Arrangement of 3′-terminus of tRNA on the human ribosome as revealed from cross-linking data

Biochimie

Volumn 90, Issue 11-12, 2008, Pages 1624-1636

  Bulygin, Konstantin ^a,b   Favre, Alain ^b   Baouz Drahy, Soria ^b   Hountondji, Codjo ^b   Vorobjev, Yury ^a   Ven'yaminova, Aliya ^a   Graifer, Dmitri ^a   Karpova, Galina ^a  

^a INSTITUTE OF CHEMICAL BIOLOGY AND FUNDAMENTAL MEDICINE   (Russian Federation)

^b CNRS   (France)

Author keywords

80S ribosome; Peptidyl transferase center; Photoaffinity cross linking, 28S rRNA; tRNA analogue with 4 thiouridine

Indexed keywords

ADENOSINE; PEPTIDYLTRANSFERASE; THIOURIDINE; TRANSFER RNA; ASPARTIC ACID TRANSFER RNA; MESSENGER RNA; PHENYLALANINE TRANSFER RNA; RNA 23S; RNA 28S;

ARTICLE; CROSS LINKING; MOLECULAR MODEL; PROTEIN DOMAIN; REVERSE TRANSCRIPTION; RIBOSOME; RNA BINDING; RNA STRUCTURE; ULTRAVIOLET IRRADIATION; CHEMISTRY; CONFORMATION; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE;

EUKARYOTA; MAMMALIA; PROKARYOTA;

BASE SEQUENCE; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RIBOSOMES; RNA, MESSENGER; RNA, RIBOSOMAL, 23S; RNA, RIBOSOMAL, 28S; RNA, TRANSFER, ASP; RNA, TRANSFER, PHE;

EID: 55349093582     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2008.06.002     Document Type: Article

References (46)

