From powerhouse to processing plant: conserved roles of mitochondrial outer membrane proteins in tRNA splicing

Wan, Yao; Hopper, Anita K.

doi:10.1101/gad.316257.118

Title: From powerhouse to processing plant: conserved roles of mitochondrial outer membrane proteins in tRNA splicing

Abstract

The mitochondrial cytoplasmic surface serves as a processing site for numerous RNAs from budding yeast to metazoans. We report that budding yeast mitochondrial outer membrane (MOM) proteins that are subunits of the translocase of the outer mitochondrial membrane (Tom70 and Tom 22) and sorting and assembly machinery (Sam37) are required for efficient pretransfer RNA (pre-tRNA) splicing. Defective pre-tRNA splicing in MOM mutants is due not to loss of respiratory metabolism but instead inefficient targeting/tethering of tRNA splicing endonuclease (SEN) subunits to mitochondria. Schizosaccharomyces pombe SEN subunits also localize to mitochondria, and Tom70 is required for this localization and pre-tRNA splicing. Thus, the role of MOM protein in targeting/tethering SEN subunits to mitochondria has been conserved for >500 million years.

Authors:

Wan, Yao ^[1]; Hopper, Anita K. ^[1]

The Ohio State Univ., Columbus, OH (United States)

Publication Date:: Tue Sep 18 00:00:00 EDT 2018

Research Org.:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC)

OSTI Identifier:: 1560569

Grant/Contract Number:: AC02-05CH11231

Resource Type:: Accepted Manuscript

Journal Name:: Genes & Development

Additional Journal Information:: Journal Volume: 32; Journal Issue: 19-20; Journal ID: ISSN 0890-9369

Publisher:: Cold Springs Harbor Press

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Wan, Yao, and Hopper, Anita K. From powerhouse to processing plant: conserved roles of mitochondrial outer membrane proteins in tRNA splicing.  United States: N. p., 2018. 
Web.  doi:10.1101/gad.316257.118.

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                    Wan, Yao, & Hopper, Anita K. From powerhouse to processing plant: conserved roles of mitochondrial outer membrane proteins in tRNA splicing.  United States.  https://doi.org/10.1101/gad.316257.118

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                    Wan, Yao, and Hopper, Anita K. Tue .  
"From powerhouse to processing plant: conserved roles of mitochondrial outer membrane proteins in tRNA splicing".  United States.  https://doi.org/10.1101/gad.316257.118.  https://www.osti.gov/servlets/purl/1560569.

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@article{osti_1560569,

  title        = {From powerhouse to processing plant: conserved roles of mitochondrial outer membrane proteins in tRNA splicing},

  author       = {Wan, Yao and Hopper, Anita K.},

  abstractNote = {The mitochondrial cytoplasmic surface serves as a processing site for numerous RNAs from budding yeast to metazoans. We report that budding yeast mitochondrial outer membrane (MOM) proteins that are subunits of the translocase of the outer mitochondrial membrane (Tom70 and Tom 22) and sorting and assembly machinery (Sam37) are required for efficient pretransfer RNA (pre-tRNA) splicing. Defective pre-tRNA splicing in MOM mutants is due not to loss of respiratory metabolism but instead inefficient targeting/tethering of tRNA splicing endonuclease (SEN) subunits to mitochondria. Schizosaccharomyces pombe SEN subunits also localize to mitochondria, and Tom70 is required for this localization and pre-tRNA splicing. Thus, the role of MOM protein in targeting/tethering SEN subunits to mitochondria has been conserved for >500 million years.},

  doi          = {10.1101/gad.316257.118},

  journal      = {Genes & Development},

  number       = 19-20,

  volume       = 32,

  place        = {United States},

  year         = {Tue Sep 18 00:00:00 EDT 2018},

  month        = {Tue Sep 18 00:00:00 EDT 2018}

}

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https://doi.org/10.1101/gad.316257.118

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Cited by: 15 works

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Figures / Tables:

Figure 1: Respiratory metabolism is not required for efficient pretRNA splicing in S. cerevisiae. (A) Northern analysis of tRNA^Ile_UAU(probe JW0041) in cells lacking mitochondrial DNA. Wild-type cells lacking mitochondrial DNA via treatment with ethidium bromide [wild-type (EtBr)] and mip1Δ cells. (P) Primary tRNA transcript; (I) end-processed intron-containing tRNA; (5S)more »

