Regulation of MicroRNA Machinery and Development by Interspecies S-Nitrosylation.

Animals Argonaute Proteins / genetics Caenorhabditis elegans / genetics Caenorhabditis elegans Proteins / genetics HEK293 Cells HeLa Cells Host Microbial Interactions / genetics Humans MicroRNAs / metabolism Microbiota / genetics Nitric Oxide / metabolism Protein Processing, Post-Translational / genetics Proteome / genetics Proteomics / methods RNA-Binding Proteins / genetics
C. elegans S-nitrosylation development miRNA microbiome nitric oxide

Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
21 02 2019
Historique:
received: 16 07 2018
revised: 20 10 2018
accepted: 23 01 2019
entrez: 23 2 2019
pubmed: 23 2 2019
medline: 7 1 2020
Statut: ppublish

Résumé

Bioactive molecules can pass between microbiota and host to influence host cellular functions. However, general principles of interspecies communication have not been discovered. We show here in C. elegans that nitric oxide derived from resident bacteria promotes widespread S-nitrosylation of the host proteome. We further show that microbiota-dependent S-nitrosylation of C. elegans Argonaute protein (ALG-1)-at a site conserved and S-nitrosylated in mammalian Argonaute 2 (AGO2)-alters its function in controlling gene expression via microRNAs. By selectively eliminating nitric oxide generation by the microbiota or S-nitrosylation in ALG-1, we reveal unforeseen effects on host development. Thus, the microbiota can shape the post-translational landscape of the host proteome to regulate microRNA activity, gene expression, and host development. Our findings suggest a general mechanism by which the microbiota may control host cellular functions, as well as a new role for gasotransmitters.

Identifiants

DOI: 10.1016/j.cell.2019.01.037 PMID: 30794773 PMC: PMC6559381
pubmed: 30794773
pii: S0092-8674(19)30100-X
doi: 10.1016/j.cell.2019.01.037
pmc: PMC6559381
mid: NIHMS1519871
pii:
doi:

Substances chimiques

AGO2 protein, human 0
ALG-1 protein, C elegans 0
Argonaute Proteins 0
Caenorhabditis elegans Proteins 0
MicroRNAs 0
Proteome 0
RNA-Binding Proteins 0
Nitric Oxide 31C4KY9ESH

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

1014-1025.e12

Subventions

Organisme : NHLBI NIH HHS
ID : R01 HL126900
Pays : United States
Organisme : NCATS NIH HHS
ID : TL1 TR002549
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM125086
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM118018
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM080465
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM099921
Pays : United States
Organisme : NHLBI NIH HHS
ID : P01 HL128192
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007250
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK111468
Pays : United States
Organisme : NHLBI NIH HHS
ID : U10 HL109250
Pays : United States
Organisme : NHLBI NIH HHS
ID : R35 HL135789
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK119506
Pays : United States
Organisme : NHLBI NIH HHS
ID : P01 HL075443
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM067945
Pays : United States
Organisme : NIA NIH HHS
ID : F30 AG054237
Pays : United States

Commentaires et corrections

Type : CommentIn
Type : CommentIn

Informations de copyright

Copyright © 2019 Elsevier Inc. All rights reserved.

