A Conserved Mechanism for Controlling the Translation of β-F1-ATPase mRNA between the Fetal Liver and Cancer Cells

To characterize the mechanisms governing the biogenesis of mitochondria in cancer, we studied the mitochondrial phenotype and the mechanisms controlling the expression of the β subunit of the mitochondrial H+-ATP synthase (β-F1-ATPase) gene in the rat FAO and AS30D hepatomas. When compared with normal adult rat liver, the relative cellular content of the mitochondrial β-F1-ATPase and glutamate dehydrogenase, as well as of mitochondrial DNA, was severely reduced in both cell lines. A paradoxical increase in the cellular abundance of β-F1-ATPase mRNA was observed in cancer cells. Run-on transcription assays and the estimation of mRNA half-lives revealed that the increased abundance of β-F1-ATPase mRNA results from the stabilization of the transcript in cancer. In vitro translation assays revealed a specific inhibition of the synthesis of the β-precursor when translation reactions were carried out in the presence of extracts derived from cancer cells. The inhibitory effect was recapitulated using an RNA chimera that contained the 3′-untranslated region of β-F1-ATPase mRNA. Hepatoma extracts also contained an increased activity of the developmentally regulated translation-inhibitory proteins that bind the 3′-untranslated region of β-F1-ATPase mRNA. The results indicate that the expression of this gene in hepatoma cells is controlled by the same mechanisms that regulate its expression in the liver during fetal development. To characterize the mechanisms governing the biogenesis of mitochondria in cancer, we studied the mitochondrial phenotype and the mechanisms controlling the expression of the β subunit of the mitochondrial H+-ATP synthase (β-F1-ATPase) gene in the rat FAO and AS30D hepatomas. When compared with normal adult rat liver, the relative cellular content of the mitochondrial β-F1-ATPase and glutamate dehydrogenase, as well as of mitochondrial DNA, was severely reduced in both cell lines. A paradoxical increase in the cellular abundance of β-F1-ATPase mRNA was observed in cancer cells. Run-on transcription assays and the estimation of mRNA half-lives revealed that the increased abundance of β-F1-ATPase mRNA results from the stabilization of the transcript in cancer. In vitro translation assays revealed a specific inhibition of the synthesis of the β-precursor when translation reactions were carried out in the presence of extracts derived from cancer cells. The inhibitory effect was recapitulated using an RNA chimera that contained the 3′-untranslated region of β-F1-ATPase mRNA. Hepatoma extracts also contained an increased activity of the developmentally regulated translation-inhibitory proteins that bind the 3′-untranslated region of β-F1-ATPase mRNA. The results indicate that the expression of this gene in hepatoma cells is controlled by the same mechanisms that regulate its expression in the liver during fetal development. β subunit of the mitochondrial H+-ATP synthase 3′-untranslated region 3′UTR β-F1-ATPase mRNA-binding proteins ADP ribosylation factor 1 electrophoretic mobility shift assay glyceraldehyde-3-phosphate dehydrogenase glutamate dehydrogenase mitochondrial ATPase subunits 6 and 8 mitochondrial DNA mitochondrial 12 S rRNA nucleotides polyacrylamide gel electrophoresis phosphoenolpyruvate carboxykinase A common feature of the phenotype of many cancer cells is their abnormal bioenergetics, i.e. an increased glycolytic capacity accompanied by an impaired respiration (1.Warburg O. Science. 1956; 123: 309-314Crossref PubMed Scopus (9322) Google Scholar, 2.Lo C. Cristofalo V.J. Morris H.P. Weinhouse S. Cancer Res. 1968; 28: 1-10PubMed Google Scholar, 3.Weinhouse S. Fed. Proc. 1973; 32: 2162-2167PubMed Google Scholar, 4.Pedersen P.L. Prog. Exp. Tumor Res. 1978; 22: 190-274Crossref PubMed Google Scholar, 5.Cuezva J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google The abnormal capacity of cancer cells a in the cellular content of mitochondria P.L. Prog. Exp. Tumor Res. 1978; 22: 190-274Crossref PubMed Google Scholar, 5.Cuezva J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google the the of mitochondrial biogenesis is in cancer is In this that a in their mitochondrial content P.L. Prog. Exp. Tumor Res. 1978; 22: 190-274Crossref PubMed Google Scholar, S. PubMed Scopus Google a paradoxical increase in the cellular abundance of mitochondrial proteins S. PubMed Scopus Google The paradoxical of also in PubMed Scopus Google Scholar, PubMed Scopus Google in cancer cells S. PubMed Scopus Google Scholar, PubMed Scopus Google as well as in cellular with and cellular S. PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Google biogenesis results from the expression of the and mitochondrial PubMed Scopus Google In the fetal liver that the mitochondrial