Structural basis for Gemin5 decamer-mediated mRNA binding.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
02 09 2022
Historique:
received: 10 04 2022
accepted: 23 08 2022
entrez: 2 9 2022
pubmed: 3 9 2022
medline: 9 9 2022
Statut: epublish

Résumé

Gemin5 in the Survival Motor Neuron (SMN) complex serves as the RNA-binding protein to deliver small nuclear RNAs (snRNAs) to the small nuclear ribonucleoprotein Sm complex via its N-terminal WD40 domain. Additionally, the C-terminal region plays an important role in regulating RNA translation by directly binding to viral RNAs and cellular mRNAs. Here, we present the three-dimensional structure of the Gemin5 C-terminal region, which adopts a homodecamer architecture comprised of a dimer of pentamers. By structural analysis, mutagenesis, and RNA-binding assays, we find that the intact pentamer/decamer is critical for the Gemin5 C-terminal region to bind cognate RNA ligands and to regulate mRNA translation. The Gemin5 high-order architecture is assembled via pentamerization, allowing binding to RNA ligands in a coordinated manner. We propose a model depicting the regulatory role of Gemin5 in selective RNA binding and translation. Therefore, our work provides insights into the SMN complex-independent function of Gemin5.

Identifiants

pubmed: 36056043
doi: 10.1038/s41467-022-32883-z
pii: 10.1038/s41467-022-32883-z
pmc: PMC9440017
doi:

Substances chimiques

Ligands 0
RNA, Messenger 0
RNA, Small Nuclear 0
Ribonucleoproteins, Small Nuclear 0
SMN Complex Proteins 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

5166

Informations de copyright

© 2022. The Author(s).

Références

Cell. 2020 Dec 23;183(7):1801-1812.e13
pubmed: 33308477
J Comput Chem. 2004 Oct;25(13):1605-12
pubmed: 15264254
Cell. 2021 Sep 2;184(18):4680-4696.e22
pubmed: 34380047
RNA Biol. 2020 Sep;17(9):1331-1341
pubmed: 32476560
Genes Dev. 2016 Nov 1;30(21):2376-2390
pubmed: 27881600
Nucleic Acids Res. 2014 May;42(9):5742-54
pubmed: 24598255
Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32
pubmed: 15572765
Nat Commun. 2020 May 29;11(1):2677
pubmed: 32472050
Nat Methods. 2017 Apr;14(4):331-332
pubmed: 28250466
J Proteome Res. 2006 Jun;5(6):1367-78
pubmed: 16739988
Nat Methods. 2012 Jul;9(7):671-5
pubmed: 22930834
Nature. 2020 Jul;583(7818):711-719
pubmed: 32728246
Nat Rev Mol Cell Biol. 2007 Oct;8(10):761-73
pubmed: 17786152
RNA Biol. 2021 Oct 15;18(sup1):496-506
pubmed: 34424823
Biomolecules. 2015 Apr 17;5(2):528-44
pubmed: 25898402
Bioessays. 2019 Apr;41(4):e1800241
pubmed: 30919488
Genes Dev. 2016 Nov 1;30(21):2391-2403
pubmed: 27881601
J Biol Chem. 2015 Jun 19;290(25):15662-15669
pubmed: 25911097
Sci Rep. 2018 Apr 3;8(1):5545
pubmed: 29615727
J Struct Biol. 2015 Nov;192(2):216-21
pubmed: 26278980
Nature. 2022 Apr;604(7904):184-189
pubmed: 35114687
Mol Cell. 2018 Dec 20;72(6):1035-1049.e5
pubmed: 30503769
Nat Methods. 2017 Mar;14(3):290-296
pubmed: 28165473
Bioessays. 2010 Dec;32(12):1077-89
pubmed: 20954180
Mol Cell. 2019 Apr 4;74(1):196-211.e11
pubmed: 30799147
Nucleic Acids Res. 2018 Aug 21;46(14):7339-7353
pubmed: 29771365
Trends Biochem Sci. 2017 May;42(5):369-382
pubmed: 28268044
Curr Opin Cell Biol. 2002 Jun;14(3):305-12
pubmed: 12067652
Nucleic Acids Res. 2012 Jun;40(11):4942-53
pubmed: 22362733
EMBO J. 2015 Jul 14;34(14):1925-41
pubmed: 26069323
Nat Struct Mol Biol. 2009 May;16(5):486-91
pubmed: 19377484
Nucleic Acids Res. 2013 Jan;41(2):1017-28
pubmed: 23221641
RNA. 2001 Sep;7(9):1213-26
pubmed: 11565745
Nucleic Acids Res. 2009 Feb;37(2):582-90
pubmed: 19066202
Wiley Interdiscip Rev RNA. 2018 May;9(3):e1465
pubmed: 29341429
Nat Commun. 2021 May 7;12(1):2558
pubmed: 33963192
Science. 2002 Nov 29;298(5599):1775-9
pubmed: 12459587
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21
pubmed: 20124702
Life Sci Alliance. 2022 Apr 7;5(7):
pubmed: 35393353
Cell Res. 2016 Dec;26(12):1353-1356
pubmed: 27834343
Nucleic Acids Res. 2020 Jan 24;48(2):788-801
pubmed: 31799608
Clin Genet. 2021 Dec;100(6):722-730
pubmed: 34569062
Front Cell Dev Biol. 2022 Feb 28;10:783762
pubmed: 35295849
Mol Cell. 2010 May 28;38(4):551-62
pubmed: 20513430
J Proteome Res. 2021 Jun 4;20(6):3165-3178
pubmed: 33939924
J Biol Chem. 2007 Sep 21;282(38):27953-9
pubmed: 17640873
Mol Cell. 2006 Jul 21;23(2):273-9
pubmed: 16857593
Structure. 2000 May 15;8(5):505-14
pubmed: 10801492
J Biol Chem. 2002 Feb 15;277(7):5631-6
pubmed: 11714716

