The Mitochondrial Translation System

Buetow, D.E.; Wood, William M.

doi:10.1007/978-1-4615-7942-7_1

Cited by 45 publications

(22 citation statements)

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“…Conversely, in bacteria and chloroplasts, polyadenylation destabilizes mRNAs and their endonucleolytic cleavage products (13,23,49). Although mitochondrial mRNAs are polyadenylated in many systems (6), little is known about the role of mitochondrial polyadenylation and its possible effect on RNA turnover. The only two studies, to our knowledge, that directly address this subject are the recent reports by Gagliardi and Leaver (18) and Lupold et al (31), which provide evidence that polyadenylation destabilizes mitochondrial mRNAs in plants.…”

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UTP-Dependent and -Independent Pathways of mRNA Turnover in Trypanosoma brucei Mitochondria

Militello

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2000

Molecular and Cellular Biology

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Although primary transcripts are polycistronic in the mitochondria of Trypanosoma brucei, steady-state levels of mature, monocistronic RNAs change throughout the parasitic life cycle. This indicates that steadystate RNA abundance is controlled by posttranscriptional mechanisms involving differential RNA stability. In this study, in organello pulse-chase labeling experiments were used to analyze the stability of different T. brucei mitochondrial RNA populations. In this system, total RNA and rRNA are stable for many hours. In contrast, mRNAs can be degraded by two biochemically distinct turnover pathways. The first pathway results in the rapid degradation of mRNA (half-life [t 1/2 ] of 11 to 18 min) and is dependent upon the presence of an mRNA poly(A) tail. Remarkably, this pathway also requires the addition of UTP and therefore is termed UTP dependent. The second pathway results in slow turnover of mitochondrial mRNA (t 1/2 of ϳ3 h) and is not dependent upon the presence of an mRNA poly(A) tail or the addition of exogenous UTP. In summary, these results demonstrate the presence of a novel, UTP-dependent degradation pathway for T. brucei mitochondrial mRNAs and reveal an unprecedented role for both UTP and mRNA polyadenylation in T. brucei mitochondrial gene expression.The regulation of RNA stability plays a pivotal role in controlling gene expression in many organisms. Although RNA stability in bacteria (12), chloroplasts (23), and the eukaryotic cytoplasm (43, 47) has been extensively studied, little is known about turnover mechanisms of mitochondrial mRNAs. A common theme in all systems examined to date is the regulation of mRNA stability through polyadenylation (32). In the eukaryotic cytoplasm, polyadenylation increases the stability of mRNAs in a mechanism dependent upon the poly(A)-binding protein I (25, 48). Conversely, in bacteria and chloroplasts, polyadenylation destabilizes mRNAs and their endonucleolytic cleavage products (13,23,49). Although mitochondrial mRNAs are polyadenylated in many systems (6), little is known about the role of mitochondrial polyadenylation and its possible effect on RNA turnover. The only two studies, to our knowledge, that directly address this subject are the recent reports by Gagliardi and Leaver (18) and Lupold et al. (31), which provide evidence that polyadenylation destabilizes mitochondrial mRNAs in plants.Both mitochondrial and nuclear gene expression in the protozoan parasite Trypanosoma brucei are primarily regulated at the posttranscriptional level (42, 55). Reverse transcriptase PCR and Northern blot experiments have demonstrated that primary transcripts in the mitochondria are polycistronic and contain at least two different open reading frames (17,28,35,44,53). The generation of mature mitochondrial RNAs requires several posttranscriptional processing events, and the order of these events is variable. Polycistronic RNAs require cleavage to release individual, monocistronic RNAs with correct 5Ј and 3Ј ends. mRNAs are also modified by the addition of either a sh...

