Gene- and Species-Specific Hox mRNA Translation by Ribosome Expansion Segments.

5' Untranslated Regions / genetics Gene Expression Regulation / genetics Genes, Homeobox / genetics Homeodomain Proteins / genetics Nucleic Acid Conformation Protein Biosynthesis / genetics RNA, Messenger / genetics RNA, Ribosomal / genetics Ribosomes / genetics Saccharomyces cerevisiae / genetics Species Specificity
ES9S Hox cluster RNA structure RNA-protein interaction expansion segment internal initiation internal ribosome entry site mRNA translation ribosomal RNA ribosome ribosome engineering stem-loop yeast

Journal

Molecular cell
ISSN: 1097-4164
Titre abrégé: Mol Cell
Pays: United States
ID NLM: 9802571

Informations de publication

Date de publication:
17 12 2020
Historique:
received: 25 05 2020
revised: 13 10 2020
accepted: 15 10 2020
pubmed: 18 11 2020
medline: 16 1 2021
entrez: 17 11 2020
Statut: ppublish

Résumé

Ribosomes have been suggested to directly control gene regulation, but regulatory roles for ribosomal RNA (rRNA) remain largely unexplored. Expansion segments (ESs) consist of multitudes of tentacle-like rRNA structures extending from the core ribosome in eukaryotes. ESs are remarkably variable in sequence and size across eukaryotic evolution with largely unknown functions. In characterizing ribosome binding to a regulatory element within a Homeobox (Hox) 5' UTR, we identify a modular stem-loop within this element that binds to a single ES, ES9S. Engineering chimeric, "humanized" yeast ribosomes for ES9S reveals that an evolutionary change in the sequence of ES9S endows species-specific binding of Hoxa9 mRNA to the ribosome. Genome editing to site-specifically disrupt the Hoxa9-ES9S interaction demonstrates the functional importance for such selective mRNA-rRNA binding in translation control. Together, these studies unravel unexpected gene regulation directly mediated by rRNA and how ribosome evolution drives translation of critical developmental regulators.

Identifiants

DOI: 10.1016/j.molcel.2020.10.023 PMID: 33202249 PMC: PMC7769145
pubmed: 33202249
pii: S1097-2765(20)30730-9
doi: 10.1016/j.molcel.2020.10.023
pmc: PMC7769145
mid: NIHMS1646088
pii:
doi:

Substances chimiques

5' Untranslated Regions 0
Homeodomain Proteins 0
RNA, Messenger 0
RNA, Ribosomal 0
homeobox protein HOXA9 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

980-995.e13

Subventions

Organisme : NICHD NIH HHS
ID : R01 HD086634
Pays : United States

Informations de copyright

Copyright © 2020 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Interest K.L. and M.B. are inventors on patents and submitted provisional patent applications related to the Hoxa9 P4 stem-loop and RNA therapeutics and their various uses.