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Similar Records

Title: From powerhouse to processing plant: conserved roles of mitochondrial outer membrane proteins in tRNA splicing

Abstract

Citation Formats

Figures / Tables:

The tRNA Splicing Endonuclease Complex Cleaves the Mitochondria-localized CBP1 mRNA journal, May 2015

Balanced production of ribosomal proteins journal, October 2007

Induction of the cytoplasmic ‘petite’ mutation by chemical and physical agents in Saccharomyces cerevisiae journal, January 1992

tRNA transfers to the limelight journal, January 2003

The Activity-Dependent Regulation of Protein Kinase Stability by the Localization to P-Bodies journal, May 2016

The structural biochemistry of Zucchini implicates it as a nuclease in piRNA biogenesis journal, October 2012

A cyclic form of N6-threonylcarbamoyladenosine as a widely distributed tRNA hypermodification journal, December 2012

A common lipid links Mfn-mediated mitochondrial fusion and SNARE-regulated exocytosis journal, October 2006

Identification and Functional Analysis of the Pre-piRNA 3′ Trimmer in Silkworms journal, February 2016

Identification of a Human Endonuclease Complex Reveals a Link between tRNA Splicing and Pre-mRNA 3′ End Formation journal, April 2004

Proofreading and Aminoacylation of tRNAs Before Export from the Nucleus journal, December 1998

Processing of intervening sequences: a new yeast mutant which fails to excise intervening sequences from precursor tRNAs journal, March 1980

Order and intracellular location of the events involved in the maturation of a spliced tRNA journal, March 1980

Nuclear processing and export of microRNAs in Arabidopsis journal, February 2005

Minimal, encapsulated proteomic-sample processing applied to copy-number estimation in eukaryotic cells journal, February 2014

tRNA Nuclear Export in Saccharomyces cerevisiae : In Situ Hybridization Analysis journal, November 1998

Global analysis of protein expression in yeast journal, October 2003

Cleavage of pre-tRNAs by the splicing endonuclease requires a composite active site journal, May 2006

Genome-wide screen uncovers novel pathways for tRNA processing and nuclear–cytoplasmic dynamics journal, December 2015

Global analysis of protein localization in budding yeast journal, October 2003

Sam37 is crucial for formation of the mitochondrial TOM–SAM supercomplex, thereby promoting β-barrel biogenesis journal, September 2015

Mechanisms of Protein Sorting in Mitochondria journal, October 2012

GtRNAdb: a database of transfer RNA genes detected in genomic sequence journal, January 2009

ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe journal, June 2006

Queuosine Formation in Eukaryotic tRNA Occurs via a Mitochondria-localized Heteromeric Transglycosylase journal, May 2009

The indispensable genome journal, November 2015

Altered nuclear tRNA metabolism in La-deleted Schizosaccharomyces pombe is accompanied by a nutritional stress response involving Atf1p and Pcr1p that is suppressible by Xpo-t/Los1p journal, February 2012

Comparative Functional Genomics of the Fission Yeasts journal, April 2011

Plant pre-tRNA splicing enzymes are targeted to multiple cellular compartments journal, November 2007

MITOPLD Is a Mitochondrial Protein Essential for Nuage Formation and piRNA Biogenesis in the Mouse Germline journal, March 2011

piRNA-Associated Germline Nuage Formation and Spermatogenesis Require MitoPLD Profusogenic Mitochondrial-Surface Lipid Signaling journal, March 2011

Possibility of Cytoplasmic pre-tRNA Splicing: the Yeast tRNA Splicing Endonuclease Mainly Localizes on the Mitochondria journal, August 2003

tRNA dynamics between the nucleus, cytoplasm and mitochondrial surface: Location, location, location journal, April 2018

The RNase PARN-1 Trims piRNA 3′ Ends to Promote Transcriptome Surveillance in C. elegans journal, February 2016

A nuclear mutant of Saccharomyces cerevisiae deficient in mitochondrial DNA replication and polymerase activity. journal, July 1986

Mutations in the anticodon stem of tRNA cause accumulation and Met22-dependent decay of pre-tRNA in yeast journal, October 2019

tRNA Processing and Subcellular Trafficking Proteins Multitask in Pathways for Other RNAs journal, February 2019

PARP1 Enhances Influenza A Virus Propagation by Facilitating Degradation of Host Type I Interferon Receptor journal, January 2020

tRNA Processing and Subcellular Trafficking Proteins Multitask in Pathways for Other RNAs journal, February 2019