Auteurs

Qiong Guo (Q)

MOE Key Laboratory for Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, 230027, Hefei, China.

Shidong Zhao (S)

MOE Key Laboratory for Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, 230027, Hefei, China.

Rosario Francisco-Velilla (R)

Centro de Biología Molecular Severo Ochoa, CSIC-UAM, Nicolás Cabrera 1, 28049, Madrid, Spain.

Jiahai Zhang (J)

MOE Key Laboratory for Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, 230027, Hefei, China.

Azman Embarc-Buh (A)

Centro de Biología Molecular Severo Ochoa, CSIC-UAM, Nicolás Cabrera 1, 28049, Madrid, Spain.

Salvador Abellan (S)

Centro de Biología Molecular Severo Ochoa, CSIC-UAM, Nicolás Cabrera 1, 28049, Madrid, Spain.

Mengqi Lv (M)

MOE Key Laboratory for Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, 230027, Hefei, China.

Peiping Tang (P)

MOE Key Laboratory for Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, 230027, Hefei, China.

Qingguo Gong (Q)

MOE Key Laboratory for Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, 230027, Hefei, China.

Huaizong Shen (H)

Key Laboratory of Structural Biology of Zhejiang Province, School of Life Sciences, Westlake University, 310024, Hangzhou, Zhejiang, China.

Linfeng Sun (L)

MOE Key Laboratory for Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, 230027, Hefei, China.

Xuebiao Yao (X)

MOE Key Laboratory for Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, 230027, Hefei, China.

Jinrong Min (J)

Structural Genomics Consortium, University of Toronto, Toronto, ON, M5G 1L7, Canada.
Department of Physiology, University of Toronto, Toronto, ON, M5S 1A8, Canada.

Yunyu Shi (Y)

MOE Key Laboratory for Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, 230027, Hefei, China.

Encarnacion Martínez-Salas (E)

Centro de Biología Molecular Severo Ochoa, CSIC-UAM, Nicolás Cabrera 1, 28049, Madrid, Spain. emartinez@cbm.csic.es.

Kaiming Zhang (K)

MOE Key Laboratory for Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, 230027, Hefei, China. kmzhang@ustc.edu.cn.

Chao Xu (C)

MOE Key Laboratory for Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, 230027, Hefei, China. xuchaor@ustc.edu.cn.

Articles similaires

Humans Endoribonucleases RNA, Messenger RNA Caps Gene Expression Regulation
Arabidopsis Arabidopsis Proteins Osmotic Pressure Cytoplasm RNA, Messenger

Conservation of the cooling agent binding pocket within the TRPM subfamily.

Kate Huffer, Matthew C S Denley, Elisabeth V Oskoui et al.
1.00
TRPM Cation Channels Animals Binding Sites Mice Pyrimidinones
Fucosyltransferases Drug Repositioning Molecular Docking Simulation Molecular Dynamics Simulation Humans

Classifications MeSH