Abstract
We recently demonstrated, using yeast DNA microarrays, that mRNAs of polysomes that coisolate with mitochondria code for a subset of mitochondrial proteins. The majority of these mRNAs encode proteins of prokaryotic origin. Herein, we show that a similar association occurs between polysomes and mitochondria in human cells. To determine whether mRNA transport machinery is conserved from yeast to human cells, we examined the subcellular localization of human OXA1 mRNA in yeast. Oxa1p is a key component in the biogenesis of mitochondrial inner membrane and is conserved from bacteria to eukaryotic organelles. The expression of human OXA1 cDNA partially restores the respiratory capacity of yeast oxa1–cells. In this study, we demonstrate that 1) OXA1 mRNAs are remarkably enriched in mitochondrion-bound polysomes purified from yeast and human cells; 2) the presence of the human OXA1 3′ untranslated region (UTR) is required for the function of the human Oxa1p inside yeast mitochondria; and 3) the accurate sorting of the human OXA1 mRNA to the vicinity of yeast mitochondria is due to the recognition by yeast proteins of the human 3′ UTR. Therefore, it seems that the recognition mechanism of OXA1 3′ UTR is conserved throughout evolution and is necessary for Oxa1p function.
References
27
Referenced
117
-
Bassell, G.J., Oleynikov, Y., and Singer, R.H. (1999). The travels of mRNAs through all cells large and small.FASEB J.13, 447–454.
(
10.1096/fasebj.13.3.447
) -
Beach, D.L., Salmon, E.D., and Bloom, K. (1999). Localization and anchoring of mRNA in budding yeast.Curr. Biol.9, 569–578.
(
10.1016/S0960-9822(99)80260-7
) -
Bonnefoy, N., Kermorgant, M., Groudinsky, O., and Dujardin, G. (2000). The respiratory geneOXA1has two fission yeast orthologs which together encode a function essential for cellular viability.Mol. Microbiol.35, 1135–1145.
(
10.1046/j.1365-2958.2000.01781.x
) -
Bonnefoy, N., Kermorgant, M., Groudinsky, O., Minet, M., Slonimski, P.P., and Dujardin, G. (1994). Cloning of a human gene involved in cytochrome oxidase assembly by functional complementation of an oxa1–mutation inSaccharomyces cerevisiae.Proc. Natl. Acad. Sci. USA91, 11978–11982.
(
10.1073/pnas.91.25.11978
) -
Chartrand, P., Meng, X.H., Singer, R.H., and Long, R.M. (1999). Structural elements required for the localization of Ash1 mRNA and of a green fluorescent protein reporter particlein vivo.Curr. Biol.9, 333–336.
(
10.1016/S0960-9822(99)80144-4
) -
Corral-Debrinski, M., Belgareh, N., Blugeon, C., Claros, M.G., Doye, V., and Jacq, C. (1999). Overexpression of yeast karyopherin Pse1p/Kap121p stimulates the mitochondrial import of hydrophobic proteinsin vivo.Mol. Microbiol.31, 1499–1511.
(
10.1046/j.1365-2958.1999.01295.x
) -
Corral-Debrinski, M., Blugeon, C., and Jacq, C. (2000). In yeast, the 3′ Untranslated region or the presequence ofATM1is required for the exclusive localization of its mRNA to the vicinity of mitochondria.Mol. Cell. Biol.20, 7881–7892.
(
10.1128/MCB.20.21.7881-7892.2000
) 10.1091/mbc.10.10.3289
-
George, R., Walsh, P., Beddoe, T., and Lithgow, T. (2002). The nascent polypeptide-associated complex (NAC) promotes interaction of ribosome with the mitochondrial surface in vivo.FEBS Lett.516, 213–216.
(
10.1016/S0014-5793(02)02528-0
) -
Gietz, D., St. Jean, A., Woods, R.A., and Schiestl, R.H. (1992). Improved method for high efficiency transformation of intact yeast cells.Nucleic Acids Res.20, 1425
(
10.1093/nar/20.6.1425
) - Gonzalez, I., Buonomo, S.B.C., Nasmyth, K., and Ahsen, U.V. (1999)ASH1mRNA. localization in yeasts involves multiple secondary elements and Ash1 protein translation.Curr. Biol.9, 337–340.
-
Hamel, P., Sakamoto, W., Wintz, H., and Dujardin, G. (1997). Functional complementation of an oxa1–yeast mutation identifies anArabidopsis thalianacDNA involved in the assembly of respiratory complexes.Plant J.12, 1319–1327.
(
10.1046/j.1365-313x.1997.12061319.x
) -
Hermann, J.M., and Neupert, W. (2000). Protein transport into mitochondria.Curr. Opin. Microbiol.3, 210–214.