content of the is reduced when compared with the adult C. J.M. PubMed Google Scholar, J.M. Ostronoff L.K. J.M. PubMed Google Scholar, J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google the fetal liver a paradoxical increase in the cellular of J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google Scholar, J.M. Ostronoff L.K. J.M. PubMed Google Scholar, J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google Scholar, L.K. J.M. J.M. Res. PubMed Scopus Google Scholar, L.K. J.M. J.M. PubMed Scopus Google of the liver, the expression of the gene of is the of the J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google and translation J.M. Ostronoff L.K. J.M. PubMed Google Scholar, J.M. J.M. PubMed Google of the the of the expression of the mitochondrial is also the same L.K. J.M. J.M. Res. PubMed Scopus Google Scholar, L.K. J.M. J.M. PubMed Scopus Google of translation of the β-F1-ATPase gene in the liver mechanisms that the of the transcript as J.M. J.M. PubMed Google The of β-F1-ATPase mRNA is a mRNA translation in the developmentally regulated inhibitory proteins bind controlling the expression of the mRNA J.M. J.M. PubMed Google we that the abnormal biogenesis of mitochondria in a a fetal of expression of J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google the of the mechanisms controlling the and translation of biogenesis in hepatomas. In the we studied the of this To this we the mitochondrial phenotype of the rat FAO and AS30D hepatoma cell lines. a reduced mitochondrial content when compared with the adult rat The results indicate the in cancer cells of the same mechanisms that the expression of the β-F1-ATPase gene in the liver during fetal development. hepatoma extracts also contained an increased activity of translation-inhibitory proteins that bind the of β-F1-ATPase mRNA. The results the that the paradoxical abnormal biogenesis of mitochondria in cancer cells. is that the in the mitochondrial content of cancer cells from the of mitochondrial during cellular as a of the by mitochondrial the biogenesis of that the paradoxical in the of mitochondria in cancer and cells from a a fetal of expression of in cells J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google In the we that derived from rat liver a in their mitochondrial when compared with normal adult rat The of the mitochondrial cellular of the in a paradoxical of an increased abundance of the transcript the mitochondrial β-F1-ATPase A observed in when compared with normal C. and in that in the fetal rat liver J.M. Ostronoff L.K. J.M. PubMed Google J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google and in cell in that with and cellular S. PubMed Scopus Google Scholar, PubMed Google the of common and the of the biogenesis of indicate that the increased abundance of β-F1-ATPase mRNA in is the of an increase in the transcription of the gene is by an increase in the mRNA A the cellular of the transcript in the fetal liver J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google In a specific translation the expression of β-F1-ATPase mRNA that the of the transcript as of also with the controlling the expression of the β-F1-ATPase gene during fetal liver J.M. J.M. PubMed Google hepatoma extracts an increased activity of of the same and the of β-F1-ATPase mRNA as the that the translation of β-F1-ATPase mRNA in the fetal liver J.M. J.M. PubMed Google the results that the expression of the β-F1-ATPase gene in and in cancer results from a in cancer the of expression of the gene that in the liver during J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google that the observed also the expression of in in the biogenesis of β-F1-ATPase mRNA in of the that controlling the of the transcript J.M. Ricart C. J.M. PubMed Scopus Google Scholar, J.M. C. J.M. PubMed Scopus Google as well as the of the mitochondria J.M. C. J.M. PubMed Scopus Google Scholar, J.M. 22: PubMed Scopus Google in the and of mRNA the of the PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google The of β-F1-ATPase mRNA is a that also the mRNA translation J.M. J.M. PubMed Google the of β-F1-ATPase we the of a of in the of in controlling its and In the in an during J.M. Ostronoff L.K. J.M. PubMed Google Scholar, J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google Scholar, J.M. J.M. PubMed Google in in the and in the cellular of the transcript in its translation In this we that proteins the of β-F1-ATPase mRNA in both of the of the In the translation of the mRNA its and its cellular both mechanisms the same cellular that as the regulated proteins that bind the of the transcript J.M. J.M. PubMed Google the in also an in the of in both the and mitochondrial in J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google Scholar, L.K. J.M. J.M. Res. PubMed Scopus Google the that a common controlling mRNA in both