Two Distinct Components of Release Factor Function Uncovered by Nucleophile Partitioning Analysis

Molecular Cell

Volumn 28, Issue 3, 2007, Pages 458-467

  Shaw, Jeffrey J ^a   Green, Rachel ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

RNA

Indexed keywords

TRANSFER RNA;

AMINO ACID ANALYSIS; ARTICLE; CATALYSIS; PROTEIN SECRETION; STEADY STATE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ESCHERICHIA COLI PROTEINS; HYDROLYSIS; KINETICS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PEPTIDE CHAIN TERMINATION, TRANSLATIONAL; PEPTIDE TERMINATION FACTORS; PROTEIN STRUCTURE, TERTIARY; RIBOSOMES; SEQUENCE ALIGNMENT; WATER;

EID: 35648950403     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.09.007     Document Type: Article

References (38)

1. Beringer M., and Rodnina M.V. Importance of tRNA interactions with 23S rRNA for peptide bond formation on the ribosome: studies with substrate analogs. Biol. Chem. 388 (2007) 687-691
2. Beringer M., and Rodnina M.V. The ribosomal peptidyl transferase. Mol. Cell 26 (2007) 311-321
3. Brunelle J.L., Youngman E.M., Sharma D., and Green R. The interaction between C75 of tRNA and the A loop of the ribosome stimulates peptidyl transferase activity. RNA 12 (2006) 33-39
4. Caskey C.T., Beaudet A.L., Scolnick E.M., and Rosman M. Hydrolysis of fMet-tRNA by peptidyl transferase. Proc. Natl. Acad. Sci. USA 68 (1971) 3163-3167
5. Das G.K., Bhattacharyya D., and Burma D.P. A possible mechanism of peptide bond formation on ribosome without mediation of peptidyl transferase. J. Theor. Biol. 200 (1999) 193-205
6. Dincbas-Renqvist V., Engstrom A., Mora L., Heurgue-Hamard V., Buckingham R., and Ehrenberg M. A post-translational modification in the GGQ motif of RF2 from Escherichia coli stimulates termination of translation. EMBO J. 19 (2000) 6900-6907
7. Dorner S., Panuschka C., Schmid W., and Barta A. Mononucleotide derivatives as ribosomal P-site substrates reveal an important contribution of the 2′-OH to activity. Nucleic Acids Res. 31 (2003) 6536-6542
8. Edwards J., and Pearson R. The factors determining nucleophilic reactivities. J. Am. Chem. Soc. 84 (1962) 16-24
9. Frolova L.Y., Tsivkovskii R.Y., Sivolobova G.F., Oparina N.Y., Serpinsky O.I., Blinov V.M., Tatkov S.I., and Kisselev L.L. Mutations in the highly conserved GGQ motif of class 1 polypeptide release factors abolish ability of human eRF1 to trigger peptidyl-tRNA hydrolysis. RNA 5 (1999) 1014-1020
10. Heurgue-Hamard V., Champ S., Mora L., Merkulova-Rainon T., Kisselev L.L., and Buckingham R.H. The glutamine residue of the conserved GGQ motif in Saccharomyces cerevisiae release factor eRF1 is methylated by the product of the YDR140w gene. J. Biol. Chem. 280 (2005) 2439-2445
11. Jencks W., and Carriuolo J. Reactivity of nucleophilic reagents toward esters. J. Am. Chem. Soc. 82 (1960) 1778-1786
12. Kim D.F., and Green R. Base-pairing between 23S rRNA and tRNA in the ribosomal A site. Mol. Cell 4 (1999) 859-864
13. Lieberman K.R., and Dahlberg A.E. Ribosome-catalyzed peptide-bond formation. Prog. Nucleic Acid Res. Mol. Biol. 50 (1995) 1-23
14. Ma B., and Nussinov R. Release factors eRF1 and RF2: a universal mechanism controls the large conformational changes. J. Biol. Chem. 279 (2004) 53875-53885
15. McCaughan K.K., Poole E.S., Pel H.J., Mansell J.B., Mannering S.A., and Tate W.P. Efficient in vitro translational termination in Escherichia coli is constrained by the orientations of the release factor, stop signal and peptidyl-tRNA within the termination complex. Biol. Chem. 379 (1998) 857-866
16. Mora L., Heurgue-Hamard V., Champ S., Ehrenberg M., Kisselev L.L., and Buckingham R.H. The essential role of the invariant GGQ motif in the function and stability in vivo of bacterial release factors RF1 and RF2. Mol. Microbiol. 47 (2003) 267-275
17. Nakahigashi K., Kubo N., Narita S., Shimaoka T., Goto S., Oshima T., Mori H., Maeda M., Wada C., and Inokuchi H. HemK, a class of protein methyl transferase with similarity to DNA methyl transferases, methylates polypeptide chain release factors, and hemK knockout induces defects in translational termination. Proc. Natl. Acad. Sci. USA 99 (2002) 1473-1478
18. Petry S., Brodersen D.E., Murphy IV F.V., Dunham C.M., Selmer M., Tarry M.J., Kelley A.C., and Ramakrishnan V. Crystal structures of the ribosome in complex with release factors RF1 and RF2 bound to a cognate stop codon. Cell 123 (2005) 1255-1266