(
10.1016/S1369-5274(00)00077-1
) -
Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., and Pearse, L.R. (1989). Site-directed mutageneses by overlap extension using the polymerase chain reaction.Gene77, 51–59.
(
10.1016/0378-1119(89)90358-2
) -
Jansen, R.P. (2001). mRNA localization: message on the move. Nature reviews.Mol. Cell. Biol.2, 247–256.
(
10.1038/35067016
) -
Luirink, J., Samuelsson, T., and Gier, J.W.D. (2001) YidC/Oxa1p/Alb3: evolutionarily conserved mediators of membrane protein assembly.FEBS Lett.501, 1–5.
(
10.1016/S0014-5793(01)02616-3
) -
Marc, P., Margeot, A., Devaux, F., Blugeon, C., Corral-Debrinski, M., and Jacq, C. (2002). Genome-wide analysis of mRNAs targeted to yeast mitochondria.EMBO Rep.3, 159–164.
(
10.1093/embo-reports/kvf025
) -
Margeot, A., Blugeon, C., Sylvestre, J., Jacq, C., and Corral-Debrinski, M. (2002). InSaccharomyces cerevisiae, ATP2mRNA sorting to the vicinity of mitochondria is essential for respiratory function.EMBO J.21, 6893–6904.
(
10.1093/emboj/cdf690
) -
Minet, M., Dufour, M.E., and Lacroute, F. (1992). Complementation ofSaccharomyces cerevisiaeauxotrophic mutants byArabidopsis thalianacDNAs.Plant J.2, 417–422.
(
10.1046/j.1365-313X.1992.t01-38-00999.x
) -
Nargang, F.E., Preuss, M., Neupert, W., and Herrmann, J.M. (2002). The Oxa1 protein forms a homooligomeric complex and is an essential part of the mitochondrial export translocase inNeurospora crassa.J. Biol. Chem.277, 12846–12853.
(
10.1074/jbc.M112099200
) -
Ni, L., Heard, T.S., and Weiner, H. (1999). In vitro mitochondrial import: a comparison of leader sequence charge and structural relationships with the in vitro model resulting in evidence for co-translational import.J. Biol. Chem.274, 12685–12691.
(
10.1074/jbc.274.18.12685
) -
Nobumoto, M., Yamada, M., Song, S., Inouye, S., and Nakasawa, A. (1998). Mechanism of mitochondrial import of adenylate kinase enzymes.J. Biochem.123, 128–135.
(
10.1093/oxfordjournals.jbchem.a021899
) -
Rötig, A., Parfait, B., Heidet, L., Dujardin, G., Rustin, P., and Munnich, A. (1997). Sequence and structure of the humanOXA1Land its upstream elements.Biochem. Biophys. Acta1361, 6–10.
(
10.1016/S0925-4439(97)00031-8
) -
Saint-Georges, Y., Hamel, P., Lemaire, C., and Dujardin, G. (2001). Role of positively charged transmembrane segments in the insertion and assembly of mitochondrial inner-membrane proteins.Proc. Natl. Acad. Sci. USA98, 13814–13819.
(
10.1073/pnas.251503098
) - Sambrook, K.J., Fritsch, E.F., and Maniatis, T. (1989).Molecular Cloning, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
-
Tekotte, H., and Davis, I. (2002). Intracellular mRNA localization: motors move messages.Trends Genet.18, 636–642.
(
10.1016/S0168-9525(02)02819-6
) -
Zuker, M. (1989). On finding all suboptimal foldings of an RNA molecule.Science244, 48–52.
(
10.1126/science.2468181
)
Dates
Type | When |
---|---|
Created | 22 years, 2 months ago (June 16, 2003, 8:35 p.m.) |
Deposited | 1 year, 7 months ago (Jan. 9, 2024, 7:06 p.m.) |
Indexed | 1 month, 4 weeks ago (July 2, 2025, 2:31 p.m.) |
Issued | 21 years, 11 months ago (Sept. 1, 2003) |
Published | 21 years, 11 months ago (Sept. 1, 2003) |
Published Print | 21 years, 11 months ago (Sept. 1, 2003) |
@article{Sylvestre_2003, title={The Role of the 3′ Untranslated Region in mRNA Sorting to the Vicinity of Mitochondria Is Conserved from Yeast to Human Cells}, volume={14}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.e03-02-0074}, DOI={10.1091/mbc.e03-02-0074}, number={9}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Sylvestre, J. and Margeot, A. and Jacq, C. and Dujardin, G. and Corral-Debrinski, M.}, year={2003}, month=sep, pages={3848–3856} }