of the a that from that in cells PubMed Google the the that the of translation the expression of L.K. J.M. J.M. PubMed Scopus Google during J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google Scholar, C. J.M. PubMed Google that translation also the expression of in cancer of mechanisms of stabilization of and translation the in both the in the mitochondrial of cancer cells as a of cellular The of in cancer cells from the of mitochondrial during cellular is also that of the of also In this is that both DNA PubMed Scopus Google Scholar, PubMed Scopus Google and mitochondrial transcription factor A PubMed Scopus Google also with the of β-F1-ATPase mRNA translation in the fetal rat liver J.M. J.M. PubMed Google we that the increased activity of in the translation of β-F1-ATPase mRNA in cancer. of the proteins the of the the an of β-F1-ATPase mRNA translation J.M. J.M. PubMed Google the proteins that β-F1-ATPase mRNA translation in the fetal liver the same as in FAO and In is in the that a from the in S. PubMed Scopus Google is that the observed in AS30D and from of of in fetal liver and the FAO The of proteins the of translation of PubMed Google Scholar, PubMed Google Scholar, PubMed Scopus Google fetal liver and in the biogenesis of mitochondria S. Fed. Proc. 1973; 32: 2162-2167PubMed Google Scholar, 4.Pedersen P.L. Prog. Exp. Tumor Res. 1978; 22: 190-274Crossref PubMed Google Scholar, 5.Cuezva J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google Scholar, S. PubMed Scopus Google is that from common liver and is a and during J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google and also a feature of C. Cancer Res. Google an increased expression of in the glycolytic Res. PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google a of both the fetal liver and cancer cells S. Fed. Proc. 1973; 32: 2162-2167PubMed Google Scholar, 4.Pedersen P.L. Prog. Exp. Tumor Res. 1978; 22: 190-274Crossref PubMed Google Scholar, 5.Cuezva J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google Scholar, S. PubMed Scopus Google also an in the cellular of by controlling the of the PubMed Scopus Google Scholar, PubMed Google Scholar, S. PubMed Scopus Google In of the of mRNA is by proteins S. PubMed Scopus Google Scholar, PubMed Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, O. PubMed Scopus Google is that the of the and of β-F1-ATPase mRNA observed in the fetal rat liver J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google and in the the same and the of a H+-ATP synthase S. PubMed Scopus Google is a of cell that is normal of the PubMed Scopus Google and that also the of Science. PubMed Scopus Google Scholar, PubMed Scopus Google a as of cell PubMed Scopus Google Scholar, Science. PubMed Google a of cancer cells is their PubMed Scopus Google Scholar, C. Google In with that cancer cells mechanisms the cellular content of this mitochondrial In that the β-F1-ATPase an increased in the hepatoma S. PubMed Scopus Google this a of controlling the cellular content of the a that is regulated the of The of the of of mechanisms is the in the content activity of mitochondria in cancer cells. that a the of cancer cells that in that in the of C. PubMed Scopus Google the by mitochondria as and of PubMed Scopus Google Scholar, Science. PubMed Google that a mitochondrial content also cancer cells with a In this the of the that the activity of an cell in cell A common feature of the phenotype of many cancer cells is their abnormal bioenergetics, i.e. an increased glycolytic capacity accompanied by an impaired respiration (1.Warburg O. Science. 1956; 123: 309-314Crossref PubMed Scopus (9322) Google Scholar, 2.Lo C. Cristofalo V.J. Morris H.P. Weinhouse S. Cancer Res. 1968; 28: 1-10PubMed Google Scholar, 3.Weinhouse S. Fed. Proc. 1973; 32: 2162-2167PubMed Google Scholar, 4.Pedersen P.L. Prog. Exp. Tumor Res. 1978; 22: 190-274Crossref PubMed Google Scholar, 5.Cuezva J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google The abnormal capacity of cancer cells a in the cellular content of mitochondria P.L. Prog. Exp. Tumor Res. 1978; 22: 190-274Crossref PubMed Google Scholar, 5.Cuezva J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google the the of mitochondrial biogenesis is in cancer is In this that a in their mitochondrial content P.L. Prog. Exp. Tumor Res. 1978; 22: 190-274Crossref PubMed Google Scholar, S. PubMed Scopus Google a paradoxical increase in the cellular abundance of mitochondrial proteins S. PubMed Scopus Google The paradoxical of also in PubMed Scopus Google Scholar, PubMed Scopus Google in cancer cells S. PubMed Scopus Google Scholar, PubMed Scopus Google as well as in cellular with and cellular S. PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Google biogenesis results from the expression of the and mitochondrial PubMed Scopus Google In the fetal liver that