1. Yusupova G.Zh., Yusupov M.M., Cate J.H.D., and Noller H.F. The path of messenger RNA through the ribosome. Cell 106 (2001) 233-241
2. Baram D., and Yonath A. From peptide-bond formation to cotranslational folding: dynamic, regulatory and evolutionary aspects. FEBS Lett. 579 (2005) 948-954
3. Steitz T.A. On the structural basis of peptide-bond formation and antibiotic resistance from atomic structures of the large ribosomal subunit. FEBS Lett. 579 (2005) 955-958
4. Selmer M., Dunham C.M., Murphy IV F.V., Weixlbaumer A., Petry S., Kelley A.C., Weir J.R., and Ramakrishnan V. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313 (2006) 1935-1942
5. Wilden B., Savelsbergh A., Rodnina M.V., and Wintermeyer W. Role and timing of GTP binding and hydrolysis during EF-G-dependent tRNA translocation on the ribosome. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 13670-13675
6. Noller H.F. Biochemical characterization of the ribosomal decoding site. Biochimie 88 (2006) 935-941
7. Beringer M., and Rodnina M.V. The ribosomal peptidyl transferase. Mol. Cell 26 (2007) 311-321
8. Vladimirov S.N., Babkina G.T., Venijaminova A.G., Gimautdinova O.I., Zenkova M.A., and Karpova G.G. Structural arrangement of the decoding site of Escherichia coli ribosomes as revealed from the data on affinity labelling of ribosomes by analogs of mRNA-derivatives of oligoribonucleotides. Biochim. Biophys. Acta. 1048 (1990) 245-256
9. Graifer D.M., Karpova G.G., and Knorre D.G. Location of template on human ribosome as revealed from data on cross-linking with reactive mRNA analogs. Biochemistry (Moscow) 66 (2001) 585-602 (translated from Biokhimiya 66 725-744)
10. Sergiev P.V., Dontsova O.A., and Bogdanov A.A. Study of ribosome structure using the biochemical methods: judgment day. Mol. Biol. (Moscow) 35 (2001) 559-583
11. Demeshkina N., Repkova M., Ven'yaminova A., Graifer D., and Karpova G. Nucleotides of 18S rRNA surrounding mRNA codons at the human ribosomal A, P and E sites, respectively: a cross-linking study with mRNA analogues carrying aryl azide group at either the uracil or the guanine residue. RNA 6 (2000) 1727-1736
12. Demeshkina N., Laletina E., Meschaninova M., Ven'yaminova A., Graifer D., and Karpova G. Positioning of mRNA codons with respect to 18S rRNA at the P and E sites of human ribosome. Biochim. Biophys. Acta. 1627 (2003) 39-46
13. Graifer D., Molotkov M., Styazhkina V., Demeshkina N., Bulygin K., Eremina A., Ivanov A., Laletina E., Ven'yaminova A., and Karpova G. Variable and conserved elements of human ribosomes surrounding the mRNA at the decoding and upstream sites. Nucleic Acids Res. 32 (2004) 3282-3293
14. Molotkov M., Graifer D., Demeshkina N., Repkova M., Ven'yaminova A., and Karpova G. Arrangement of mRNA 3′ of the A site codon on the human 80S ribosome. RNA Biol. 2 (2005) 63-69
15. Molotkov M.V., Graifer D.M., Popugaeva E.A., Bulygin K.N., Meschaninova M.I., Ven'yaminova A.G., and Karpova G.G. mRNA 3′ of the A site bound codon is located close to protein S3 on the human 80S ribosome. RNA Biol. 3 (2006) 122-129
16. Graifer D.M., Juzumiene D.I., Karpova G.G., and Wollenzien P. mRNA binding track in the human 80S ribosome for mRNA analogues randomly substituted with 4-thiouridine residues. Biochemistry 33 (1994) 6201-6206
17. Graifer D.M., Juzumiene D.I., Wollenzien P., and Karpova G.G. Cross-linking of mRNA analogues containing 4-thiouridine residues on the 3′- or 5′-side of the coding triplet to the mRNA binding center of the human ribosome. Biochemistry 33 (1994) 3878-3884
18. Bulygin K., Chavatte L., Frolova L., Karpova G., and Favre A. The first position of a codon placed in the A site of the human 80S ribosome contacts nucleotide C1696 of the 18S rRNA as well as proteins S2, S3, S3a, S30 and S15. Biochemistry 44 (2005) 2153-2162
19. Favre A. 4-Thiouridine as an intrinsic photoaffinity probe of nucleic acid structure and interactions. In: Morrison D. (Ed). Bioorganic Photochemistry: Photochemistry and the Nucleic Acids (1990), Wiley, New York 379-425
20. Favre A., and Fourrey J.-L. Structural probing of small endonucleolytic ribozymes in solution using thio-substituted nucleobases as intrinsic photolabels. Acc. Chem. Res. 28 (1995) 375-382
21. Phe nucleotides contacting the subunits of Thermus thermophilus phenylalanyl-tRNA synthetase by photoaffinity crosslinking. Biochim. Biophys. Acta. 1518 (2001) 226-236
22. 4UGA stop codon located in the A site of eukaryotic ribosomes. Eur. J. Biochem. 268 (2001) 2896-2904
