Messenger RNA stability in mitochondria: different means to an end

Gagliardi, Dominique; Stępień, Piotr P.; Temperley, Richard; Lightowlers, Robert N.; Chrzanowska-Lightowlers, Zofia M.A.

doi:10.1016/j.tig.2004.04.006

Cited by 122 publications

(124 citation statements)

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“…To simultaneously estimate the expression of mtDNA and nuclear genes, in the present study we revisited published RNA-seq data 8,9 that included a large number of polyadenylated [10][11][12][13] mitochondrial transcripts. We quantified between-individual variation in the expression of mtDNA genes in HapMap samples of European (CEU) and African (YRI) ancestry to evaluate this variation at the population level.…”

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Population-level expression variability of mitochondrial DNA-encoded genes in humans

et al. 2014

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Human mitochondria contain multiple copies of a circular genome made up of double-stranded DNA (mtDNA) that encodes proteins involved in cellular respiration. Transcript abundance of mtDNA-encoded genes varies between human individuals, yet the level of variation in the general population has not been systematically assessed. In the present study, we revisited large-scale RNA sequencing data generated from lymphoblastoid cell lines of HapMap samples of European and African ancestry to estimate transcript abundance and quantify expression variation for mtDNA-encoded genes. In both populations, we detected up to over 100-fold difference in mtDNA gene expression between individuals. The marked variation was not due to differences in mtDNA copy number between individuals, but was shaped by the transcription of hundreds of nuclear genes. Many of these nuclear genes were co-expressed with one another, resulting in a module-enriched co-expression network. Significant correlations in expression between genes of the mtDNA and nuclear genomes were used to identify factors involved with the regulation of mitochondrial functions. In conclusion, we determined the baseline amount of variability in mtDNA gene expression in general human populations and cataloged a complete set of nuclear genes whose expression levels are correlated with those of mtDNA-encoded genes. Our findings will enable the integration of information from both mtDNA and nuclear genetic systems, and facilitate the discovery of novel regulatory pathways involving mitochondrial functions.

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Population-level expression variability of mitochondrial DNA-encoded genes in humans

et al. 2014

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“…The enzymes controlling RNA turnover in cells and organelles show great evolutionary divergence and are only partially conserved between mitochondria of different organisms (Gagliardi et al, 2004). The enzymatic activity responsible for turnover is, however, on the basic level, similar in all the systems discovered so far-it is that of a 3Ј-to-5Ј processive exoribonuclease, either hydrolytic or phosphorolytic.…”

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confidence: 99%

“…The mitochondrial degradosome is the main exoribonuclease in yeast mitochondria, which, unlike bacteria and animal or plant mitochondria, lack the phosphorolytic polynucleotide phosphorylase activity. Like the bacterial degradosome it contains an RNase and an RNA helicase; the subunit composition is, however, markedly different (Gagliardi et al, 2004). The yeast mitochondrial degradosome is composed of only two protein subunits-an RNR (RNase II-like) superfamily exoribonuclease encoded by the DSS1/MSU1 (YMR287C) gene (Dmochowska et al, 1995) and an NTP-dependent RNA helicase related to the DExH superfamily, encoded by the SUV3 (YPL029W) gene (Stepien et al, 1992).…”

Section: Introductionmentioning

confidence: 99%

“…The single RNA polymerase (RNAP) of Saccharomyces cerevisiae mitochondria is composed of only two nuclear-encoded protein subunits-the core enzyme encoded by the RPO41 gene and a transcription initiation factor encoded by the MTF1 gene (Masters et al, 1987;Jang and Jaehning, 1991). The RNAP holoenzyme recognizes a simple nonanucleotide promoter sequence (Osinga et al, 1982;Mangus et al, 1994) and initiates synthesis of at least 13 primary multicistronic transcripts that undergo extensive processing to form mature RNAs (Christianson and Rabinowitz, 1983;Tzagoloff and Myers, 1986;Foury et al, 1998;Gagliardi et al, 2004;Schafer, 2005). Such organization leaves little room for regulation at the transcription initiation level and makes posttranscriptional processes, including RNA degradation, key control points for mitochondrial gene expression.…”

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confidence: 99%

“…The RNAP holoenzyme recognizes a simple nonanucleotide promoter sequence (Osinga et al, 1982;Mangus et al, 1994) and initiates synthesis of at least 13 primary multicistronic transcripts that undergo extensive processing to form mature RNAs (Christianson and Rabinowitz, 1983;Tzagoloff and Myers, 1986;Foury et al, 1998;Gagliardi et al, 2004;Schafer, 2005). Such organization leaves little room for regulation at the transcription initiation level and makes posttranscriptional processes, including RNA degradation, key control points for mitochondrial gene expression.The enzymes controlling RNA turnover in cells and organelles show great evolutionary divergence and are only partially conserved between mitochondria of different organisms (Gagliardi et al, 2004). The enzymatic activity responsible for turnover is, however, on the basic level, similar in all the systems discovered so far-it is that of a 3Ј-to-5Ј processive exoribonuclease, either hydrolytic or phosphorolytic.…”