the mitochondrial content of the is reduced when compared with the adult C. J.M. PubMed Google Scholar, J.M. Ostronoff L.K. J.M. PubMed Google Scholar, J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google the fetal liver a paradoxical increase in the cellular of J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google Scholar, J.M. Ostronoff L.K. J.M. PubMed Google Scholar, J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google Scholar, L.K. J.M. J.M. Res. PubMed Scopus Google Scholar, L.K. J.M. J.M. PubMed Scopus Google of the liver, the expression of the gene of is the of the J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google and translation J.M. Ostronoff L.K. J.M. PubMed Google Scholar, J.M. J.M. PubMed Google of the the of the expression of the mitochondrial is also the same L.K. J.M. J.M. Res. PubMed Scopus Google Scholar, L.K. J.M. J.M. PubMed Scopus Google of translation of the β-F1-ATPase gene in the liver mechanisms that the of the transcript as J.M. J.M. PubMed Google The of β-F1-ATPase mRNA is a mRNA translation in the developmentally regulated inhibitory proteins bind controlling the expression of the mRNA J.M. J.M. PubMed Google we that the abnormal biogenesis of mitochondria in a a fetal of expression of J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google the of the mechanisms controlling the and translation of biogenesis in hepatomas. In the we studied the of this To this we the mitochondrial phenotype of the rat FAO and AS30D hepatoma cell lines. a reduced mitochondrial content when compared with the adult rat The results indicate the in cancer cells of the same mechanisms that the expression of the β-F1-ATPase gene in the liver during fetal development. hepatoma extracts also contained an increased activity of translation-inhibitory proteins that bind the of β-F1-ATPase mRNA. The results the that the paradoxical abnormal biogenesis of mitochondria in cancer cells. is that the in the mitochondrial content of cancer cells from the of mitochondrial during cellular as a of the by mitochondrial the biogenesis of that the paradoxical in the of mitochondria in cancer and cells from a a fetal of expression of in cells J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google In the we that derived from rat liver a in their mitochondrial when compared with normal adult rat The of the mitochondrial cellular of the in a paradoxical of an increased abundance of the transcript the mitochondrial β-F1-ATPase A observed in when compared with normal C. and in that in the fetal rat liver J.M. Ostronoff L.K. J.M. PubMed Google J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google and in cell in that with and cellular S. PubMed Scopus Google Scholar, PubMed Google the of common and the of the biogenesis of indicate that the increased abundance of β-F1-ATPase mRNA in is the of an increase in the transcription of the gene is by an increase in the mRNA A the cellular of the transcript in the fetal liver J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google In a specific translation the expression of β-F1-ATPase mRNA that the of the transcript as of also with the controlling the expression of the β-F1-ATPase gene during fetal liver J.M. J.M. PubMed Google hepatoma extracts an increased activity of of the same and the of β-F1-ATPase mRNA as the that the translation of β-F1-ATPase mRNA in the fetal liver J.M. J.M. PubMed Google the results that the expression of the β-F1-ATPase gene in and in cancer results from a in cancer the of expression of the gene that in the liver during J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google that the observed also the expression of in in the biogenesis of β-F1-ATPase mRNA in of the that controlling the of the transcript J.M. Ricart C. J.M. PubMed Scopus Google Scholar, J.M. C. J.M. PubMed Scopus Google as well as the of the mitochondria J.M. C. J.M. PubMed Scopus Google Scholar, J.M. 22: PubMed Scopus Google in the and of mRNA the of the PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google The of β-F1-ATPase mRNA is a that also the mRNA translation J.M. J.M. PubMed Google the of β-F1-ATPase we the of a of in the of in controlling its and In the in an during J.M. Ostronoff L.K. J.M. PubMed Google Scholar, J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google Scholar, J.M. J.M. PubMed Google in in the and in the cellular of the transcript in its translation In this we that proteins the of β-F1-ATPase mRNA in both of the of the In the translation of the mRNA its and its cellular both mechanisms the same cellular that as the regulated proteins that bind the of the transcript J.M. J.M. PubMed Google the in also an in the of in both the and mitochondrial in J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google Scholar, L.K. J.M. J.M. Res. PubMed Scopus Google the that a common