HIS & HERS, magic magnesium and the ballet of protein synthesis

Current Opinion in Chemical Biology

Volumn 7, Issue 5, 2003, Pages 528-533

  Parnell, K Mark ^a   Strobel, Scott A ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANION; MAGNESIUM; MESSENGER RNA; PEPTIDYLTRANSFERASE; PROTEIN; RIBOSOME RNA; RIBOZYME; RNA; TRANSFER RNA;

CATALYSIS; CHEMICAL REACTION; COMPUTER MODEL; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME SUBSTRATE; MOLECULAR INTERACTION; NONHUMAN; PROTEIN SYNTHESIS; REVIEW; RIBOSOME;

EID: 0142199917     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpa.2003.08.003     Document Type: Review

References (42)

1. Green R., Noller H.F. Ribosomes and translation. Annu. Rev. Biochem. 66:1997;679-716.
2. Monro R.E., Marcker K.A. Ribosome-catalysed reaction of puromycin with a formylmethionine-containing oligonucleotide. J. Mol. Biol. 25:1967;347-350.
3. Maden B.E.H., Traut R.R., Monro R.E. Ribosome-catalyzed peptidyl transfer: the polyphenylalanine system. J. Mol. Biol. 35:1968;335-345.
4. Wagner T., Cramer F., Sprinzl M. Activity of the 2′ and 3′ isomers of aminoacyl transfer ribonucleic acid in the in vitro peptide elongation on Escherichia coli ribosomes. Biochemistry. 21:1982;1521-1529.
5. Bhuta A., Quiggle K., Ott T., Ringer D., Chladek S. Stereochemical control of ribosomal peptidyltransferase reaction. Role of amino acid side-chain orientation of acceptor substrate. Biochemistry. 20:1981;8-15.
6. Nierhaus K.H., Schulze H., Cooperman B.S. Molecular mechanisms of the ribosomal peptidyltransferase center. Biochem. Int. 1:1980;185-192.
7. Samaha R.R., Green R., Noller H.F. A base pair between tRNA and 23S rRNA in the peptidyl transferase centre of the ribosome. Nature. 377:1995;309-314.
8. Kim D.F., Green R. Base-pairing between 23S rRNA and tRNA in the ribosomal A site. Mol. Cell. 4:1999;859-864.
9. Nissen P., Hansen J., Ban N., Moore P.B., Steitz T.A. The structural basis of ribosome activity in peptide bond synthesis. Science. 289:2000;920-930.
10. Ban N., Nissen P., Hansen J., Moore P.B., Steitz T.A. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science. 289:2000;905-920.
11. Nissen P., Ippolito J.A., Ban N., Moore P.B., Steitz T.A. RNA tertiary interactions in the large ribosomal subunit: the A-minor motif. Proc. Natl. Acad. Sci. U.S.A. 98:2001;4899-4903 The A-minor motif, in which the minor grooves of adenine bases interact with the minor groove of neighboring helices, is reported to be an important structural motif in the ribosome. It is involved in the placement of the 3′-terminal A76 of both A-site and P-site tRNAs.
12. Schmeing T.M., Seila A.C., Hansen J.L., Freeborn B., Soukup J.K., Scaringe S.A., Strobel S.A., Moore P.B., Steitz T.A. A pre-translocational intermediate in protein synthesis observed in crystals of enzymatically active 50S subunits. Nat. Struct. Biol. 9:2002;225-230 The observation of product formation within H. marismortui 50S subunit crystals provides evidence that the crystals are active. The product, formed in a novel 'no methanol' fragment assay, is bound to the A-site, which provides evidence for a pre-translocational intermediate.
13. Hansen J.L., Schmeing T.M., Moore P.B., Steitz T.A. Structural insights into peptide bond formation. Proc. Natl. Acad. Sci. U.S.A. 99:2002;11670-11675 An in silico model including both A- and P-site substrates, based upon the binding of each substrate individually, makes important predictions about the positioning of reactants. Additionally, the authors propose a transition state based on the trajectory formed between the substrate and product structures.
14. Bashan A., Agmon I., Zarivach R., Schluenzen F., Harms J., Berislo R., Bartels H., Franceschi F., Auerbach T., Hansen H.A.S.et al. Structural basis of the ribosomal machinery for peptide bond formation, translocation, and nascent chain progression. Mol. Cell. 11:2003;91-102.
15. Harms J., Schluenzen F., Zarivach R., Bashan A., Gat S., Agmon I., Bartels H., Franceschi F., Yonath A. High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell. 107:2001;679-688.
16. Chamberlin S.I., Merino E.J., Weeks K.M. Catalysis and amide synthesis by RNA phosphodiester and hydroxyl groups. Proc. Natl. Acad. Sci. U.S.A. 99:2002;14688-14693 Based upon rate constants for model aminolysis reactions, the importance of a neighboring hydroxyl group in amide bond formation is shown. These results are extrapolated to the peptidyl transferase reaction to argue that the ribosomal P-site tRNA A76 2′-OH is involved in positioning and/ or activating the α-amino group for nucleophilic attack.
17. Quiggle K., Kumar G., Ott T.W., Ryu E.K., Chládek S. Donor site of ribosomal peptidyltransferase: investigation of substrate specificity using 2′(3′)-O-(N-acylaminoacyl)dinucleoside phosphates as models of the 3′ terminus of N-acylaminoacyl transfer ribonucleic acid. Biochemistry. 20:1981;3480-3485.
18. Moore P.B., Steitz T.A. After the ribosome structures: how does peptidyl transferase work? RNA. 9:2003;155-159.