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Balance between Transcription and RNA Degradation Is Vital forSaccharomyces cerevisiaeMitochondria: Reduced Transcription Rescues the Phenotype of Deficient RNA Degradation

Rogowska

Puchta

Czarnecka

et al. 2006

MBoC

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The Saccharomyces cerevisiae SUV3 gene encodes the helicase component of the mitochondrial degradosome (mtEXO), the principal 3 -to-5 exoribonuclease of yeast mitochondria responsible for RNA turnover and surveillance. Inactivation of SUV3 (suv3⌬) causes multiple defects related to overaccumulation of aberrant transcripts and precursors, leading to a disruption of mitochondrial gene expression and loss of respiratory function. We isolated spontaneous suppressors that partially restore mitochondrial function in suv3⌬ strains devoid of mitochondrial introns and found that they correspond to partial loss-of-function mutations in genes encoding the two subunits of the mitochondrial RNA polymerase (Rpo41p and Mtf1p) that severely reduce the transcription rate in mitochondria. These results show that reducing the transcription rate rescues defects in RNA turnover and demonstrates directly the vital importance of maintaining the balance between RNA synthesis and degradation. INTRODUCTIONThe degradation of RNA is an essential element in the expression of genetic information. It is required to control RNA abundance and thus gene expression and to eliminate aberrant or defective molecules that inevitably form during RNA synthesis and maturation (RNA surveillance) (Vasudevan and Peltz, 2003). The posttranscriptional mechanisms affecting mitochondrial gene expression, including RNA turnover, are of particular importance because transcriptional control is relatively simple and rudimentary. The single RNA polymerase (RNAP) of Saccharomyces cerevisiae mitochondria is composed of only two nuclear-encoded protein subunits-the core enzyme encoded by the RPO41 gene and a transcription initiation factor encoded by the MTF1 gene (Masters et al., 1987;Jang and Jaehning, 1991). The RNAP holoenzyme recognizes a simple nonanucleotide promoter sequence (Osinga et al., 1982;Mangus et al., 1994) and initiates synthesis of at least 13 primary multicistronic transcripts that undergo extensive processing to form mature RNAs (Christianson and Rabinowitz, 1983;Tzagoloff and Myers, 1986;Foury et al., 1998;Gagliardi et al., 2004;Schafer, 2005). Such organization leaves little room for regulation at the transcription initiation level and makes posttranscriptional processes, including RNA degradation, key control points for mitochondrial gene expression.The enzymes controlling RNA turnover in cells and organelles show great evolutionary divergence and are only partially conserved between mitochondria of different organisms (Gagliardi et al., 2004). The enzymatic activity responsible for turnover is, however, on the basic level, similar in all the systems discovered so far-it is that of a 3Ј-to-5Ј processive exoribonuclease, either hydrolytic or phosphorolytic. In most cases, the exoribonuclease activity is contained in a larger multiprotein complex that, in addition to exoribonucleases, also contains RNA helicases, and in certain cases, endonucleases. A model example of such a complex is the eubacterial degradosome (Carpousis, 2002).The first mitoc...

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Creative partnerships in diabetes nursing: Promoting learning through collaborative practice – a preliminary evaluation

Sewell

Costa

Dempsey

et al. 2006

European Diabetes Nursing

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This paper describes the collaborative partnership between two geographically diverse NHS trusts in the UK serving patient populations with very different demographic profiles. A programme of structured exchange has been developed allowing diabetes specialist nurses (DSNs) to visit the partner trust to share and compare clinical practice. The model allows the individuals involved to critically reflect on their own and others' practice and has facilitated networking between the DSNs and service developments within the trusts.Eur Diabetes Nursing 2006; 3(2): 98-101.

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Messenger RNA stability in mitochondria: different means to an end

Cited by 122 publications

References 59 publications

Population-level expression variability of mitochondrial DNA-encoded genes in humans

Population-level expression variability of mitochondrial DNA-encoded genes in humans

Balance between Transcription and RNA Degradation Is Vital forSaccharomyces cerevisiaeMitochondria: Reduced Transcription Rescues the Phenotype of Deficient RNA Degradation

Creative partnerships in diabetes nursing: Promoting learning through collaborative practice – a preliminary evaluation

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