Assembly of the ribonucleoprotein complex containing the mRNA of the β-subunit of the mitochondrial H+-ATP synthase requires the participation of two distal cis-acting elements and a complex set of cellular trans-acting proteins

Biochemical Journal

Volumn 365, Issue 2, 2002, Pages 417-428

  Ricart, Javier ^a,b   Izquierdo, José M ^a,c   Di Liegro, Carlo M ^a   Cuezva, José M ^a  

^a CSIC   (Spain)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c UNIVERSITY OF PALERMO   (Italy)

Author keywords

MRNA localization; Oxidative phosphorylation; Translation

Indexed keywords

PROTEINS; RNA; SEDIMENTATION;

MITROCHONDRIAL PRESEQUENCE;

BIOCHEMISTRY;

EDETIC ACID; MESSENGER RNA; PROTEIN; PROTEIN P88; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; RIBONUCLEOPROTEIN; SUCROSE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHIMERA; COMPLEX FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CROSS LINKING; FEMALE; FETUS; IN SITU HYBRIDIZATION; IN VITRO STUDY; LIVER CELL; MITOCHONDRION; NONHUMAN; OPEN READING FRAME; OXIDATIVE PHOSPHORYLATION; POLYSOME; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RAT; RETICULOCYTE LYSATE; RNA TRANSLATION; SEDIMENTATION; STRUCTURE ANALYSIS;

3' UNTRANSLATED REGIONS; ANIMALS; BLOTTING, WESTERN; FEMALE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MITOCHONDRIA, LIVER; PREGNANCY; PROTON-TRANSLOCATING ATPASES; RATS; RATS, WISTAR; RNA, MESSENGER; RNA-BINDING PROTEINS;

ANIMALIA; MAMMALIA;

EID: 0037101778     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20011726     Document Type: Article

References (58)