19. Polacek N., Gomez M.J., Ito K., Xiong L., Nakamura Y., 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 Mutation of A2602 in the context of reconstituted ribosomes abolishes the ability of ribosomes to release the nascent peptide from the P-site tRNA analog under peptide termination conditions.
20. Tamura K., Schimmel P. Oligonucleotide-directed peptide synthesis in a ribosome- and ribozyme-free system. Proc. Natl. Acad. Sci. U.S.A. 98:2001;1393-1397 Peptide bond formation is shown in a ribosome- and ribozyme-free model system. The reaction relies upon oligonucleotide base pairing interactions, which bring the substrates within close proximity, and upon the addition of imidazole. This suggests the need for a general base in this model reaction.
21. Oyelere AK: Abiotic models for ribosomal polypeptide biosynthesis. Brown University: Providence; 1999.
22. Krayevsky A.A., Kukhanova M.K. The peptidyltransferase center of ribosomes. Prog. Nucl. Acid Res. Mol. Biol. 23:1979;1-51.
23. Polacek N., Gaynor M., Yassin A., Mankin A.S. Ribosomal peptidyl transferase can withstand mutations at the putative catalytic nucleotide. Nature. 411:2001;498-501 In response to the proposal that A2451 acts as a general base in peptide bond formation, this study demonstrated that reconstituted ribosomes with A2451 mutations showed only minor reductions in peptidyl transferase activity.
24. Matthaei J.H., Nirenberg M.W. Characteristics and stabilization of DNAase-sensitive protein synthesis in E. coli extracts. Proc. Natl. Acad. Sci. U.S.A. 47:1961;1580-1588.
25. Maden B.E.H., Monro R.E. Ribosome-catalyzed peptidyl transfer: effects of cations and pH value. Eur. J. Biochem. 6:1968;309-316.
26. Pestka S. Peptidyl-puromycin synthesis on polyribosomes from Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 69:1972;624-628.
27. Welch M., Chastang J., Yarus M. An inhibitor of ribosomal peptidyl transferase using transition-state analogy. Biochemistry. 34:1995;385-390.
28. Gesteland R.F. Unfolding of Escherichia coli ribosomes by removal of magnesium. J. Mol. Biol. 18:1966;356-375.
29. Polacek N., Barta A. Metal ion probing of rRNAs: evidence for evolutionarily conserved divalent cation binding pockets. RNA. 4:1998;1282-1294.
30. Dorner S., Barta A. Probing ribosome structure by europium-induced RNA cleavage. Biol. Chem. 380:1999;243-251.
31. Green R., Lorsch J.R. The path to perdition is paved with protons. Cell. 110:2002;665-668.
32. a in the ribosomal peptidyl transferase center. Science. 289:2000;947-950.
33. Bayfield M.A., Dahlberg A.E., Schulmeister U., Dorner S., Barta A. A conformational change in the ribosomal peptidyl transferase center upon active/inactive transition. Proc. Natl. Acad. Sci. U.S.A. 98:2001;10096-10101 Evidence for a pH-dependent conformational change in the ribosomal active site. A2451, which had been shown earlier to have a pH-dependent dimethyl sulfate modification, was shown to be accessible to dimethyl sulfate only in inactive E. coli ribosomes.
34. Muth G.W., Chen L., Kosek A.B., Strobel S.A. pH-dependent conformational flexibility within the ribosomal peptidyl transferase center. RNA. 7:2001;1403-1415 Evidence for a pH-dependent conformational change in the ribosomal active site based upon chemical footprinting in S. cerevisiae, H. marismortui and E. coli ribosomes. A model is proposed in which the conserved and possibly protonated A2450+C2063 base pair at the active site is responsible for this observation.
35. a of adenine 2451 in the ribosomal peptidyl transferase center remains elusive. RNA. 7:2001;1365-1369.
36. Thompson J., Kim D.F., O'Connor M., Lieberman K.R., Bayfield M.A., Gregory S.T., Green R., Noller H.F., Dahlberg A.E. Analysis of mutations at residues A2451 and G2447 of 23S rRNA in the peptidyl transferase active site of the 50S ribosomal subunit. Proc. Natl. Acad. Sci. U.S.A. 98:2001;9002-9007 Ribosomes containing A2451U mutations are capable of synthesizing full-length protein chains in vitro.
37. Green R., Noller H.F. Reconstitution of functional 50S ribosomes from in vitro transcripts of Bacillus stearothermophilus 23S rRNA. Biochemistry. 38:1999;1772-1779.
38. -1). Unlike previous studies on reactions with slow rates, two ionizable groups affect the kinetic parameters for catalysis. These are the α-amino group of the A-site substrate and an ionizable group on the ribosome, either A2451 or a pH dependent conformational change that affects the ability of A2451 to contribute to catalysis.
39. Wolfenden R. Analog approaches to the structure of the transition state in enzyme reactions. Acc. Chem. Res. 5:1972;10.
40. a-perturbed RNA base in the peptidyl transferase center. Proc. Natl. Acad. Sci. U.S.A. 99:2002;11658-11663 This work explores the possibility that an ionizable group within the ribosome is involved in stabilization of the oxyanion in the transition state. The biochemical results argue against such a stabilization, at least to the extent that CCdApPmn accurately mimics the transition state.
41. Cate J.H., Yusupov M.M., Yusopova G.Z., Earnest T.N., Noller H.F. X-ray crystal structures of 70S ribosomal functional complexes. Science. 285:1999;2095-2104.
42. Berg J.M., Lorsch J.R. Technical comment: mechanism of ribosomal peptide bond formation. Science. 291:2001;203a-204a.