Structural aspects of mitochondrial translational apparatus

Current Opinion in Structural Biology

Volumn 22, Issue 6, 2012, Pages 797-803

  Agrawal, Rajendra K ^a,b   Sharma, Manjuli R ^a  

^a WADSWORTH CENTER   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 1; INITIATION FACTOR 2; MEMBRANE PROTEIN; MESSENGER RNA; POLYPEPTIDE; PROTEIN OXA1P; RIBOSOME RNA; UNCLASSIFIED DRUG;

CELL FUNCTION; CELL INTERACTION; CRYOELECTRON MICROSCOPY; GENE INTERACTION; MAMMAL CELL; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL TRANSLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; REVIEW; RIBOSOME; RIBOSOME SUBUNIT; RNA STRUCTURE; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

ANIMALS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; PEPTIDES; PROKARYOTIC INITIATION FACTOR-2; PROTEIN BIOSYNTHESIS; RIBOSOMES;

BACTERIA (MICROORGANISMS); EUKARYOTA; MAMMALIA;

EID: 84870392446     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2012.08.003     Document Type: Review

References (50)

1. Harris E.H., Boynton J.E., Gillham N.W. Chloroplast ribosomes and protein synthesis. Microbiol Rev 1994, 58:700-754.
2. O'Brien T.W. Evolution of a protein-rich mitochondrial ribosome: implications for human genetic disease. Gene 2002, 286:73-79.
3. Margulis L. Origin of Eukaryotic Cells 1970, Yale University Press, New Haven.
4. Gray M.W., Burger G., Lang B.F. The origin and early evolution of mitochondria. Genome Biol 2001, 2:1018.1-10185.
5. Schuwirth B.S., Borovinskaya M.A., Hau C.W., Zhang W., Vila-Sanjurjo A., Holton J.M., Cate J.H. Structures of the bacterial ribosome at 3.5Å resolution. Science 2005, 310:827-834.
6. Selmer M., Dunham C.M., Murphy F.V., Weixlbaumer A., Petry S., Kelley A.C., Weir J.R., Ramakrishnan V. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 2006, 313:1935-1942.
7. Ben-Shem A., Garreau de Loubresse N., Mekinikov S., Jenner L., Yusupova G., Yusupov M. The structure of the eukaryotic ribosome at 3.0Å resolution. Science 2011, 334:1524-1529.
8. Klinge S., Voigts-Hoffmann F., Leibundgut M., Arpagaus S., Ban N. Crystal structure of the eukaryotic 60S ribosomal subunit in complex with initiation factor 6. Science 2011, 334:941-948.
9. Sharma M.R., Wilson D.N., Datta P.P., Barat C., Schluenzen F., Fucini P., Agrawal R.K. Cryo-EM study of the spinach chloroplast ribosome reveals the structural and functional roles of plastid-specific ribosomal proteins. Proc Natl Acad Sci USA 2007, 104:19315-19320.
10. Manuell A.L., Quispe J., Mayfield S.P. Structure of the chloroplast ribosome: novel domains for translation regulation. PLoS Biol 2007, 5:e209. 10.1371/journal.pbio.0050209.
11. Schmeing T.M., Ramakrishnan V. What recent ribosome structures have revealed about the mechanism of translation. Nature 2009, 461:1234-1242.
12. Klinge S., Voigts-Hoffmann F., Leibundgut M., Ban N. Atomic structures of eukaryotic ribosomes. Trends Biochem Sci 2012, 37:189-198.
13. Melnikov S., Ben-Shem A., Garreau de Loubresse N., Jenner L., Yusupova G., Yusupov M. One core, two shells: bacterial and eukaryotic ribosomes. Nat Struct Mol Biol 2012, 19:560-567.
14. Sharma M.R., Koc E.C., Datta P.P., Booth T.M., Spremulli L.L., Agrawal R.K. Structure of the mammalian mitochondrial ribosomes reveals an expanded role for its component proteins. Cell 2003, 115:97-108.
15. Sharma M.R., Booth T.M., Simpson L., Maslov D.A., Agrawal R.K. Structure of a mitochondrial ribosome with minimal RNA. Proc Natl Acad Sci USA 2009, 106:9637-9642.