23. Chavatte L., Seit-Nebi A., Dubovaya V., and Favre A. The invariant uridine of stop codons contacts the conserved NIKSR loop of human eRF1 in the ribosome. EMBO J. 21 (2002) 5302-5311
24. Chavatte L., Frolova L.Y., Laugaa P., Kisselev L.L., and Favre A. Stop codons and UGG promote efficient binding of the polypeptide release factor eRF1 to the ribosomal A site. J. Mol. Biol. 331 (2003) 745-758
25. Matasova N.B., Myltseva S.V., Zenkova M.A., Graifer D.M., Vladimirov S.N., and Karpova G.G. Isolation of ribosomal subunits containing intact rRNA from human placenta. Estimation of functional activity of 80S ribosomes. Anal. Biochem. 198 (1991) 219-223
26. Ven'yaminova A.G., Gorn V.V., Zenkova M.A., Komarova N.I., and Repkova M.N. An automated H-phosphonate method for synthesis of oligoribonucleotides with the use of 2′-O-tetrahydropyranyl protecting group. Bioorgan. Khim. (Moscow) 16 (1990) 941-950
27. Moor N., Lavrik O., Favre A., and Safro M. Prokaryotic and eukaryotic tetrameric phenylalanyl-tRNA synthetases display conservation of the binding mode of the tRNA(Phe) CCA end. Biochemistry 42 (2003) 10697-10708
28. 3. Mol. Biol. (Moscow) 31 (1997) 120-126 (translated from Molekularnaya Biologiya)
29. Malygin A.A., Graifer D.M., Bulygin K.N., Zenkova M.A., Yamkovoy V.I., Stahl J., and Karpova G.G. Arrangement of mRNA at the decoding site of human ribosomes. 18S rRNA nucleotides and ribosomal proteins cross-linked to oligouridylate derivatives with alkylating groups at either the 3′ or the 5′ termini. Eur. J. Biochem. 226 (1994) 715-723
30. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of the bacterophage T4. Nature 227 (1970) 680-685
31. Graifer D.M., Malygin A.A., Matasova N.B., Mundus D.A., Zenkova M.A., and Karpova G.G. Studying functional significance of the sequence 980-1061 in the central domain of human 18S rRNA using complementary DNA probes. Biochim. Biophys. Acta. 1350 (1997) 335-344
32. Wollenzien P. Isolation and identification of RNA cross-links. Methods Enzymol. 164 (1988) 319-329
33. Bashan A., Agmon I., Zarivach R., Schluenzen F., Harms J., Berisio R., Bartels H., Franceschi F., Auerbach T., Hansen H.A., Kossoy E., Kessler M., and Yonath A. Structural basis of the ribosomal machinery for peptide bond formation, translocation, and nascent chain progression. Mol. Cell 11 (2003) 91-102
34. Vorobjev Yu.N. Study of the Mechanism of Interaction of Oligonucleotides with the 3′-Terminal Region of tRNA-Phe by Computer Modeling. Mol. Biol. (Moscow) 39 (2005) 777-784 (translated from Molekulyarnaya Biologiya 39 887-895)
35. Phe with human 80S ribosomes in the presence of oligo- and polyurydilate template. Biochim. Biophys. Acta. 1171 (1992) 56-64
36. Nissen P., Hansen J., Ban N., Moore P.B., and Steitz T.A. The structural basis of ribosome activity in peptide bond synthesis. Science 289 (2000) 920-930
37. Bocchetta M., Xiong L., and Mankin A.S. 23S rRNA positions essential for tRNA binding in ribosomal functional sites. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 3525-3530
38. Moazed D., and Noller H.F. Sites of interaction of the CCA end of peptidyl-tRNA with 23S rRNA. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 3725-3728
39. Yusupov M.M., Yusupova G.Zh., Albion Baucom A., Lieberman K., Earnest T.N., Cate J.H.D., and Noller H.F. Crystal structure of the ribosome at 5.5 Å resolution. Science 292 (2001) 883-896
40. O'Connor M., and Dahlberg A.E. Mutations at U2555, a tRNA-protected base in 23S rRNA, affect translational fidelity. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 9214-9218
41. Kim D.F., and Green R. Base-Pairing between 23S rRNA and tRNA in the Ribosomal A Site. Mol. Cell 4 (1999) 859-864
42. Steiner G., Kuechler E., and Barta A. Photo-affinity labelling at the peptidyl transferase centre reveals two different positions for the A- and P-sites in domain V of 23S rRNA. EMBO J. 7 (1988) 3949-3955
43. Rodriguez-Fonseca C., Phan H., Long K.S., Porse B.T., Kirillov S.V., Amils R., and Garrett R.A. Puromycin-rRNA interaction sites at the peptidyl transferase center. RNA 6 (2000) 744-754
44. Gindulyte A., Bashan A., Agmon I., Massa L., Yonath A., and Karle J. The transition state for formation of the peptide bond in the ribosome. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 13327-13332
45. Manuilov A.V., Hixson S.S., and Zimmermann R.A. New photoreactive tRNA derivatives for probing the peptidyl transferase center of the ribosome. RNA 13 (2007) 793-800
46. Dresios J., Panopoulos P., and Synetos D. Eukaryotic ribosomal proteins lacking a eubacterial counterpart: important players in ribosomal function. Mol. Microbiol. 59 (2006) 1651-1663