The tRNA Splicing Endonuclease Complex Cleaves the Mitochondria-localized CBP1 mRNA
journal, May 2015

Balanced production of ribosomal proteins
journal, October 2007

Induction of the cytoplasmic ‘petite’ mutation by chemical and physical agents in Saccharomyces cerevisiae
journal, January 1992

tRNA transfers to the limelight
journal, January 2003

The Activity-Dependent Regulation of Protein Kinase Stability by the Localization to P-Bodies
journal, May 2016

The structural biochemistry of Zucchini implicates it as a nuclease in piRNA biogenesis
journal, October 2012

A cyclic form of N6-threonylcarbamoyladenosine as a widely distributed tRNA hypermodification
journal, December 2012

A common lipid links Mfn-mediated mitochondrial fusion and SNARE-regulated exocytosis
journal, October 2006

Identification and Functional Analysis of the Pre-piRNA 3′ Trimmer in Silkworms
journal, February 2016

Identification of a Human Endonuclease Complex Reveals a Link between tRNA Splicing and Pre-mRNA 3′ End Formation
journal, April 2004

Proofreading and Aminoacylation of tRNAs Before Export from the Nucleus
journal, December 1998

Processing of intervening sequences: a new yeast mutant which fails to excise intervening sequences from precursor tRNAs
journal, March 1980

Order and intracellular location of the events involved in the maturation of a spliced tRNA
journal, March 1980

Nuclear processing and export of microRNAs in Arabidopsis
journal, February 2005

Minimal, encapsulated proteomic-sample processing applied to copy-number estimation in eukaryotic cells
journal, February 2014

tRNA Nuclear Export in Saccharomyces cerevisiae : In Situ Hybridization Analysis
journal, November 1998

Global analysis of protein expression in yeast
journal, October 2003

Cleavage of pre-tRNAs by the splicing endonuclease requires a composite active site
journal, May 2006

Genome-wide screen uncovers novel pathways for tRNA processing and nuclear–cytoplasmic dynamics
journal, December 2015

Global analysis of protein localization in budding yeast
journal, October 2003

Sam37 is crucial for formation of the mitochondrial TOM–SAM supercomplex, thereby promoting β-barrel biogenesis
journal, September 2015

Mechanisms of Protein Sorting in Mitochondria
journal, October 2012

GtRNAdb: a database of transfer RNA genes detected in genomic sequence
journal, January 2009

ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe
journal, June 2006

Queuosine Formation in Eukaryotic tRNA Occurs via a Mitochondria-localized Heteromeric Transglycosylase
journal, May 2009

The indispensable genome
journal, November 2015

Altered nuclear tRNA metabolism in La-deleted Schizosaccharomyces pombe is accompanied by a nutritional stress response involving Atf1p and Pcr1p that is suppressible by Xpo-t/Los1p
journal, February 2012

Comparative Functional Genomics of the Fission Yeasts
journal, April 2011

Plant pre-tRNA splicing enzymes are targeted to multiple cellular compartments
journal, November 2007

MITOPLD Is a Mitochondrial Protein Essential for Nuage Formation and piRNA Biogenesis in the Mouse Germline
journal, March 2011

piRNA-Associated Germline Nuage Formation and Spermatogenesis Require MitoPLD Profusogenic Mitochondrial-Surface Lipid Signaling
journal, March 2011

Possibility of Cytoplasmic pre-tRNA Splicing: the Yeast tRNA Splicing Endonuclease Mainly Localizes on the Mitochondria
journal, August 2003

tRNA dynamics between the nucleus, cytoplasm and mitochondrial surface: Location, location, location
journal, April 2018

The RNase PARN-1 Trims piRNA 3′ Ends to Promote Transcriptome Surveillance in C. elegans
journal, February 2016

A nuclear mutant of Saccharomyces cerevisiae deficient in mitochondrial DNA replication and polymerase activity.
journal, July 1986

Mutations in the anticodon stem of tRNA cause accumulation and Met22-dependent decay of pre-tRNA in yeast
journal, October 2019

tRNA Processing and Subcellular Trafficking Proteins Multitask in Pathways for Other RNAs
journal, February 2019

PARP1 Enhances Influenza A Virus Propagation by Facilitating Degradation of Host Type I Interferon Receptor
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