Références

Genesis. 2019 Jul;57(7-8):e23306
pubmed: 31111645
Mol Cell Biol. 1989 Feb;9(2):551-9
pubmed: 2540422
J Struct Biol. 1999 Dec 1;128(1):82-97
pubmed: 10600563
Proc Natl Acad Sci U S A. 2005 Sep 20;102(38):13421-6
pubmed: 16174738
Development. 2013 Oct;140(19):3951-63
pubmed: 24046316
Nucleic Acids Res. 1996 Dec 1;24(23):4817-24
pubmed: 8972871
Genes Dev. 2009 Apr 15;23(8):963-74
pubmed: 19390089
Proc Natl Acad Sci U S A. 1975 Dec;72(12):4734-8
pubmed: 1107998
J Comput Chem. 2004 Oct;25(13):1605-12
pubmed: 15264254
Cell. 1989 May 19;57(4):525-9
pubmed: 2655923
Cell. 2017 Jun 1;169(6):1051-1065.e18
pubmed: 28575669
Electrophoresis. 1999 Dec;20(18):3551-67
pubmed: 10612281
J Struct Biol. 2016 Jan;193(1):1-12
pubmed: 26592709
PLoS One. 2008 Mar 26;3(3):e1843
pubmed: 18365001
Dev Biol. 1987 May;121(1):1-9
pubmed: 3569655
Cancers (Basel). 2019 Mar 07;11(3):
pubmed: 30866492
Nucleic Acids Res. 2014 Jan;42(2):e13
pubmed: 24157833
Proc Natl Acad Sci U S A. 2010 Nov 16;107(46):19748-53
pubmed: 20980660
Cell. 2013 May 9;153(4):869-81
pubmed: 23663784
Nature. 1990 Aug 23;346(6286):763-6
pubmed: 1975088
RNA. 2016 Aug;22(8):1153-62
pubmed: 27317789
Wiley Interdiscip Rev RNA. 2012 Mar-Apr;3(2):195-212
pubmed: 22215521
Mol Cell. 2014 May 8;54(3):407-417
pubmed: 24746697
Methods Enzymol. 2007;430:111-45
pubmed: 17913637
Proc Natl Acad Sci U S A. 1974 Apr;71(4):1342-6
pubmed: 4598299
Proc Natl Acad Sci U S A. 2002 Sep 17;99(19):12031-6
pubmed: 12221294
Nucleic Acids Res. 1993 Mar 25;21(6):1449-55
pubmed: 8464736
Mol Cell. 2018 Dec 20;72(6):1013-1020.e6
pubmed: 30576652
Science. 2018 Apr 20;360(6386):323-327
pubmed: 29567807
Mol Cell Biol. 1994 Jun;14(6):4203-15
pubmed: 8196658
Cell. 2009 Feb 20;136(4):731-45
pubmed: 19239892
RNA. 1997 May;3(5):476-88
pubmed: 9149229
Development. 1992 Oct;116(2):357-68
pubmed: 1363087
Nat Biotechnol. 2015 Jan;33(1):73-80
pubmed: 25357182
Nature. 2017 Nov 23;551(7681):472-477
pubmed: 29143818
Nucleic Acids Res. 2013 Oct;41(18):8706-14
pubmed: 23873958
Elife. 2018 Jun 01;7:
pubmed: 29856314
Nat Commun. 2015 Jul 08;6:7646
pubmed: 26155016
Nat Rev Mol Cell Biol. 2018 Mar;19(3):158-174
pubmed: 29165424
Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501
pubmed: 20383002
Nat Rev Drug Discov. 2018 Apr;17(4):261-279
pubmed: 29326426
Development. 2019 Jul 4;146(13):
pubmed: 31273085
Mol Cell. 2015 Feb 5;57(3):433-44
pubmed: 25578875
Sci Adv. 2018 Feb 28;4(2):eaao0665
pubmed: 29503865
Nucleic Acids Res. 1991 Oct 25;19(20):5497-506
pubmed: 1682879
Proc Natl Acad Sci U S A. 1991 May 1;88(9):3962-6
pubmed: 2023944
J Struct Biol. 2005 Oct;152(1):36-51
pubmed: 16182563
Biol Reprod. 2006 May;74(5):807-15
pubmed: 16421232
Cell. 1994 Jul 29;78(2):191-201
pubmed: 7913880
Dev Dyn. 1995 Mar;202(3):312-23
pubmed: 7780180
Cold Spring Harb Perspect Biol. 2019 Jun 3;11(6):
pubmed: 30082467
Nucleic Acids Res. 1994 Nov 25;22(23):5139-47
pubmed: 7800512
Cell. 2011 Apr 29;145(3):383-397
pubmed: 21529712
J Biol Chem. 2008 Nov 28;283(48):33087-93
pubmed: 18832380
Cell. 2007 Jan 26;128(2):257-67
pubmed: 17254965
Mol Cell Biol. 2010 Sep;30(17):4308-23
pubmed: 20584987
Proc Natl Acad Sci U S A. 1998 Oct 13;95(21):12238-43
pubmed: 9770470
J Biol Chem. 2010 Oct 15;285(42):32200-12
pubmed: 20699223
Stem Cells. 2014 Jun;32(6):1451-8
pubmed: 25099890
Nat Struct Mol Biol. 2006 Jan;13(1):30-4
pubmed: 16341227
Elife. 2017 Jul 18;6:
pubmed: 28718767
Proc Natl Acad Sci U S A. 2014 Oct 28;111(43):15385-9
pubmed: 25313046
Nature. 2013 May 2;497(7447):80-5
pubmed: 23636399
Nucleic Acids Res. 2013 Sep;41(16):7625-34
pubmed: 23804757
J Struct Biol. 2003 Jun;142(3):334-47
pubmed: 12781660
Nature. 2015 Jan 1;517(7532):33-8
pubmed: 25409156
Science. 2014 Nov 28;346(6213):1258096
pubmed: 25430774
J Virol. 2011 Jan;85(2):853-64
pubmed: 21068241
Nat Methods. 2017 Apr;14(4):331-332
pubmed: 28250466
Front Genet. 2018 Mar 07;9:66
pubmed: 29563925
Nature. 2013 Jul 25;499(7459):471-5
pubmed: 23823723
Nat Protoc. 2013 Nov;8(11):2281-2308
pubmed: 24157548
Mol Cell. 2017 Jul 6;67(1):71-83.e7
pubmed: 28625553
Science. 2003 Jul 18;301(5631):331-3
pubmed: 12869751
Mol Cell. 2018 Aug 2;71(3):364-374
pubmed: 30075139
Anal Chem. 2003 Apr 15;75(8):1895-904
pubmed: 12713048
Nucleic Acids Res. 2000 Sep 15;28(18):3524-34
pubmed: 10982872
Genome Res. 2015 Aug;25(8):1229-43
pubmed: 26025802
Nat Commun. 2016 Aug 24;7:12622
pubmed: 27554013
Science. 2006 May 12;312(5775):902-6
pubmed: 16690864
J Struct Biol. 2012 Dec;180(3):519-30
pubmed: 23000701

