International Review of Cytology: 222 (International Review of Cell and Molecular Biology)
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Hormone Effects on Transcription in Isolated Mitochondria The wealth of data amassed on the action of glucocorticoids and thyroid hormones on mitochondrial RNA and protein metabolism referred to in Section IV. A led to the conclusion that the hormones regulate transcription and perhaps also the stability of the transcripts. Furthermore, the hormones act indirectly, by way of induction of nuclear genes encoding mitochondrial transcription, and other regulatory factors.
Kwang W. Jeon
The development of an in organello mitochondrial system capable of maintaining DNA transcription for several hours was instrumental in evaluating the possible direct action of steroid and thyroid hormones on this process Enriquez et al. The authors demonstrated that the processing of the RNA precursors and the stability of the mature rRNAs, but not transcription itself, are severely impaired after short periods of incubation of mitochondria, indicating that these processes are strongly dependent on the mitochondrial interaction with the nucleocytoplasmic compartment.
However, the events that lead to the synthesis, processing, and turnover of the mt-mRNAs do not require the continuous supply of nucleocytoplasmic factors that are accumulated in excess by mitochondria. Provided that ADP plus oxidizable substrates are added to the system, allowing endogenous ATP synthesis, transcription is maintained in the in organello system in the absence of nuclear gene transcription, rendering the system autonomous for several hours.
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This in organello system has been exploited by Enriquez et al. Enriquez et al. The detection of nucleotide sequences with strong similarity to hormone responsive elements in the genome of eubacteria and archaebacteria and their possible relation to similar sequences present in the mitochondrial genome. A B FIG. The dimethyl sulfate footprinting patterns of mitochondria derived from euthyroid and hypothyroid rats show conspicuous differences at the transcription initiation sites but not at the termination factor mTERF -binding region.
These differences can be abolished by the addition of T3 to the mitochondria, which apparently acts on the initiation of the transcriptional process and this effect is very probably mediated by the thyroid receptor. Casas et al.
The addition of T3 to the system induced a strong rise in the precursor transcript levels within 5 min. Similar effects could be observed in the absence of p43 FIG. A—F In organello transcription experiments were performed as described by Ostronoff et al. Transcription experiments were stopped by cooling on ice. Mitochondria were collected by centrifugation and mitochondrial RNA was extracted twice at room temperature.
A—D After in organello transcription experiments, precursor transcript were detected by Northern blotting with the indicated mitochondrial probes. A and B Precursor transcript levels recorded after 60 min of in organello transcription.
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E Northern blot experiments were performed with agarose stab gels containing deionized CH3HgOH after in organello transcription studies. Mature transcripts are detected by hybridization with the indicated mitochondrial probes after 60 min of in organello transcription. Although no 12 S or 16 S rRNA precursor transcript could be detected, mature ribosomal RNAs were found in increased amounts after addition of p43 to the in organello system. The authors suggest that the extent and rapidity of the increase in precursor transcript levels make the possibility of effects on RNA stability unlikely.
As already mentioned, the precursor transcripts induced by p43 do not contain the genes for the 12 S and 16 S rRNAs. The presence of a putative TRE in the 16 S rRNA gene suggests that initiation of transcription in the presence of p43 could start at this site, accounting for the lack of the ribosomal transcripts. In the in organello system, the addition of mt-TFA also led to an increase in precursor transcript levels and, in the presence of T3, to an increase in the levels of mature transcripts.
Preliminary evidence has been presented that p43 and mt-TFA use different response elements of the D-loop. The direct action of T3 on transcription in the in organello mitochondrial system raises the question as to the molecular mechanism of the hormonal action.
Nuclear genes, each endowed with its own regulatory region, most having exons and introns, are organized in nucleosomal structures composed of DNA and the well-characterized histone octamer Pruss et al. Mitochondrial DNA is a tightly packed genome forming complexes with not well-characterized proteins Fisher et al. The nucleus is packed with several transcription factors, coactivators, histone-modifying enzymes, and other coregulators, whereas only a few transcription factors have to now been demonstrated in mitochondria.
The nuclear genome is monocistronic, each individual gene transcribed and processed separately, whereas the mitochondrial genome is polycistronic, transcription starts at two promoters, each in one of the two DNA strands, the whole strands are read through, and the RNA transcripts are subsequently cleaved to produce the 38 RNA species. The mt genome and the RNA transcription process are obviously of a prokaryotic type and this should be taken into consideration when considering the possible role of the mitochondrial receptors on the mitochondrial transcription process.
The hormone receptors could act as ligand-activated positive regulators, but also as repressors, dissociating from the D-loop initiation sites in the presence of the hormonal ligand or from other HREs interspersed in the mitochondrial genome, raising the possibility of control of transcript elongation and termination. Increase in gene dosage, i. It should be mentioned, however, that in the mitochondrial compartment, in contrast to the cytosol, mRNAs are present in molar excess and to increase the synthesis of proteins encoded by mitochondrial DNA the availability of ribosomes is more important than of mRNAs, a situation that is observed in cardiac growth Wiesner et al.
One possibility for the elevated resting metabolic rates observed upon hormonal induction could be the increased expression of uncoupling proteins. However, Weber et al. The biosynthesis of mitochondria and the de novo formation of complexes of the respiratory chain necessitate coordination of nuclear and mitochondrial gene transcription and translation Nagley, In steady-state conditions, COX activities and levels of representative mRNAs derived from the two genomes in several tissues are correlated and the ratio of nuclear and mitochondrial mRNA expression is constant and coordinated.
