Developmental mRNA clearance by PIWI-bound endo-siRNAs in Paramecium.

RNA, Small Interfering / genetics RNA Interference Paramecium / genetics RNA, Messenger / genetics RNA, Double-Stranded Argonaute Proteins / genetics
Argonaute CP: Cell biology CP: Molecular biology PTGS Piwi ciliates mRNA clearance siRNAs small RNA clusters small RNAs unicellular untranslated mRNA

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
28 03 2023
Historique:
received: 06 10 2022
revised: 21 12 2022
accepted: 17 02 2023
medline: 3 4 2023
pubmed: 5 3 2023
entrez: 4 3 2023
Statut: ppublish

Résumé

The clearance of untranslated mRNAs by Argonaute proteins is essential for embryonic development in metazoans. However, it is currently unknown whether similar processes exist in unicellular eukaryotes. The ciliate Paramecium tetraurelia harbors a vast array of PIWI-clade Argonautes involved in various small RNA (sRNA) pathways, many of which have not yet been investigated. Here, we investigate the function of a PIWI protein, Ptiwi08, whose expression is limited to a narrow time window during development, concomitant with the start of zygotic transcription. We show that Ptiwi08 acts in an endogenous small interfering RNA (endo-siRNA) pathway involved in the clearance of untranslated mRNAs. These endo-siRNAs are found in clusters that are strictly antisense to their target mRNAs and are a subset of siRNA-producing clusters (SRCs). Furthermore, the endo-siRNAs are 2'-O-methylated by Hen1 and require Dcr1 for their biogenesis. Our findings suggest that sRNA-mediated developmental mRNA clearance extends beyond metazoans and may be a more widespread mechanism than previously anticipated.

Identifiants

DOI: 10.1016/j.celrep.2023.112213 PMID: 36870062 PMC: PMC10066578
pubmed: 36870062
pii: S2211-1247(23)00224-3
doi: 10.1016/j.celrep.2023.112213
pmc: PMC10066578
pii:
doi:

Substances chimiques

RNA, Small Interfering 0
RNA, Messenger 0
RNA, Double-Stranded 0
Argonaute Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

112213

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Références

Nat Commun. 2019 Apr 4;10(1):1551
pubmed: 30948728
Curr Biol. 2005 Aug 23;15(16):1501-7
pubmed: 16111943
Science. 2005 Feb 11;307(5711):932-5
pubmed: 15705854
Nucleic Acids Res. 2015 Apr 20;43(7):e47
pubmed: 25605792
Rapid Commun Mass Spectrom. 2003;17(20):2310-6
pubmed: 14558131
Nature. 2006 Nov 9;444(7116):171-8
pubmed: 17086204
BMC Genomics. 2017 Jun 26;18(1):483
pubmed: 28651633
Genome Res. 2004 Jun;14(6):1188-90
pubmed: 15173120
Nat Biotechnol. 2011 Jan;29(1):24-6
pubmed: 21221095
Nat Struct Mol Biol. 2007 Apr;14(4):349-50
pubmed: 17384646
Science. 2004 Sep 3;305(5689):1437-41
pubmed: 15284456
Nucleic Acids Res. 2014 Jun;42(11):7268-80
pubmed: 24860163
Nat Struct Mol Biol. 2007 Apr;14(4):347-8
pubmed: 17384647
Nat Rev Genet. 2011 Jan;12(1):19-31
pubmed: 21116305
Nat Methods. 2017 May;14(5):513-520
pubmed: 28394336
J Proteome Res. 2008 Jan;7(1):286-92
pubmed: 18078310
Cell Rep. 2017 Jul 11;20(2):505-520
pubmed: 28700949
RNA Biol. 2021 Nov 12;18(sup2):757-769
pubmed: 34663180
Nucleic Acids Res. 2020 Jan 8;48(D1):D599-D605
pubmed: 31733062
Nat Commun. 2014 Oct 31;5:5277
pubmed: 25358478
Cell. 2005 Nov 18;123(4):621-9
pubmed: 16271385
Cell. 2010 Mar 5;140(5):692-703
pubmed: 20211138
Nucleic Acids Res. 2020 Jan 24;48(2):879-894
pubmed: 31777931
Cell Death Discov. 2020 Nov 27;6(1):133
pubmed: 33298889
Nat Biotechnol. 2019 Aug;37(8):907-915
pubmed: 31375807
Mol Biosyst. 2007 May;3(5):354-60
pubmed: 17460794
Genes Dev. 2007 Jul 1;21(13):1603-8
pubmed: 17606638
RNA. 2009 Apr;15(4):675-85
pubmed: 19240163
Cold Spring Harb Protoc. 2010 Jan;2010(1):pdb.prot5363
pubmed: 20150122
Cold Spring Harb Protoc. 2010 Jan;2010(1):pdb.prot5364
pubmed: 20150123
Curr Biol. 2007 Jul 17;17(14):1265-72
pubmed: 17604629
Nucleic Acids Res. 2009 Feb;37(3):903-15
pubmed: 19103667
Nucleic Acids Res. 2016 Jul 8;44(12):5908-23
pubmed: 27085807
Nucleic Acids Res. 2019 Sep 5;47(15):8036-8049
pubmed: 31251800
BMC Genomics. 2012 Oct 16;13:556
pubmed: 23067041
Nat Commun. 2021 Mar 4;12(1):1441
pubmed: 33664268
Anal Chem. 2010 Mar 15;82(6):2272-81
pubmed: 20166708
Genes Dev. 2006 Jan 1;20(1):28-33
pubmed: 16357212
Nucleic Acids Res. 2011 May;39(10):4249-64
pubmed: 21216825
Nat Rev Genet. 2019 Feb;20(2):89-108
pubmed: 30446728
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
Proteomics. 2010 Mar;10(6):1150-9
pubmed: 20101611
Mol Cell Proteomics. 2011 Dec;10(12):M111.007690
pubmed: 21876204
J Am Soc Mass Spectrom. 2015 Nov;26(11):1865-74
pubmed: 26115965
Nat Commun. 2021 Jun 9;12(1):3492
pubmed: 34108460
J Proteome Res. 2007 Feb;6(2):654-61
pubmed: 17269722
Dev Cell. 2014 Jan 27;28(2):174-88
pubmed: 24439910
Nat Struct Mol Biol. 2005 Apr;12(4):340-9
pubmed: 15800637
Science. 2006 Apr 7;312(5770):75-9
pubmed: 16484454
Genes Dev. 2009 Sep 1;23(17):2016-32
pubmed: 19656801
Nucleic Acids Res. 2006 Jan 30;34(2):667-75
pubmed: 16449203
Cell Mol Life Sci. 2020 Nov;77(22):4615-4629
pubmed: 32462406
Cell. 2005 Nov 18;123(4):607-20
pubmed: 16271386
Mol Cell. 2018 Sep 6;71(5):775-790.e5
pubmed: 30193099
Genes Dev. 2005 Dec 1;19(23):2837-48
pubmed: 16287716
Anal Chem. 2003 Sep 1;75(17):4646-58
pubmed: 14632076