controlling mRNA in both of the a that from that in cells PubMed Google the the that the of translation the expression of L.K. J.M. J.M. PubMed Scopus Google during J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google Scholar, C. J.M. PubMed Google that translation also the expression of in cancer of mechanisms of stabilization of and translation the in both the in the mitochondrial of cancer cells as a of cellular The of in cancer cells from the of mitochondrial during cellular is also that of the of also In this is that both DNA PubMed Scopus Google Scholar, PubMed Scopus Google and mitochondrial transcription factor A PubMed Scopus Google also with the of β-F1-ATPase mRNA translation in the fetal rat liver J.M. J.M. PubMed Google we that the increased activity of in the translation of β-F1-ATPase mRNA in cancer. of the proteins the of the the an of β-F1-ATPase mRNA translation J.M. J.M. PubMed Google the proteins that β-F1-ATPase mRNA translation in the fetal liver the same as in FAO and In is in the that a from the in S. PubMed Scopus Google is that the observed in AS30D and from of of in fetal liver and the FAO The of proteins the of translation of PubMed Google Scholar, PubMed Google Scholar, PubMed Scopus Google fetal liver and in the biogenesis of mitochondria S. Fed. Proc. 1973; 32: 2162-2167PubMed Google Scholar, 4.Pedersen P.L. Prog. Exp. Tumor Res. 1978; 22: 190-274Crossref PubMed Google Scholar, 5.Cuezva J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google Scholar, S. PubMed Scopus Google is that from common liver and is a and during J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google and also a feature of C. Cancer Res. Google an increased expression of in the glycolytic Res. PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google a of both the fetal liver and cancer cells S. Fed. Proc. 1973; 32: 2162-2167PubMed Google Scholar, 4.Pedersen P.L. Prog. Exp. Tumor Res. 1978; 22: 190-274Crossref PubMed Google Scholar, 5.Cuezva J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google Scholar, S. PubMed Scopus Google also an in the cellular of by controlling the of the PubMed Scopus Google Scholar, PubMed Google Scholar, S. PubMed Scopus Google In of the of mRNA is by proteins S. PubMed Scopus Google Scholar, PubMed Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, O. PubMed Scopus Google is that the of the and of β-F1-ATPase mRNA observed in the fetal rat liver J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google and in the the same and the of a H+-ATP synthase S. PubMed Scopus Google is a of cell that is normal of the PubMed Scopus Google and that also the of Science. PubMed Scopus Google Scholar, PubMed Scopus Google a as of cell PubMed Scopus Google Scholar, Science. PubMed Google a of cancer cells is their PubMed Scopus Google Scholar, C. Google In with that cancer cells mechanisms the cellular content of this mitochondrial In that the β-F1-ATPase an increased in the hepatoma S. PubMed Scopus Google this a of controlling the cellular content of the a that is regulated the of The of the of of mechanisms is the in the content activity of mitochondria in cancer cells. that a the of cancer cells that in that in the of C. PubMed Scopus Google the by mitochondria as and of PubMed Scopus Google Scholar, Science. PubMed Google that a mitochondrial content also cancer cells with a In this the of the that the activity of an cell in cell that the paradoxical in the of mitochondria in cancer and cells from a a fetal of expression of in cells J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google In the we that derived from rat liver a in their mitochondrial when compared with normal adult rat The of the mitochondrial cellular of the in a paradoxical of an increased abundance of the transcript the mitochondrial β-F1-ATPase A observed in when compared with normal C. and in that in the fetal rat liver J.M. Ostronoff L.K. J.M. PubMed Google J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google and in cell in that with and cellular S. PubMed Scopus Google Scholar, PubMed Google the of common and the of the biogenesis of The indicate that the increased abundance of β-F1-ATPase mRNA in is the of an increase in the transcription of the gene is by an increase in the mRNA A the cellular of the transcript in the fetal liver J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google In a specific translation the expression of β-F1-ATPase mRNA that the of the transcript as of also with the controlling the expression of the β-F1-ATPase gene during fetal liver J.M. J.M. PubMed Google hepatoma extracts an increased activity of of the same and the of β-F1-ATPase mRNA as the that the translation of β-F1-ATPase mRNA in the fetal liver J.M. J.M. PubMed Google the results that the expression of the β-F1-ATPase gene in and in cancer results from a in cancer