1. Boyer, P. D. (1997) The ATP synthase. A splendid molecular machine. Annu. Rev. Biochem. 66, 717-749
2. Dey, R. and Moraes, C. T. (2000) Lack of oxidative phosphorylation and low mitochondrial membrane potential decrease susceptibility to apoptosis and do not modulate the protective effect of Bcl-x(L) in osteosarcoma cells. J. Biol. Chem. 275, 7087-7094
3. Harris, M. H., Vander Heiden, M. G., Kron, S. J. and Thompson, C. B. (2000) Role of oxidative phosphorylation in Bax toxicity. Mol. Cell Biol. 20, 3590-3596
4. Matsuyama, S., Llopis, J., Deveraux, Q. L., Tsien, R. Y. and Reed, J. C. (2000) Changes in intramitochondrial and cytosolic pH: early events that modulate caspase activation during apoptosis. Nat. Cell. Biol. 2, 318-325
5. Matsuyama, S., Xu, Q., Velours, J. and Reed, J. C. (1998) The mitochondrial F0F1-ATPase proton pump is required for function of the proapoptotic protein Bax in yeast and mammalian cells. Mol. Cell 1, 327-336
6. Cuezva, J. M., Ostronoff, L. K., Ricart, J., López de Heredia, M., Di Liegro, C. M. and Izquierdo, J. M. (1997) Mitochondrial biogenesis in the liver during development and oncogenesis. J Bioenerg. Biomembr. 29, 365-377
7. Izquierdo, J. M. and Cuezva, J. M. (1997) Control of the translational efficiency of β-F1-ATPase mRNA depends on the regulation of a protein that binds the 3′-untranslated region of the mRNA. Mol. Cell Biol. 17, 5255-5268
8. Izquierdo, J. M., Ricart, J., Ostronoff, L. K., Egea, G. and Cuezva, J. M. (1995) Changing patterns of transcriptional and post-transcriptional control of β-F1-ATPase gene expression during mitochondrial biogenesis in liver. J. Biol. Chem. 270, 10342-10350
9. Luis, A. M., Izquierdo, J. M., Ostronoff, L. K., Salinas, M., Santarén, J. F. and Cuezva, J. M. (1993) Translational regulation of mitochondrial differentiation in neonatal rat liver. Specific increase in the translational efficiency of the nuclear-encoded mitochondrial β-F1-ATPase mRNA. J. Biol. Chem. 268, 1868-1875
10. López de Heredia, M., Izquierdo, J. M. and Cuezva, J. M. (2000) A conserved mechanism for controlling the translation of β-F1-ATPase mRNA between the fetal liver and cancer cells. J. Biol. Chem. 275, 7430-7437
11. Egea, G., Izquierdo, J. M., Ricart, J., San Martín, C. and Cuezva, J. M. (1997) mRNA encoding the β-subunit of the mitochondrial F1-ATPase complex is a localized mRNA in rat hepatocytes. Biochem. J. 322, 557-565
12. Lithgow, T., Cuezva, J. M. and Silver, P. A. (1997) Highways for protein delivery to the mitochondria. Trends Biochem. Sci. 22, 110-113
13. +-ATP synthase in rat hepatocytes is translationally active. Biochem. J. 324, 635-643
14. Oleynikov, Y. and Singer, R. H. (1998) RNA localization: different zipcodes, same postman? Trends Cell. Biol. 8, 381-383
15. Carson, J. H., Kwon, S. and Barbarese, E. (1998) RNA trafficking in myelinating cells. Curr. Opin. Neurobiol. 8, 607-612
16. Kiebler, M. A. and DesGroseillers, L. (2000) Molecular insights into mRNA transport and local translation in the mammalian nervous system. Neuron 25, 19-28
17. Bassell, G. J., Zhang, H., Byrd, A. L., Femino, A. M., Singer, R. H., Taneja, K. L., Lifshitz, L M., Herman, I. M. and Kosik, K. S. (1998) Sorting of β-actin mRNA and protein to neurites and growth cones in culture. J. Neurosci. 18, 251-265
18. Kohrmann, M., Luo, M., Kaether, C., DesGroseillers, L., Dotti, C. G. and Kiebler, M. A. (1999) Microtubule-dependent recruitment of Staufen-green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons. Mol. Biol. Cell 10, 2945-2953
19. Marión, R. M, Fortes, P., Beloso, A., Dotti, C. and Ortin, J. (1999) A human sequence homologue of Staufen is an RNA-binding protein that is associated with polysomes and localizes to the rough endoplasmic reticulum. Mol. Cell Biol. 19, 2212-2219
20. Wickham, L., Duchaine, T., Luo, M., Nabi, I. R. and DesGroseillers, L. (1999) Mammalian staufen is a double-stranded-RNA- and tubulin-binding protein which localizes to the rough endoplasmic reticulum. Mol. Cell Biol. 19, 2220-2230
21. Di Liegro, C. M., Bellafiore, M., Izquierdo, J. M., Rantanen, A. and Cuezva, J. M. (2000) 3′-Untranslated regions of oxidative phosphorylation mRNAs function in vivo as enhancers of translation. Biochem. J. 352, 109-115
22. +-ATP synthase. Biochem. J. 346, 849-855
23. Danthinne, X., Seurinck, J., Meulewaeter, F., Van Montagu, M. and Cornelissen, M. (1993) The 3′-untranslated region of satellite tobacco necrosis virus RNA stimulates translation in vitro. Mol. Cell Biol. 13, 3340-3349
24. Hann, L. E., Webb, A. C., Cai, J. M. and Gehrke, L. (1997) Identification of a competitive translation determinant in the 3′-untranslated region of alfalfa mosaic virus coat protein mRNA. Mol. Cell Biol. 17, 2005-2013
25. Wang, S., Browning, K. S. and Miller, W. A. (1997) A viral sequence in the 3′-untranslated region mimics a 5′ cap in facilitating translation of uncapped mRNA. EMBO J. 16, 4107-4116
26. Bashirullah, A., Cooperstock, R. L. and Lipshitz, H. D. (1998) RNA localization in development. Annu. Rev. Biochem. 67, 335-394
27. 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
28. Hazelrigg, T. (1998) The destinies and destinations of RNAs. Cell (Cambridge, Mass.) 95, 451-460
29. Ades, I. Z. and Butow, R. A. (1980) The products of mitochondria-bound cytoplasmic polysomes in yeast. J. Biol. Chem. 255, 9918-9924