However, in the case of hormonal regulation of oxidative metabolism and in the absence of mitochondrial replication and although both nuclear and mitochondrial gene products are needed for a correct assembly or activity of respiratory complexes [e. In the mitochondrial compartment, programmed by the nucleus with a given transcription potential, repression mechanisms activated by a local increase in ATP concentrations would determine the level at which this potential is used in each individual organelle B.
From Enriquez et al.
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T3 induces transcripts for nuclear-encoded subunits IV, Va, and VI of cytochrome oxidase within 24 hr in rat liver, whereas the mitochondrial mRNAs were elevated with a considerable time lag. The reverse is true in the skeletal muscle rapid increase of mitochondrial mRNAs and delay of accumulation of nuclear mRNAs. In every case, however, transcript levels are correlated with enzyme levels in both tissues, which conforms to a regulation of transcription as the main control mechanism by T3 in liver and muscle Wiesner et al. The possibility of hormonal regulation of gene products controlling assembly or stability of mitochondria Altamura et al.
As already mentioned, dexamethasone stimulates transcription of the genes encoding cytochrome c oxidase subunits II and III, but not of the nuclear-encoded subunit VI gene.
As reported by Capaldi and Kadenbach et al. Based on our knowledge of the molecular mechansims of steroid and thyroid hormone regulation of nuclear genes, it is possible to hypothesize that not only the nuclear but also the mitochondrially encoded OXPHOS are likely regulated.
As regards nuclear genes, although more than such genes encode subunits of OXPHOs, only nine are induced by T3, and only in rare cases have sequences corresponding to TREs in their regulatory regions been detected Pillar and Seitz, In only one case, that of the cytochrome c1 gene, has the sequence proved by TR-DNA binding to be involved in T3 regulation and to respond directly to thyroid receptor-mediated induction Nelson et al. These observations and the time period needed for manisfestation of the hormonal effect led Pillar and Seitz and Scarpulla to question a direct effect of T3 on the majority of genes involved in oxidative phosphorylation.
As mentioned in Section IV. Virbasius and Scarpulla made the important observation that the mt TFA gene possesses NRF-1 but also NRF-2binding sites in its promoter, and that activity of mt TFA is dependent on binding of the nuclear factors on its promoter, providing a link between the expression of nuclear and mitochondrial genes. It is important to note that the mt TFA gene possesses a TRE in its regulatory region and is T3 induced, indirectly linking T3 action and mitochondrial gene transcription. However, as regards dexamethasone, no effect of the hormone on TFA gene transcription could be observed in rat muscle under conditions of increased mt gene transcription Larsson et al.
Suzuki et al. Nuclear protein factors that recognize nuclear Mt3 and Mt4 cis-elements and the respective trans-acting protein regulatory factors are shared by the two genetic systems and these trans-acting factors are involved in the communication between the nuclear and mt genomes. Binding of proteins to these REBOX sequences in gel mobility assays is sensitive to the presence of T3 or the reducing agent dithiothreitol Chang et al.
The scanning of the mt genome for putative binding sites for other regulatory molecules has revealed sequences homologous to ones present in the nuclear genome for several known transcription factors Solakidi and Sekeris, submitted. Coordination of nuclear-mitochondrial transcription also involves signals emanating from the mitochondria and directed to the nucleus, as demonstrated by the sensitivity of expression of nuclear genes to the functional state of the mitochondria.
This interorganelle communication, called retrograde regulation, is beeing studied mainly in yeast. Available data point to a role of the Rtg1 protein as both a positive and negative regulator of the retrograde response.
Meertens et al. The presence of glucocorticoid and thyroid hormore receptors in mitochondria of animal cells, described in Section IV. C considered in the context of the effects of these hormones on mt-RNA synthesis, was a strong indication that the respective hormones, by way of their receptors, could directly affect mitochondrial transcription. This hypothesis was further supported by the demonstration of the presence of putative GREs and TREs at various sites of the mitochondrial genome, hormone response elements that were shown to bind the respective receptors in gel shift assays and to confer hormone responsiveness in transfection studies, applying various constructs consisting of reporter genes linked to the HREs.
The in organello mitochondrial system described in Section IV. Although initiation, on the basis of the dimethyl sulfate footprinting patterns, is the transcription stage affected by T3, the placing of putative HREs for glucocorticoid hormone and TH within the structural mt genes, some in the boundary between the 16 S ribosomal gene and leu-tRNA Demonakos et al. In liver Gadaleta et al.
The results of the studies mentioned above lead to the conclusion that mitochondrial gene transcription is subjected to hormonal regulation, both by signals emanating from the nucleus in response to a primary action of the hormones on nuclear genes encoding mitochondrial transcription factors and by the direct action of the hormones on mitochondrial genes by way of the mitochondrially localized hormone receptors Fig. Details are in the text Section IV.
Concluding Remarks The detection of glucocorticoid and thyroid receptors in mitochondria of animal cells and of nucleotide sequences in the mitochondrial genome, with similarity to hormone responsive elements, focused attention on the potential role of these receptors in mitochondrial gene transcription. Steroid and thyroid hormones regulate mitochondrial energy production in part through stimulation of OXPHOS gene transcription and the known molecular mode of action of the hormones on nuclear gene transcription involves binding of the hormone to cognate receptors and interaction with HREs.