

Söderberg O, Leuchowius KJ, Gullberg M, et al. Characterizing proteins and their interactions in cells and tissues using the in situ proximity ligation assay. Methods. 2008;45:227–232. PubMed

Erickson SL, Lykke-Andersen J. Cytoplasmic mRNP granules at a glance. J Cell Sci. 2011;124:293–297. PubMed PMC

Lai A, Valdez-Sinon AN, Bassell GJ. Regulation of RNA granules by FMRP and implications for neurological diseases. Traffic. 2020;21:454–462. PubMed PMC

Rosario R, Filis P, Tessyman V, et al. FMRP associates with cytoplasmic granules at the onset of meiosis in the human oocyte. PLoS One. 2016;11:1–14. PubMed PMC

Wheeler JR, Matheny T, Jain S, et al. Distinct stages in stress granule assembly and disassembly. Elife. 2016;5:e18413. PubMed PMC

Pakos‐Zebrucka K, Koryga I, Mnich K, et al. The integrated stress response. EMBO Rep. 2016;17:1374–1395. PubMed PMC

Shi Z, Barna M. Translating the genome in time and space: specialized ribosomes, RNA regulons, and RNA-binding proteins. Annu Rev Cell Dev Biol. 2015;31:31–54. PubMed

Monti M, Zanoni M, Calligaro A, et al. Developmental arrest and mouse antral not-surrounded nucleolus oocytes. Biol Reprod. 2013;88:1–7. PubMed PMC

Del Llano E, Masek T, Gahurova L, et al. Age-related differences in the translational landscape of mammalian oocytes. Aging Cell. 2020;19:e13231. PubMed PMC

Burkholder GD, Comings DE, Okada TA. A storage form of ribosomes in mouse oocytes. Exp Cell Res. 1971;69:361–371. PubMed

Yurttas P, Vitale AM, Fitzhenry RJ, et al. Role for PADI6 and the cytoplasmic lattices in ribosomal storage in oocytes and translational control in the early mouse embryo. Development. 2008;135:2627–2636. PubMed PMC

Chen E, Sharma MR, Shi X, et al. Fragile X mental retardation protein regulates translation by binding directly to the ribosome. Mol Cell. 2014;54:407–417. PubMed PMC

Ishizuka A, Siomi MC, Siomi H. A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev. 2002;16:2497–2508. PubMed PMC

Didiot MC, Subramanian M, Flatter E, et al. Cells lacking the fragile X mental retardation protein (FMRP) have normal RISC activity but exhibit altered stress granule assembly. Mol Biol Cell. 2009;20:428–437. PubMed PMC

Lee EK, Kim HH, Kuwano Y, et al. HnRNP C promotes APP translation by competing with FMRP for APP mRNA recruitment to P bodies. Nat Struct Mol Biol. 2010;17:732–739. PubMed PMC

Feng Y, Absher D, Eberhart DE, et al. FMRP associates with polyribosomes as an mRNP, and the I304N mutation of severe fragile X syndrome abolishes this association. Mol Cell. 1997;1:109–118. PubMed

Khandjian EW, Huot ME, Tremblay S, et al. Biochemical evidence for the association of fragile X mental retardation protein with brain polyribosomal ribonucleoparticles. Proc Natl Acad Sci U S A. 2004;101:13357–13362. PubMed PMC

Stefani G, Fraser CE, Darnell JC, et al. Fragile X mental retardation protein is associated with translating polyribosomes in neuronal cells. J Neurosci. 2004;24:7272–7276. PubMed PMC

Davidson EH. Gene Activity in Early Development. 3rd Edition. Academic Press, Inc; 1986. p. 158-159.

Graber TE, Hébert-Seropian S, Khoutorsky A, et al. Reactivation of stalled polyribosomes in synaptic plasticity. Proc Natl Acad Sci U S A. 2013;110:16205–16210. PubMed PMC

Shah S, Molinaro G, Liu B, et al. FMRP control of ribosome translocation promotes chromatin modifications and alternative splicing of neuronal genes linked to autism. Cell Rep. 2020;30:4459–4472.e6. PubMed PMC

Dalton CM, Carroll J. Biased inheritance of mitochondria during asymmetric cell division in the mouse oocyte. J Cell Sci. 2013;126:2955–2964. PubMed PMC

FitzHarris G, Marangos P, Carroll J. Changes in endoplasmic reticulum structure during mouse oocyte maturation are controlled by the cytoskeleton and cytoplasmic dynein. Dev Biol. 2007;305:133–144. PubMed

Schlaitz AL, Thompson J, Wong CCL, et al. REEP3/4 ensure endoplasmic reticulum clearance from metaphase chromatin and proper nuclear envelope architecture. Dev Cell. 2013;26:315–323. PubMed PMC

Susor A, Jansova D, Cerna R, et al. Temporal and spatial regulation of translation in the mammalian oocyte via the mTOR-eIF4F pathway. Nat Commun. 2015;6:1–12. PubMed PMC

Flemr M, Ma J, Schultz RM, et al. P-body loss is concomitant with formation of a messenger RNA storage domain in mouse oocytes. Biol Reprod. 2010;82:1008–1017. PubMed PMC

Chan SP, Slack FJ. microRNA-mediated silencing inside P-bodies. RNA Biol. 2006;3:97–100. PubMed

Jakymiw A, Pauley KM, Li SL, et al. The role of GW/P-bodies in RNA processing and silencing. J Cell Sci. 2007;120:1702. PubMed

Parker R, Sheth U. P bodies and the control of mRNA translation and degradation. Mol Cell. 2007;25:635–646. PubMed

Ma J, Flemr M, Stein P, et al. MicroRNA activity is suppressed in mouse oocytes. Curr Biol. 2010;20:265–270. PubMed PMC

Suh N, Baehner L, Moltzahn F, et al. MicroRNA function is globally suppressed in mouse oocytes and early embryos. Curr Biol. 2010;20:271–277. PubMed PMC

Sternlicht AL, Schultz RM. Biochemical studies of mammalian oogenesis: kinetics of accumulation of total and poly(A)‐containing RNA during growth of the mouse oocyte. J Exp Zool. 1981;215:191–200. PubMed

Lin CJ, Koh FM, Wong P, et al. Hira-mediated H3.3 incorporation is required for DNA replication and ribosomal RNA transcription in the mouse zygote. Dev Cell. 2014;30:268–279. PubMed PMC

Thoreen CC, Chantranupong L, Keys HR, et al. A unifying model for mTORC1-mediated regulation of mRNA translation. Nature. 2012;485:109–113. PubMed PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...