30. 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 proteins in vivo. Mol. Microbiol. 31, 1499-1511
31. Corral-Debrinski, M., Blugeon, C. and Jacq, C. (2000) In yeast, the 3′-untranslated region or the presequence of ATM1 is required for the exclusive localization of its mRNA to the vicinity of mitochondria. Mol. Cell Biol. 20, 7881-7892
32. Ellis, E. M. and Reid, G. A. (1993) The Saccharomyces cerevisiae MTS1 gene encodes a putative RNA-binding protein involved in mitochondrial protein targeting. Gene 132, 175-183
33. Suissa, M. and Schatz, G. (1982) Import of proteins into mitochondria. Translatable mRNAs for imported mitochondrial proteins are present in free as well as mitochondria-bound cytoplasmic polysomes. J. Biol. Chem. 257, 13048-13055
34. Zoladek, T., Vaduva, G., Hunter, L. A., Boguta, M., Go, B. D., Martin, N. C. and Hopper, A. K. (1995) Mutations altering the mitochondrial-cytoplasmic distribution of Mod5p implicate the actin cytoskeleton and mRNA 3′ ends and/or protein synthesis in mitochondrial delivery. Mol. Cell Biol. 15, 6884-8894
35. Ni, L., Heard, T. S. and Weiner, H. (1999) In vivo 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
36. Valcarce, C., Navarrete, R M., Encabo, P., Loeches, E., Satrústegui, J. and Cuezva, J. M. (1988) Postnatal development of rat liver mitochondrial functions. The roles of protein synthesis and of adenine nucleotides. J. Biol. Chem. 263, 7767-7775
37. Izquierdo, J. M. and Cuezva, J. M. (1993) Thyroid hormones promote transcriptional activation of the nuclear gene coding for mitochondrial β-F1-ATPase in rat liver. FEBS Lett. 323, 109-112
38. Lee, J. H., Garboczi, D. N., Thomas, P. J. and Pedersen, P. L. (1990) Mitochondrial ATP synthase. cDNA cloning, amino acid sequence, overexpression, and properties of the rat liver α subunit. J. Biol. Chem. 265, 4664-4669
39. Elkon, K. B., Pamassa, A. P. and Foster, C. L. (1985) Lupus autoantibodies target ribosomal P proteins. J. Exp. Med. 162, 459-471
40. 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
41. Wachter, C, Schatz, G. and Glick, B. S. (1994) Protein import into mitochondria: the requirement for external ATP is precursor-specific whereas intramitochondrial ATP is universally needed for translocation into the matrix. Mol. Biol. Cell 5, 465-474
42. Dibbens, J. A., Miller, D. L., Damert, A., Risau, W., Vadas, M. A. and Goodall, G. J. (1999) Hypoxic regulation of vascular endothelial growth factor mRNA stability requires the cooperation of miltiple RNA elements. Mol. Biol. Cell 10, 907-919
43. Grosset, C., Chen, C. Y., Xu, N., Sonenberg, N., Jacquemin-Sablon, H. and Shyu, A. B. (2000) A mechanism for translationally coupled mRNA turnover: interaction between the poly(A) tail and a c-fos RNA coding determinant via a protein complex. Cell (Cambridge, Mass.) 103, 29-40
44. Gunkel, N., Yano, T., Markussen, F. H., Olsen, L. C. and Ephrussi, A. (1998) Localization-dependent translation requires a functional interaction between the 5′ and 3′ ends of oskar mRNA. Genes Dev. 12, 1652-1664
45. Guo, L., Allen, E. M. and Miller, W. A. (2001) Base-pairing between untranslated regions facilitates translation of uncapped, nonpolyadenylated viral RNA. Mol. Cell 7, 1103-1109
46. Thio, G. L., Ray, R. P., Barcelo, G. and Schupbach, T. (2000) Localization of gurken RNA in Drosophila oogenesis requires elements in the 5′ and 3′ regions of the transcript. Dev. Biol. 221, 435-446
47. Johannes, G. and Sarnow, P. (1998) Cap-independent polysomal association of natural mRNAs encoding c-myc, BiP, and elF4G conferred by internal ribosome entry sites. RNA 4, 1500-1513
48. Hentze, M. W. (1997) elF4G: a multipurpose ribosome adapter? Science 275, 500-501
49. Preiss, T. and Hentze, M. W. (1999) From factors to mechanisms: translation and translational control in eukaryotes. Curr. Opin. Genet. Dev. 9, 515-521
50. Tarun, Jr. S. Z. and Sachs, A. B. (1996) Association of the yeast poly(A) tail binding protein with translation initiation factor elF-4G. EMBO J. 15, 7168-7177
51. Ito, T., Tahara, S. M. and Lai, M. M. (1998) The 3′-untranslated region of hepatitis C virus RNA enhances translation from an internal ribosomal entry site. J. Virol. 72, 8789-8796
52. Williamson, J. R. (2000) Induced fit in RNA-protein recognition. Nat. Struct. Biol. 7, 834-837
53. Lipshitz, H. D. and Smibert, C. A. (2000) Mechanisms of RNA localization and translational regulation. Curr. Opin. Genet. Dev. 10, 476-488
54. Fujiki, M. and Verner, K. (1991) Coupling of protein synthesis and mitochondrial import in a homologous yeast in vitro system. J. Biol. Chem. 266, 6841-6847
55. Fujiki, M. and Verner, K. (1993) Coupling of cytosolic protein synthesis and mitochondrial protein import in yeast. Evidence for cotranslational import in vivo. J. Biol. Chem. 268, 1914-1920
56. Funfschilling, U. and Rospert, S. (1999) Nascent polypeptide-associated complex stimulates protein import into yeast mitochondria. Mol. Biol. Cell 10, 3289-3299
57. Ferro-Novick, S., Hansen, W., Schauer, I. and Schekman, R. (1984) Genes required for completion of import of proteins into the endoplasmic reticulum in yeast. J. Cell. Biol. 98, 44-53
58. Schatz, G. and Dobberstein, B. (1996) Common principles of protein translocation across membranes. Science 271, 1519-1526