16. Agrawal R.K., Sharma M.R., Yassin A., Lahiri I., Spremulli L.L. Structure and function of organellar ribosomes as revealed by cryo-EM. Ribosomes: Structure, Function, and Dynamics 2011, 83-96. SpringerWien, New York. M. Rodnina, W. Wintermeyer, R. Green (Eds.).
17. Herrmann JM, Woellhaf MW, Bonnefoy N: Control of protein synthesis in yeast mitochondria: the concept of translational activators. Biochim Biophys Acta 2012, in press. doi:10.1016/j.bbamcr.2012.03.007.
18. Jia L., Kaur J., Stuart R.A. Mapping of the Saccharomyces cerevisiae Oxa1-mitochondrial ribosome interface and identification of MrpL40, a ribosomal protein in close proximity to Oxa1 and critical for oxidative phosphorylation complex assembly. Eukaryot Cell 2009, 8:1792-1802.
19. Gruschke S., Ott M. The polypeptide tunnel exit of the mitochondrial ribosome is tailored to meet the specific requirements of the organelle. Bioessays 2010, 32:1050-1057.
20. Koc E.C., Haque M.E., Spremulli L.L. Current views of the structure of the mammalian mitochondrial ribosome. Israel J Chem 2010, 50:45-59.
21. Zíková A., Panigrahi A.K., Dalley R.A., Acestor N., Anupama A., Ogata Y., Myler P.J., Stuart K.D. Trypanosoma brucei mitochondrial ribosomes: affinity purification and component identification by mass spectrometry. Mol Cell Proteomics 2008, 7:1286-1296.
22. Ogle J.M., Broderson D.E., Clemons W.M., Tarry M.J., Carter A.P., Ramakrishnan V. Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 2001, 292:897-902.
23. Ban N., Nissen P., Hansen J., Moore P.B., Steitz T.A. The complete atomic structure of the large ribosomal subunit at 2.4Å resolution. Science 2000, 289:905-920.
24. Yusupov M.M., Yusupova G.Z., Baucom A., Lieberman K., Earnest T.N., Cate J.H., Noller H.F. Crystal structure of the ribosome at 5.5Å resolution. Science 2001, 292:883-896.
25. Mears J.A., Cannone J.J., Stagg S.M., Gutell R.R., Agrawal R.K., Harvey S.C. Modeling a minimal ribosome based on comparative sequence analysis. J Mol Biol 2002, 321:215-234.
26. Mears J.A., Sharma M.R., Gutell R.R., McCook A.S., Richardson P.E., Caulfield T.R., Agrawal R.K., Harvey S.C. A structural model for the large subunit of the mammalian mitochondrial ribosome. J Mol Biol 2006, 358:193-212.
27. Agrawal R.K., Spahn C.M., Penczek P., Grassucci R.A., Nierhaus K.H., Frank J. Visualization of tRNA movements on the Escherichia coli 70S ribosome during the elongation cycle. J Cell Biol 2000, 150:447-460.
28. Temperley R.J., Wydro M., Lightowlers R.N., Chrzanowska-Lightowlers Z.M. Human mitochondrial mRNAs-like members of all families, similar but different. Biochim Biophys Acta 2010, 1797:1081-1085.
29. Smirnov A., Entelis N., Martin R.P., Tarassov I. Biological significance of 5S rRNA import into human mitochondria: role of ribosomal protein MRP-L18. Genes Dev 2011, 25:1289-1305.
30. Watanabe K. Unique features of animal mitochondrial translation systems: the non-universal genetic code, unusual features of the translational apparatus and their relevance to human diseases. Proc Jpn Acad Ser B 2010, 86:11-39. 10.2183/pjab.86.11.
31. Koc E.C., Spremulli L.L. Identification of mammalian mitochondrial translational initiation factor 3 and examination of its role in initiation complex formation with natural mRNAs. J Biol Chem 2002, 277:35541-35549.
32. Spremulli L.L., Coursey A., Navratil T., Hunter S.E. Initiation and elongation factors in mammalian mitochondrial protein biosynthesis. Prog Nucleic Acid Res Mol Biol 2004, 77:211-261.
33. Christian B.E., Spremulli L.L. Mechanism of protein synthesis in mammalian mitochondria. Biochim Biophys Acta 2012, 1819:1035-1054.