19. Polacek N., Gomez M.J., Ito K., Xiong L., Nakamura Y., and Mankin A. The critical role of the universally conserved A2602 of 23S ribosomal RNA in the release of the nascent peptide during translation termination. Mol. Cell 11 (2003) 103-112
20. Rawat U.B., Zavialov A.V., Sengupta J., Valle M., Grassucci R.A., Linde J., Vestergaard B., Ehrenberg M., and Frank J. A cryo-electron microscopic study of ribosome-bound termination factor RF2. Nature 421 (2003) 87-90
21. Rawat U., Gao H., Zavialov A., Gursky R., Ehrenberg M., and Frank J. Interactions of the release factor RF1 with the ribosome as revealed by cryo-EM. J. Mol. Biol. 357 (2006) 1144-1153
22. Robinson R., and Bower V. The ionization constant of hydroxylamine. J. Phys. Chem. 65 (1961) 1279-1280
23. Scarlett D.J., McCaughan K.K., Wilson D.N., and Tate W.P. Mapping functionally important motifs SPF and GGQ of the decoding release factor RF2 to the Escherichia coli ribosome by hydroxyl radical footprinting. Implications for macromolecular mimicry and structural changes in RF2. J. Biol. Chem. 278 (2003) 15095-15104
24. Schmeing T.M., Huang K.S., Kitchen D.E., Strobel S.A., and Steitz T.A. Structural insights into the roles of water and the 2′ hydroxyl of the P site tRNA in the peptidyl transferase reaction. Mol. Cell 20 (2005) 437-448
25. Schmeing T.M., Huang K.S., Strobel S.A., and Steitz T.A. An induced-fit mechanism to promote peptide bond formation and exclude hydrolysis of peptidyl-tRNA. Nature 438 (2005) 520-524
26. Seit-Nebi A., Frolova L., Justesen J., and Kisselev L. Class-1 translation termination factors: invariant GGQ minidomain is essential for release activity and ribosome binding but not for stop codon recognition. Nucleic Acids Res. 29 (2001) 3982-3987
27. Shin D.H., Brandsen J., Jancarik J., Yokota H., Kim R., and Kim S.H. Structural analyses of peptide release factor 1 from Thermotoga maritima reveal domain flexibility required for its interaction with the ribosome. J. Mol. Biol. 341 (2004) 227-239
28. Song H., Mugnier P., Das A.K., Webb H.M., Evans D.R., Tuite M.F., Hemmings B.A., and Barford D. The crystal structure of human eukaryotic release factor eRF1-mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell 100 (2000) 311-321
29. Trobro S., and Aqvist J. Mechanism of peptide bond synthesis on the ribosome. Proc. Natl. Acad. Sci. USA 102 (2005) 12395-12400
30. Trobro S., and Aqvist J. A model for how ribosomal release factors induce peptidyl-tRNA cleavage in termination of protein synthesis. Mol. Cell 27 (2007) 758-766
31. Vestergaard B., Van L.B., Andersen G.R., Nyborg J., Buckingham R.H., and Kjeldgaard M. Bacterial polypeptide release factor RF2 is structurally distinct from eukaryotic eRF1. Mol. Cell 8 (2001) 1375-1382
32. Vestergaard B., Sanyal S., Roessle M., Mora L., Buckingham R.H., Kastrup J.S., Gajhede M., Svergun D.I., and Ehrenberg M. The SAXS solution structure of RF1 differs from its crystal structure and is similar to its ribosome bound cryo-EM structure. Mol. Cell 20 (2005) 929-938
33. Weinger J.S., Parnell K.M., Dorner S., Green R., and Strobel S.A. Substrate-assisted catalysis of peptide bond formation by the ribosome. Nat. Struct. Mol. Biol. 11 (2004) 1101-1106
34. Wilson K.S., Ito K., Noller H.F., and Nakamura Y. Functional sites of interaction between release factor RF1 and the ribosome. Nat. Struct. Biol. 7 (2000) 866-870
35. Youngman E.M., and Green R. Affinity purification of in vivo-assembled ribosomes for in vitro biochemical analysis. Methods 36 (2005) 305-312
36. Youngman E.M., Brunelle J.L., Kochaniak A.B., and Green R. The active site of the ribosome is composed of two layers of conserved nucleotides with distinct roles in peptide bond formation and peptide release. Cell 117 (2004) 589-599
37. Zavialov A.V., Mora L., Buckingham R.H., and Ehrenberg M. Release of peptide promoted by the GGQ motif of class 1 release factors regulates the GTPase activity of RF3. Mol. Cell 10 (2002) 789-798
38. Zoldak G., Redecke L., Svergun D.I., Konarev P.V., Voertler C.S., Dobbek H., Sedlak E., and Sprinzl M. Release factors 2 from Escherichia coli and Thermus thermophilus: structural, spectroscopic and microcalorimetric studies. Nucleic Acids Res. 35 (2007) 1343-1353