Myg1 exonuclease couples the nuclear and mitochondrial translational programs through RNA processing.
Animals
Cell Nucleolus
/ metabolism
Cell Nucleus
/ metabolism
Endoribonucleases
/ metabolism
Exonucleases
/ metabolism
Humans
Mice
Mitochondria
/ genetics
Mitochondrial Proteins
/ metabolism
Nuclear Proteins
/ metabolism
Protein Biosynthesis
Proteins
/ metabolism
Quality Control
RNA, Ribosomal
/ metabolism
Ribosomes
/ metabolism
Saccharomyces cerevisiae
/ genetics
Sequence Analysis, DNA
Vitiligo
/ genetics
Journal
Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011
Informations de publication
Date de publication:
20 06 2019
20 06 2019
Historique:
accepted:
30
04
2019
revised:
12
04
2019
received:
12
09
2018
pubmed:
14
5
2019
medline:
4
12
2019
entrez:
14
5
2019
Statut:
ppublish
Résumé
Semi-autonomous functioning of mitochondria in eukaryotic cell necessitates coordination with nucleus. Several RNA species fine-tune mitochondrial processes by synchronizing with the nuclear program, however the involved components remain enigmatic. In this study, we identify a widely conserved dually localized protein Myg1, and establish its role as a 3'-5' RNA exonuclease. We employ mouse melanoma cells, and knockout of the Myg1 ortholog in Saccharomyces cerevisiae with complementation using human Myg1 to decipher the conserved role of Myg1 in selective RNA processing. Localization of Myg1 to nucleolus and mitochondrial matrix was studied through imaging and confirmed by sub-cellular fractionation studies. We developed Silexoseqencing, a methodology to map the RNAse trail at single-nucleotide resolution, and identified in situ cleavage by Myg1 on specific transcripts in the two organelles. In nucleolus, Myg1 processes pre-ribosomal RNA involved in ribosome assembly and alters cytoplasmic translation. In mitochondrial matrix, Myg1 processes 3'-termini of the mito-ribosomal and messenger RNAs and controls translation of mitochondrial proteins. We provide a molecular link to the possible involvement of Myg1 in chronic depigmenting disorder vitiligo. Our study identifies a key component involved in regulating spatially segregated organellar RNA processing and establishes the evolutionarily conserved ribonuclease as a coordinator of nucleo-mitochondrial crosstalk.
Identifiants
pubmed: 31081026
pii: 5488530
doi: 10.1093/nar/gkz371
pmc: PMC6582341
doi:
Substances chimiques
MYG1 protein, mouse
0
Mitochondrial Proteins
0
Nuclear Proteins
0
Proteins
0
RNA, Ribosomal
0
Endoribonucleases
EC 3.1.-
Exonucleases
EC 3.1.-
MYG1 protein, human
EC 3.1.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
5852-5866Informations de copyright
© The Author(s) 2019. Published by Oxford University Press on behalf of Nucleic Acids Research.
Références
Cell. 2007 Nov 2;131(3):557-71
pubmed: 17981122
Philos Trans R Soc Lond B Biol Sci. 2015 Sep 26;370(1678):20140330
pubmed: 26323761
Cell. 2016 Oct 20;167(3):722-738.e23
pubmed: 27768893
Mol Cell. 2018 Mar 1;69(5):757-772.e7
pubmed: 29499132
Proc Natl Acad Sci U S A. 2009 Jun 16;106(24):9613-8
pubmed: 19482942
Nucleic Acids Res. 2017 Dec 1;45(21):12469-12480
pubmed: 29040705
Genome Biol. 2014 Jan 07;15(1):R8
pubmed: 24393166
Nucleic Acids Res. 2002 Aug 15;30(16):3592-601
pubmed: 12177301
J Investig Dermatol Symp Proc. 1999 Sep;4(1):91-6
pubmed: 10537016
J Dermatol Sci. 2009 Jun;54(3):157-67
pubmed: 19282153
Nucleic Acids Res. 2017 May 19;45(9):5487-5500
pubmed: 28201688
Cell Cycle. 2015;14(14):2226-50
pubmed: 26030272
J Cell Biol. 2016 Mar 14;212(6):611-4
pubmed: 26953349
Trends Cell Biol. 2000 May;10(5):189-96
pubmed: 10754561
Mol Cell. 2013 Aug 22;51(4):539-51
pubmed: 23973377
Cell Rep. 2013 Nov 14;5(3):839-48
pubmed: 24183674
Sci Rep. 2017 Oct 20;7(1):13663
pubmed: 29057950
J Dermatol Sci. 2013 Sep;71(3):195-202
pubmed: 23706493
Science. 2017 May 26;356(6340):
pubmed: 28495876
Oxid Med Cell Longev. 2014;2014:541230
pubmed: 24876913
Sci Rep. 2017 Aug 29;7(1):9860
pubmed: 28852211
Biol Cell. 2009 Jun;101(6):361-73
pubmed: 19014353
RNA. 2011 Apr;17(4):761-72
pubmed: 21343387
Science. 2015 Apr 3;348(6230):95-98
pubmed: 25838379
Trends Endocrinol Metab. 2012 Sep;23(9):459-66
pubmed: 22817841
Nat Cell Biol. 2018 Feb;20(2):162-174
pubmed: 29335528
J Invest Dermatol. 2010 Dec;130(12):2781-9
pubmed: 20664557
Nucleic Acids Res. 2011 Sep 1;39(17):7750-63
pubmed: 21666256
Neurobiol Aging. 2008 Jul;29(7):1080-92
pubmed: 17363114
Nature. 2016 May 11;533(7604):499-503
pubmed: 27225121
Pigment Cell Res. 2003 Oct;16(5):553-9
pubmed: 12950736
Behav Brain Res. 2010 Feb 11;207(1):182-95
pubmed: 19818808
Curr Opin Microbiol. 2013 Oct;16(5):652-8
pubmed: 23932204
EMBO J. 2005 Aug 17;24(16):2862-72
pubmed: 16037817
Nucleic Acids Res. 2016 Jan 4;44(D1):D1251-7
pubmed: 26450961
J Cell Biol. 2018 Jan 2;217(1):117-126
pubmed: 29118025
Cell. 2011 Aug 19;146(4):645-58
pubmed: 21854988
J Dermatol Sci. 2006 Nov;44(2):119-22
pubmed: 16996721
Cell. 2018 Jun 28;174(1):187-201.e12
pubmed: 29779946
Cell Metab. 2014 Apr 1;19(4):618-29
pubmed: 24703694
Cell. 2010 Aug 6;142(3):456-67
pubmed: 20691904
Genes Brain Behav. 2004 Apr;3(2):80-9
pubmed: 15005716
J Invest Dermatol. 2001 Jan;116(1):167-74
pubmed: 11168813
Cell. 2009 Feb 20;136(4):763-76
pubmed: 19239894
Cell Rep. 2014 May 8;7(3):918-31
pubmed: 24746820
Cell Metab. 2006 Dec;4(6):453-64
pubmed: 17141629
Trends Biochem Sci. 1998 Jan;23(1):17-9
pubmed: 9478130