Références

J Bacteriol. 1988 Jan;170(1):359-64
pubmed: 3275620
Dev Biol. 2003 Jul 15;259(2):364-79
pubmed: 12871707
ISME J. 2016 Aug;10(8):1998-2009
pubmed: 26800234
PLoS Genet. 2016 Dec 9;12(12):e1006484
pubmed: 27935964
Genes (Basel). 2014 Mar 27;5(2):254-69
pubmed: 24705329
Nature. 2011 May 12;473(7346):174-80
pubmed: 21508958
FEBS Lett. 1999 Jul 2;454(1-2):127-30
pubmed: 10413109
Proc Natl Acad Sci U S A. 2013 Oct 1;110(40):E3770-9
pubmed: 24043833
Genetics. 2015 Sep;201(1):47-54
pubmed: 26187122
BMC Bioinformatics. 2007 Apr 20;8:133
pubmed: 17448237
Proc Natl Acad Sci U S A. 2015 Dec 29;112(52):E7213-22
pubmed: 26669440
Proc Natl Acad Sci U S A. 2014 Dec 30;111(52):18572-7
pubmed: 25512491
Cell. 2014 Jan 30;156(3):408-11
pubmed: 24485451
BMC Biol. 2012 Jun 25;10:59
pubmed: 22731941
Adv Med Sci. 2017 Sep;62(2):414-420
pubmed: 28711782
Mol Cell. 2004 Jul 23;15(2):185-97
pubmed: 15260970
Nature. 2001 Feb 1;409(6820):622-6
pubmed: 11214321
J Biol Chem. 2007 May 11;282(19):13977-83
pubmed: 17376775
EMBO J. 2018 Jun 1;37(11):
pubmed: 29712715
Cell Metab. 2006 Apr;3(4):277-87
pubmed: 16581005
Science. 2007 Mar 16;315(5818):1576-9
pubmed: 17322030
Nature. 2000 Feb 24;403(6772):901-6
pubmed: 10706289
Free Radic Biol Med. 2015 Oct;87:252-62
pubmed: 26159506
Free Radic Biol Med. 2018 Aug 20;124:21-30
pubmed: 29807159
Nat Cell Biol. 2005 Jul;7(7):719-23
pubmed: 15937477
Proc Natl Acad Sci U S A. 2018 Apr 10;115(15):E3388-E3397
pubmed: 29581312
Cell. 2018 Jun 14;173(7):1728-1741.e13
pubmed: 29804833
Mol Cell. 2016 Oct 20;64(2):320-333
pubmed: 27720646
Mol Cell. 2018 Feb 1;69(3):451-464.e6
pubmed: 29358078
Nature. 2017 Nov 30;551(7682):648-652
pubmed: 29168502
Mol Cell. 2008 Aug 8;31(3):395-405
pubmed: 18691971
Proteomics. 2009 Apr;9(7):1763-70
pubmed: 19288523
Oral Dis. 2015 Jan;21(1):7-16
pubmed: 23837897
Nature. 2000 Nov 2;408(6808):86-9
pubmed: 11081512
Nat Biotechnol. 2009 Jun;27(6):557-9
pubmed: 19483679
PLoS One. 2012;7(3):e33144
pubmed: 22427970
Dev Cell. 2015 Feb 9;32(3):335-44
pubmed: 25669883
Nature. 2008 Sep 18;455(7211):421-4
pubmed: 18690212
Nature. 1999 Sep 30;401(6752):497-502
pubmed: 10519555
Antioxid Redox Signal. 2019 Apr 1;30(10):1331-1351
pubmed: 29130312
Curr Hypertens Rep. 2017 Apr;19(4):33
pubmed: 28353075
Cell. 2014 Nov 6;159(4):789-99
pubmed: 25417156
Nat Rev Genet. 2012 Mar 13;13(4):260-70
pubmed: 22411464
PLoS One. 2010 Jun 24;5(6):e11290
pubmed: 20585580
Mol Cell. 2013 May 9;50(3):356-67
pubmed: 23603119
Cell. 2013 Feb 14;152(4):818-30
pubmed: 23415229
Cell. 2001 Jul 13;106(1):23-34
pubmed: 11461699
WormBook. 2006 Feb 11;:1-11
pubmed: 18050451
Cell. 2016 Dec 1;167(6):1469-1480.e12
pubmed: 27912057
Free Radic Biol Med. 2016 Dec;101:226-235
pubmed: 27769921
Nat Chem Biol. 2009 Dec;5(12):865-9
pubmed: 19915529
J Biol Chem. 2002 May 3;277(18):16167-71
pubmed: 11856757
Mol Cell. 2017 Aug 17;67(4):646-658.e3
pubmed: 28781232
J Biol Chem. 2012 Feb 10;287(7):4411-8
pubmed: 22147701
Circ Res. 2012 Mar 2;110(5):652-4
pubmed: 22383706
EMBO J. 2016 Jun 1;35(11):1186-203
pubmed: 27009120
BMC Biol. 2016 May 09;14:38
pubmed: 27160191
Cell Syst. 2017 Mar 22;4(3):291-305.e7
pubmed: 28189581
RNA. 2009 May;15(5):804-13
pubmed: 19324964
J Mol Biol. 2010 Jan 29;395(4):844-59
pubmed: 19854201
Science. 2015 Jul 24;349(6246):1254766
pubmed: 26206939
Nat Chem Biol. 2014 Jun;10(6):416-24
pubmed: 24838170
Appl Environ Microbiol. 1988 Jul;54(7):1791-4
pubmed: 3046492
Cell. 2013 Mar 28;153(1):228-39
pubmed: 23540700
Science. 2004 Sep 3;305(5689):1437-41
pubmed: 15284456
PLoS One. 2012;7(3):e33750
pubmed: 22448270
Bioinformatics. 2009 May 15;25(10):1341-3
pubmed: 19304874
Curr Opin Microbiol. 2017 Aug;38:142-147
pubmed: 28623729
J Biol Chem. 2019 Feb 1;294(5):1568-1578
pubmed: 30538128
Science. 2012 Apr 27;336(6080):470-3
pubmed: 22539721
Nature. 2019 Jan;565(7737):96-100
pubmed: 30487609
J Neurochem. 2010 Apr;113(1):14-26
pubmed: 20067586
Sci STKE. 2001 Jun 12;2001(86):pl1
pubmed: 11752655
Methods Cell Biol. 2011;106:289-322
pubmed: 22118282
Sci Signal. 2015 Jul 07;8(384):ra68
pubmed: 26152695
Cell. 2017 Jun 15;169(7):1249-1262.e13
pubmed: 28622510
Mol Cell. 2000 Apr;5(4):659-69
pubmed: 10882102
Genes Dev. 2004 Jan 15;18(2):132-7
pubmed: 14729570
Gut. 1997 Feb;40(2):211-4
pubmed: 9071933
Elife. 2018 Jul 17;7:
pubmed: 30014846