Auteurs

Kathrin Leppek (K)

Department of Developmental Biology, Stanford University, Stanford, CA 94305, USA; Department of Genetics, Stanford University, Stanford, CA 94305, USA.

Kotaro Fujii (K)

Department of Developmental Biology, Stanford University, Stanford, CA 94305, USA; Department of Genetics, Stanford University, Stanford, CA 94305, USA.

Nick Quade (N)

Department of Biology, Institute of Molecular Biology and Biophysics, Otto-Stern-Weg 5, ETH Zürich, Zürich 8093, Switzerland.

Teodorus Theo Susanto (TT)

Department of Developmental Biology, Stanford University, Stanford, CA 94305, USA; Department of Genetics, Stanford University, Stanford, CA 94305, USA.

Daniel Boehringer (D)

Department of Biology, Institute of Molecular Biology and Biophysics, Otto-Stern-Weg 5, ETH Zürich, Zürich 8093, Switzerland.

Tea Lenarčič (T)

Department of Biology, Institute of Molecular Biology and Biophysics, Otto-Stern-Weg 5, ETH Zürich, Zürich 8093, Switzerland.

Shifeng Xue (S)

Department of Developmental Biology, Stanford University, Stanford, CA 94305, USA; Department of Genetics, Stanford University, Stanford, CA 94305, USA.

Naomi R Genuth (NR)

Department of Developmental Biology, Stanford University, Stanford, CA 94305, USA; Department of Genetics, Stanford University, Stanford, CA 94305, USA.

Nenad Ban (N)

Department of Biology, Institute of Molecular Biology and Biophysics, Otto-Stern-Weg 5, ETH Zürich, Zürich 8093, Switzerland. Electronic address: ban@mol.biol.ethz.ch.

Maria Barna (M)

Department of Developmental Biology, Stanford University, Stanford, CA 94305, USA; Department of Genetics, Stanford University, Stanford, CA 94305, USA. Electronic address: mbarna@stanford.edu.

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Classifications MeSH

questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Composants de génome › Gènes › Composants de gène › Régions non traduites › Régions 5' non traduites › Gene- and Species-Specific Hox mRNA...
questionsmedicales.fr › Phénomènes génétiques › Régulation de l'expression des gènes › Gene- and Species-Specific Hox mRNA...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Composants de génome › Gènes › Gènes du développement › Gènes homéotiques › Gene- and Species-Specific Hox mRNA...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines de liaison à l'ADN › Protéines à homéodomaine › Gene- and Species-Specific Hox mRNA...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Conformation d'acide nucléique › Gene- and Species-Specific Hox mRNA...
questionsmedicales.fr › Phénomènes génétiques › Expression des gènes › Biosynthèse des protéines › Gene- and Species-Specific Hox mRNA...
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ARN › ARN messager › Gene- and Species-Specific Hox mRNA...
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ARN › ARN ribosomique › Gene- and Species-Specific Hox mRNA...
questionsmedicales.fr › Cellules › Structures cellulaires › Espace intracellulaire › Cytoplasme › Structures cytoplasmiques › Organites › Ribosomes › Gene- and Species-Specific Hox mRNA...
questionsmedicales.fr › Eucaryotes › Champignons › Levures › Saccharomyces › Saccharomyces cerevisiae › Gene- and Species-Specific Hox mRNA...
questionsmedicales.fr › Phénomènes biologiques › Spécificité d'espèce › Gene- and Species-Specific Hox mRNA...