Transcriptome-wide co-expression analysis identifies LRRC2 as a novel mediator of mitochondrial and cardiac function.

Mitochondrial dysfunction contributes to myriad monogenic and complex pathologies. To understand the underlying mechanisms, it is essential to define the full complement of proteins that modulate mitochondrial function. To identify such proteins, we performed a meta-analysis of publicly available ge...

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Main Authors: Chris McDermott-Roe, Marion Leleu, Glenn C Rowe, Oleg Palygin, John D Bukowy, Judy Kuo, Monika Rech, Steffie Hermans-Beijnsberger, Sebastian Schaefer, Eleonora Adami, Esther E Creemers, Matthias Heinig, Blanche Schroen, Zoltan Arany, Enrico Petretto, Aron M Geurts
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0170458&type=printable
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author Chris McDermott-Roe
Marion Leleu
Glenn C Rowe
Oleg Palygin
John D Bukowy
Judy Kuo
Monika Rech
Steffie Hermans-Beijnsberger
Sebastian Schaefer
Eleonora Adami
Esther E Creemers
Matthias Heinig
Blanche Schroen
Zoltan Arany
Enrico Petretto
Aron M Geurts
author_facet Chris McDermott-Roe
Marion Leleu
Glenn C Rowe
Oleg Palygin
John D Bukowy
Judy Kuo
Monika Rech
Steffie Hermans-Beijnsberger
Sebastian Schaefer
Eleonora Adami
Esther E Creemers
Matthias Heinig
Blanche Schroen
Zoltan Arany
Enrico Petretto
Aron M Geurts
author_sort Chris McDermott-Roe
collection DOAJ
description Mitochondrial dysfunction contributes to myriad monogenic and complex pathologies. To understand the underlying mechanisms, it is essential to define the full complement of proteins that modulate mitochondrial function. To identify such proteins, we performed a meta-analysis of publicly available gene expression data. Gene co-expression analysis of a large and heterogeneous compendium of microarray data nominated a sub-population of transcripts that whilst highly correlated with known mitochondrial protein-encoding transcripts (MPETs), are not themselves recognized as generating proteins either localized to the mitochondrion or pertinent to functions therein. To focus the analysis on a medically-important condition with a strong yet incompletely understood mitochondrial component, candidates were cross-referenced with an MPET-enriched module independently generated via genome-wide co-expression network analysis of a human heart failure gene expression dataset. The strongest uncharacterized candidate in the analysis was Leucine Rich Repeat Containing 2 (LRRC2). LRRC2 was found to be localized to the mitochondria in human cells and transcriptionally-regulated by the mitochondrial master regulator Pgc-1α. We report that Lrrc2 transcript abundance correlates with that of β-MHC, a canonical marker of cardiac hypertrophy in humans and experimentally demonstrated an elevation in Lrrc2 transcript in in vitro and in vivo rodent models of cardiac hypertrophy as well as in patients with dilated cardiomyopathy. RNAi-mediated Lrrc2 knockdown in a rat-derived cardiomyocyte cell line resulted in enhanced expression of canonical hypertrophic biomarkers as well as increased mitochondrial mass in the context of increased Pgc-1α expression. In conclusion, our meta-analysis represents a simple yet powerful springboard for the nomination of putative mitochondrially-pertinent proteins relevant to cardiac function and enabled the identification of LRRC2 as a novel mitochondrially-relevant protein and regulator of the hypertrophic response.
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spelling doaj-art-32ee4dc91d374bd4874942d7b45e85532025-08-20T03:26:10ZengPublic Library of Science (PLoS)PLoS ONE1932-62032017-01-01122e017045810.1371/journal.pone.0170458Transcriptome-wide co-expression analysis identifies LRRC2 as a novel mediator of mitochondrial and cardiac function.Chris McDermott-RoeMarion LeleuGlenn C RoweOleg PalyginJohn D BukowyJudy KuoMonika RechSteffie Hermans-BeijnsbergerSebastian SchaeferEleonora AdamiEsther E CreemersMatthias HeinigBlanche SchroenZoltan AranyEnrico PetrettoAron M GeurtsMitochondrial dysfunction contributes to myriad monogenic and complex pathologies. To understand the underlying mechanisms, it is essential to define the full complement of proteins that modulate mitochondrial function. To identify such proteins, we performed a meta-analysis of publicly available gene expression data. Gene co-expression analysis of a large and heterogeneous compendium of microarray data nominated a sub-population of transcripts that whilst highly correlated with known mitochondrial protein-encoding transcripts (MPETs), are not themselves recognized as generating proteins either localized to the mitochondrion or pertinent to functions therein. To focus the analysis on a medically-important condition with a strong yet incompletely understood mitochondrial component, candidates were cross-referenced with an MPET-enriched module independently generated via genome-wide co-expression network analysis of a human heart failure gene expression dataset. The strongest uncharacterized candidate in the analysis was Leucine Rich Repeat Containing 2 (LRRC2). LRRC2 was found to be localized to the mitochondria in human cells and transcriptionally-regulated by the mitochondrial master regulator Pgc-1α. We report that Lrrc2 transcript abundance correlates with that of β-MHC, a canonical marker of cardiac hypertrophy in humans and experimentally demonstrated an elevation in Lrrc2 transcript in in vitro and in vivo rodent models of cardiac hypertrophy as well as in patients with dilated cardiomyopathy. RNAi-mediated Lrrc2 knockdown in a rat-derived cardiomyocyte cell line resulted in enhanced expression of canonical hypertrophic biomarkers as well as increased mitochondrial mass in the context of increased Pgc-1α expression. In conclusion, our meta-analysis represents a simple yet powerful springboard for the nomination of putative mitochondrially-pertinent proteins relevant to cardiac function and enabled the identification of LRRC2 as a novel mitochondrially-relevant protein and regulator of the hypertrophic response.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0170458&type=printable
spellingShingle Chris McDermott-Roe
Marion Leleu
Glenn C Rowe
Oleg Palygin
John D Bukowy
Judy Kuo
Monika Rech
Steffie Hermans-Beijnsberger
Sebastian Schaefer
Eleonora Adami
Esther E Creemers
Matthias Heinig
Blanche Schroen
Zoltan Arany
Enrico Petretto
Aron M Geurts
Transcriptome-wide co-expression analysis identifies LRRC2 as a novel mediator of mitochondrial and cardiac function.
PLoS ONE
title Transcriptome-wide co-expression analysis identifies LRRC2 as a novel mediator of mitochondrial and cardiac function.
title_full Transcriptome-wide co-expression analysis identifies LRRC2 as a novel mediator of mitochondrial and cardiac function.
title_fullStr Transcriptome-wide co-expression analysis identifies LRRC2 as a novel mediator of mitochondrial and cardiac function.
title_full_unstemmed Transcriptome-wide co-expression analysis identifies LRRC2 as a novel mediator of mitochondrial and cardiac function.
title_short Transcriptome-wide co-expression analysis identifies LRRC2 as a novel mediator of mitochondrial and cardiac function.
title_sort transcriptome wide co expression analysis identifies lrrc2 as a novel mediator of mitochondrial and cardiac function
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0170458&type=printable
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