34. Spencer A.C., Spremulli L.L. The interaction of mitochondrial translational initiation factor 2 with the small ribosomal subunit. Biochim Biophys Acta 2005, 1750:69-81.
35. Yassin A.S., Haque M.E., Datta P.P., Elmore K., Banavali N.K., Spremulli L.L., Agrawal R.K. Insertion domain within mammalian mitochondrial translation initiation factor 2 serves the role of eubacterial initiation factor 1. Proc Natl Acad Sci USA 2011, 108:3918-3923.
36. Simonetti A., Marzid S., Jenner L., Myasnikov A., Romby P., Yusopova G., Gualerzi C.O., Klaholz B.P., Yusupov M. A structural view of translation initiation in bacteria. Cell Mol Life Sci 2009, 66:423-436.
37. Carter A.P., Clemons W.M., Brodersen D.E., Morgan-Warren R.J., Hartsch T., Wimberly B.T., Ramakrishnan V. Crystal structure of an initiation factor bound to the 30S ribosomal subunit. Science 2001, 291:498-501.
38. Gaur R., Grasso D., Datta P.P., Krishna P.D., Das G., Spencer A., Agrawal R.K., Spremulli L., Varshney U. A single mammalian mitochondrial translation initiation factor functionally replaces two bacterial factors. Mol Cell 2008, 29:180-190.
39. Yassin A.S., Agrawal R.K., Banavali N.K. Computational exploration of structural hypotheses for an additional sequence in a mammalian mitochondrial protein. PLoS ONE 2011, 6:e21871. 10.1371/journal.pone.0021871.
40. Rawat U.B., Zavialov A.V., Sengupta J., Valle M., Grassucci R.A., Linde J., Vestergaard B., Ehrenberg M., Frank J. A cryo-electron microscopic study of ribosome-bound termination factor RF2. Nature 2003, 421:87-90.
41. Srere P.A. The infrastructure of the mitochondrial matrix. Trends Biochem 1980, 5:120-121.
42. Nissen P., Hansen J., Ban N., Moore P.B., Steitz T.A. The structural basis of ribosome activity in peptide bond synthesis. Science 2000, 289:920-930.
43. Liu M., Spremulli M.M. Interaction of mammalian mitochondrial ribosomes with the inner membrane. J Biol Chem 2000, 275:29400-29406.
44. Vogel F., Bornhovd C., Neupert W., Reichert A.S. Dynamic subcompartmentalization of the mitochondrial inner membrane. J Cell Biol 2006, 175:237-247.
45. Herrmann J.M., Neupert W., Stuart R.A. Insertion into the mitochondrial inner membrane of a polytopic protein, the nuclear-encoded Oxa1p. EMBO J 1997, 16:2217-2226.
46. Funes S., Kauff F., van der Sluis E.O., Ott M., Herrmann J.M. Evolution of YidC/Oxa1/Alb3 insertases: three independent gene duplications followed by functional specialization in bacteria, mitochondria and chloroplasts. Biol Chem 2011, 392:13-19.
47. Haque M.E., Elmore K.B., Tripathy A., Koc H., Koc E.C., Spremulli L.L. Properties of C-terminal tail of human mitochondrial inner membrane protein Oxa1L and its interactions with mammalian mitochondrial ribosomes. J Biol Chem 2010, 285:28353-28362.
48. Haque M.E., Spremulli L.L., Fecko C.J. Identification of protein-protein and protein-ribosome interacting regions of the C-terminal tail of human mitochondrial inner membrane protein Oxa1L. J Biol Chem 2010, 285:34991-34998.
49. He J., Cooper H.M., Reyes A., Di Re M., Sembongi H., Litwin T.R., Gao J., Neuman K.C., Fearnley I.M., Spinazzola A., et al. Mitochondrial nucleoid interacting proteins support mitochondrial protein synthesis. Nucl Acids Res 2012, 40:6109-6121.
50. Surovtseva Y.V., Shutt T.E., Cotney J., Cimen H., Chen S.Y., Koc E.C., Shadel G.S. Mitochondrial ribosomal protein L12 selectively associates with human mitochondrial RNA polymerase to activate transcription. Proc Natl Acad Sci USA 2011, 108:17921-17926.