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UTP-Dependent and -Independent Pathways of mRNA Turnover in Trypanosoma brucei Mitochondria

Militello

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2000

Molecular and Cellular Biology

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“…Any potential significance to the different roles the PAT may play regarding mRNA degradation in the cytoplasm vs. organelles is unclear and, to date, animal mitochondria have not been studied in depth regarding RNA degradation. Although mRNAs in animal mitochondria are known to be polyadenylated (Beutow and Wood, 1978), to our knowledge there are no reports directly assessing the effect of polyadenylation on mitochondrial mRNA stability. We Polyadenylation of messenger RNA is known to be an important mechanism for regulating mRNA stability in a variety of systems, including bacteria, chloroplasts and plant mitochondria.…”

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Mitochondrial mRNA stability and polyadenylation during anoxia-induced quiescence in the brine shrimpArtemia franciscana

Eads

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2003

Journal of Experimental Biology

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In response to physiological cues, a common strategy for regulating gene expression is the modulation of RNA stability. Polyadenylation at the 3′-end of mRNAs is a major structural feature that appears to play an important role in message stability in many cases (Tharun and Parker, 1997). During development, regulated changes in length of the poly(A) + tail (PAT) of specific messages are correlated with their stability and translation (Richter, 1999). Deadenylation and 5′ decapping are rate-limiting steps in yeast mRNA decay (Muhlrad et al., 1995), while in mammals the 3′ untranslated region (UTR) and RNA binding proteins also have major effects on degradation rates (Ross, 1995). Mechanisms of RNA decay have been elucidated in bacteria (Xu and Cohen, 1995;Sarkar, 1997;Blum et al., 1999), chloroplasts (Hayes et al., 1999;Schuster et al., 1999), plant mitochondria (Gagliardi and Leaver, 1999;Kuhn et al., 2001;Lupold et al., 1999) and the eukaryotic cytoplasm (Mitchell and Tollervey, 2000). Longer PATs are generally associated with longer-lived mRNA species, and in some cases play a direct role in translational regulation as well (Rajagopalan and Malter, 1997;Sachs, 2000). In contrast to the eukaryotic cytoplasm, the degradation rate of poly(A) + mRNA is increased compared to nonadenylated mRNA in chloroplasts, plant mitochondria, and bacteria. Polyadenylated mRNAs from trypanosomes were also recently shown to degrade more rapidly in the presence of elevated UTP concentrations (Militello and Read, 2000). The unusual mitochondrial genomes and transcriptional mechanisms of trypanosomes, however, make generalizations problematic. Any potential significance to the different roles the PAT may play regarding mRNA degradation in the cytoplasm vs. organelles is unclear and, to date, animal mitochondria have not been studied in depth regarding RNA degradation. Although mRNAs in animal mitochondria are known to be polyadenylated (Beutow and Wood, 1978), to our knowledge there are no reports directly assessing the effect of polyadenylation on mitochondrial mRNA stability. We Polyadenylation of messenger RNA is known to be an important mechanism for regulating mRNA stability in a variety of systems, including bacteria, chloroplasts and plant mitochondria. By comparison, little is known about the role played by polyadenylation in animal mitochondrial gene expression. We have used embryos of the brine shrimp Artemia franciscana to test hypotheses regarding message stability and polyadenylation under conditions simulating anoxia-induced quiescence. In response to anoxia, these embryos undergo a profound and acute metabolic downregulation, characterized by a steep drop in intracellular pH (pHi) and ATP levels. Using dot blots of total mitochondrial RNA, we show that during in organello incubations both O2 deprivation and acidic pH (pH·6.4) elicit increases in half-lives of selected mitochondrial transcripts on the order of five-to tenfold or more, relative to normoxic controls at pH·7.8. Polyadenylation of these transcripts was me...

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“…The widely held endosymbiont hypothesis of evolution of organelles implies that their translation systems would be prokaryotic in nature. The translation system ofmitochondria does indeed show some prokaryotic features; however, it also shows some eukaryotic and some unique features (1,2). The mitochondrial genetic system itself has features distinct from those of its prokaryotic and eukaryotic counterparts.…”

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“…The mitochondrial genome specifies only a limited number of polypeptides, of which several have been identified (1,8). In no case, however, has the identity of all the apparent mitochondrial translation products been determined.…”

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“…It is known that mitochondria use a unique complement of tRNAs (6,34,35), that mitochondrial mRNAs have long 5' leader sequences (36), and that the mitochondrial ribosome and tRNAs may be involved in correcting commonly occurring frame-shift mutations, at least in yeast (37). Also, bacterial elongation factors substitute for mitochondrial factors in crude translation systems (1). It is not known, however, whether or not bacterial factors allow the correct translation offull-sized products from mitochondrial mRNAs.…”

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