Auteurs

Puneet Seth (P)

Institute for Transformative Molecular Medicine and Department of Medicine, Case Western Reserve University School of Medicine and University Hospitals Cleveland Medical Center, Cleveland, OH 44106, USA.

Paishiun N Hsieh (PN)

Department of Medicine, Case Cardiovascular Research Institute, Case Western Reserve University, 10900 Euclid Avenue, Cleveland, OH 44106, USA; Harrington Heart and Vascular Institute, University Hospitals Cleveland Medical Center, 2103 Cornell Road, Cleveland, OH 44106, USA; Department of Pathology, Case Western Reserve University, 10900 Euclid Avenue, Cleveland, OH 44106, USA.

Suhib Jamal (S)

Institute for Transformative Molecular Medicine and Department of Medicine, Case Western Reserve University School of Medicine and University Hospitals Cleveland Medical Center, Cleveland, OH 44106, USA.

Liwen Wang (L)

Center for Proteomics and Bioinformatics, Case Western Reserve University School of Medicine, Cleveland, OH 44106, USA.

Steven P Gygi (SP)

Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA.

Mukesh K Jain (MK)

Department of Medicine, Case Cardiovascular Research Institute, Case Western Reserve University, 10900 Euclid Avenue, Cleveland, OH 44106, USA; Harrington Heart and Vascular Institute, University Hospitals Cleveland Medical Center, 2103 Cornell Road, Cleveland, OH 44106, USA; Harrington Discovery Institute, University Hospitals Cleveland Medical Center, Cleveland, OH 44106, USA.

Jeff Coller (J)

Center for RNA Science and Therapeutics, Case Western Reserve University, Cleveland, OH 44106, USA.

Jonathan S Stamler (JS)

Institute for Transformative Molecular Medicine and Department of Medicine, Case Western Reserve University School of Medicine and University Hospitals Cleveland Medical Center, Cleveland, OH 44106, USA; Harrington Discovery Institute, University Hospitals Cleveland Medical Center, Cleveland, OH 44106, USA. Electronic address: jonathan.stamler@case.edu.

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Regulation of MicroRNA Machinery and...
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 › Regulation of MicroRNA Machinery and...
questionsmedicales.fr › Eucaryotes › Animaux › Invertébrés › Helminthes › Nematoda › Chromadorea › Rhabditida › Rhabditoidea › Caenorhabditis › Caenorhabditis elegans › Regulation of MicroRNA Machinery and...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines d'helminthes › Protéines de Caenorhabditis elegans › Regulation of MicroRNA Machinery and...
questionsmedicales.fr › Cellules › Cellules épithéliales › Cellules HEK293 › Regulation of MicroRNA Machinery and...
questionsmedicales.fr › Cellules › Cellules épithéliales › Cellules HeLa › Regulation of MicroRNA Machinery and...
questionsmedicales.fr › Phénomènes biologiques › Interactions hôte-microbes › Regulation of MicroRNA Machinery and...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Regulation of MicroRNA Machinery and...
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ARN › ARN non traduit › Petit ARN non traduit › microARN › Regulation of MicroRNA Machinery and...
questionsmedicales.fr › Environnement et santé publique › Environnement › Écosystème › Biodiversité › Biote › Microbiote › Regulation of MicroRNA Machinery and...
questionsmedicales.fr › Produits chimiques inorganiques › Composés de l'oxygène › Oxydes › Oxydes d'azote › Monoxyde d'azote › Regulation of MicroRNA Machinery and...
questionsmedicales.fr › Phénomènes génétiques › Régulation de l'expression des gènes › Modification traductionnelle des protéines › Maturation post-traductionnelle des protéines › Regulation of MicroRNA Machinery and...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéome › Regulation of MicroRNA Machinery and...
questionsmedicales.fr › Disciplines des sciences naturelles › Chimie › Biochimie › Protéomique › Regulation of MicroRNA Machinery and...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Nucléoprotéines › Protéines de liaison à l'ARN › Regulation of MicroRNA Machinery and...