Auteurs

Therese Solberg (T)

Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland.

Victor Mason (V)

Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland.

Chundi Wang (C)

Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland; Institute of Evolution & Marine Biodiversity, Ocean University of China, Qingdao 266003, China.

Mariusz Nowacki (M)

Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland. Electronic address: mariusz.nowacki@unibe.ch.

Articles similaires

Human DCP1 is crucial for mRNA decapping and possesses paralog-specific gene regulating functions.

Ting-Wen Chen, Hsiao-Wei Liao, Michelle Noble et al.
1.00
Humans Endoribonucleases RNA, Messenger RNA Caps Gene Expression Regulation

A cytoplasmic osmosensing mechanism mediated by molecular crowding-sensitive DCP5.

Zhenyu Wang, Qiuhua Yang, Dan Zhang et al.
1.00
Arabidopsis Arabidopsis Proteins Osmotic Pressure Cytoplasm RNA, Messenger

The SARS-CoV-2 ORF6 protein inhibits nuclear export of mRNA and spliceosomal U snRNA.

Ichiro Taniguchi
1.00
Animals Active Transport, Cell Nucleus RNA, Messenger Humans SARS-CoV-2

The mRNA and protein datasets after cold stress of red tilapia.

Lanmei Wang, Haoran Yang, Herbert Brightmore Munyaradzia et al.
1.00
Animals Tilapia Cold-Shock Response RNA, Messenger Transcriptome

Classifications MeSH

questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ARN › ARN non traduit › Petit ARN non traduit › Petit ARN interférent › Developmental mRNA clearance by PIWI-bound...
questionsmedicales.fr › Phénomènes génétiques › Régulation de l'expression des gènes › Épigenèse génétique › Extinction de l'expression des gènes › Interférence par ARN › Developmental mRNA clearance by PIWI-bound...
questionsmedicales.fr › Eucaryotes › Alveolata › Ciliophora › Oligohymenophorea › Hymenostomatida › Peniculina › Paramecium › Developmental mRNA clearance by PIWI-bound...
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ARN › ARN messager › Developmental mRNA clearance by PIWI-bound...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Conformation d'acide nucléique › ARN double brin › Developmental mRNA clearance by PIWI-bound...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Nucléoprotéines › Protéines de liaison à l'ARN › Ribonucléoprotéines › Complexe réprimant l'expression de l'ARN › Protéines Argonaute › Developmental mRNA clearance by PIWI-bound...