the of expression of the gene that in the liver during J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google that the observed also the expression of in in the biogenesis of The β-F1-ATPase mRNA in of the that controlling the of the transcript J.M. Ricart C. J.M. PubMed Scopus Google Scholar, J.M. C. J.M. PubMed Scopus Google as well as the of the mitochondria J.M. C. J.M. PubMed Scopus Google Scholar, J.M. 22: PubMed Scopus Google in the and of mRNA the of the PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google The of β-F1-ATPase mRNA is a that also the mRNA translation J.M. J.M. PubMed Google the of β-F1-ATPase we the of a of in the of in controlling its and In the in an during J.M. Ostronoff L.K. J.M. PubMed Google Scholar, J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google Scholar, J.M. J.M. PubMed Google in in the and in the cellular of the transcript in its translation In this we that proteins the of β-F1-ATPase mRNA in both of the of the In the translation of the mRNA its and its cellular both mechanisms the same cellular that as the regulated proteins that bind the of the transcript J.M. J.M. PubMed Google the in also an in the of in both the and mitochondrial in J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google Scholar, L.K. J.M. J.M. Res. PubMed Scopus Google the that a common controlling mRNA in both of the a that from that in cells PubMed Google the the that the of translation the expression of L.K. J.M. J.M. PubMed Scopus Google during J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google Scholar, C. J.M. PubMed Google that translation also the expression of in cancer cells. The of mechanisms of stabilization of and translation the in both the in the mitochondrial of cancer cells as a of cellular The of in cancer cells from the of mitochondrial during cellular is also that of the of also In this is that both DNA PubMed Scopus Google Scholar, PubMed Scopus Google and mitochondrial transcription factor A PubMed Scopus Google also In with the of β-F1-ATPase mRNA translation in the fetal rat liver J.M. J.M. PubMed Google we that the increased activity of in the translation of β-F1-ATPase mRNA in cancer. of the proteins the of the the an of β-F1-ATPase mRNA translation J.M. J.M. PubMed Google the proteins that β-F1-ATPase mRNA translation in the fetal liver the same as in FAO and In is in the that a from the in S. PubMed Scopus Google is that the observed in AS30D and from of of in fetal liver and the FAO The of proteins the of translation of PubMed Google Scholar, PubMed Google Scholar, PubMed Scopus Google The fetal liver and in the biogenesis of mitochondria S. Fed. Proc. 1973; 32: 2162-2167PubMed Google Scholar, 4.Pedersen P.L. Prog. Exp. Tumor Res. 1978; 22: 190-274Crossref PubMed Google Scholar, 5.Cuezva J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google Scholar, S. PubMed Scopus Google is that from common liver and is a and during J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google and also a feature of C. Cancer Res. Google an increased expression of in the glycolytic Res. PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google a of both the fetal liver and cancer cells S. Fed. Proc. 1973; 32: 2162-2167PubMed Google Scholar, 4.Pedersen P.L. Prog. Exp. Tumor Res. 1978; 22: 190-274Crossref PubMed Google Scholar, 5.Cuezva J.M. Ostronoff L.K. Ricart J.M. PubMed Scopus Google Scholar, S. PubMed Scopus Google also an in the cellular of by controlling the of the PubMed Scopus Google Scholar, PubMed Google Scholar, S. PubMed Scopus Google In of the of mRNA is by proteins S. PubMed Scopus Google Scholar, PubMed Google Scholar, PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, O. PubMed Scopus Google is that the of the and of β-F1-ATPase mRNA observed in the fetal rat liver J.M. Ricart Ostronoff L.K. J.M. PubMed Scopus Google and in the the same and the of a H+-ATP synthase S. PubMed Scopus Google is a of cell that is normal of the PubMed Scopus Google and that also the of Science. PubMed Scopus Google Scholar, PubMed Scopus Google a as of cell PubMed Scopus Google Scholar, Science. PubMed Google a of cancer cells is their PubMed Scopus Google Scholar, C. Google In with that cancer cells mechanisms the cellular content of this mitochondrial In that the β-F1-ATPase an increased in the hepatoma S. PubMed Scopus Google this a of controlling the cellular content of the a that is regulated the of The of the of of mechanisms is the in the content activity of mitochondria in cancer cells. that a the of cancer cells that in that in the of C. PubMed Scopus Google the by mitochondria as and of PubMed Scopus Google Scholar, Science. PubMed Google that a mitochondrial content also cancer cells with a In this the of the that the activity of an cell in cell and the AS30D and FAO and the of and of as in this of the and and