The chemistry of protein synthesis and voyage through the ribosomal tunnel

Current Opinion in Structural Biology

Volumn 13, Issue 2, 2003, Pages 212-219

  Jenni, Simon ^a   Ban, Nenad ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MACROLIDE; PEPTIDYLTRANSFERASE; POLYPEPTIDE; RIBOSOME PROTEIN; RIBOZYME; RNA 23S;

AMINO ACID SEQUENCE; BINDING AFFINITY; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME SUBSTRATE; MUTATION; NONHUMAN; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTEIN TARGETING; REACTION ANALYSIS; REVIEW; RIBOSOME SUBUNIT;

EID: 0037399205     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(03)00034-4     Document Type: Review

References (51)

1. Ramakrishnan V., Moore P.B. Atomic structures at last: the ribosome in 2000. Curr. Opin. Struct. Biol. 11:2001;144-154.
2. Wimberly B.T., Brodersen D.E., Clemons W.M. Jr., Morgan-Warren R.J., Carter A.P., Vonrhein C., Hartsch T., Ramakrishnan V. Structure of the 30S ribosomal subunit. Nature. 407:2000;327-339.
3. Schluenzen F., Tocilj A., Zarivach R., Harms J., Gluehmann M., Janell D., Bashan A., Bartels H., Agmon I., Franceschi F.et al. Structure of functionally activated small ribosomal subunit at 3.3 angstroms resolution. Cell. 102:2000;615-623.
4. Ban N., Nissen P., Hansen J., Moore P.B., Steitz T.A. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science. 289:2000;905-920.
5. 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.
6. 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 5.5 Å resolution. Science. 292:2001;883-896.
7. Valle M., Sengupta J., Swami N.K., Grassucci R.A., Burkhardt N., Nierhaus K.H., Agrawal R.K., Frank J. Cryo-EM reveals an active role for aminoacyl-tRNA in the accommodation process. EMBO J. 21:2002;3557-3567.
8. Stark H., Rodnina M.V., Wieden H.J., Zemlin F., Wintermeyer W., van Heel M. Ribosome interactions of aminoacyl-tRNA and elongation factor Tu in the codon-recognition complex. Nat. Struct. Biol. 9:2002;849-854.
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. 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.
11. Hansen J.L., Schmeing T.M., Moore P.B., Steitz T.A. Structural insights into peptide bond formation. Proc. Natl. Acad. Sci. USA. 99:2002;11670-11675 This paper presents a model for peptide bond formation based on the high-resolution structures of peptidyl transferase substrate, intermediate and product analogs in complex with the large ribosomal subunit.
12. Bashan A., Agmon I., Zarivach R., Schluenzen F., Harms J., Berisio R., Bartels H., Franceschi F., Auerbach T., Hansen H.A.et al. Structural basis of the ribosomal machinery for peptide bond formation, translocation, and nascent chain progression. Mol. Cell. 11:2003;91-102.
13. Green R., Noller H.F. Ribosomes and translation. Annu. Rev. Biochem. 66:1997;679-716.
14. Welch M., Chastang J., Yarus M. An inhibitor of ribosomal peptidyl transferase using transition-state analogy. Biochemistry. 34:1995;385-390.
15. DeRose V.J. Two decades of RNA catalysis. Chem. Biol. 9:2002;961-969.
16. Parnell K.M., Seila A.C., Strobel S.A. Evidence against stabilization of the transition state oxyanion by a pKa-perturbed RNA base in the peptidyl transferase center. Proc. Natl. Acad. Sci. USA. 99:2002;11658-11663.
17. Neet K.E. Enzyme catalytic power minireview series. J. Biol. Chem. 273:1998;25527-25528.
18. Cleland W.W., Frey P.A., Gerlt J.A. The low barrier hydrogen bond in enzymatic catalysis. J. Biol. Chem. 273:1998;25529-25532.
19. Cannon W.R., Benkovic S.J. Solvation, reorganization energy, and biological catalysis. J. Biol. Chem. 273:1998;26257-26260.
20. Suarez D., Merz K.M. Jr. Quantum chemical study of ester aminolysis catalyzed by a single adenine: a reference reaction for the ribosomal peptide synthesis. J. Am. Chem. Soc. 123:2001;7687-7690 A quantum mechanical treatment of the peptidyl transferase reaction is presented. The reactants are arranged as observed in structural studies and the catalytic effect of an adenine base is presented.
21. Muth G.W., Ortoleva-Donnelly L., Strobel S.A. A single adenosine with a neutral pKa in the ribosomal peptidyl transferase center. Science. 289:2000;947-950.
22. Xiong L., Polacek N., Sander P., Bottger E.C., Mankin A. pKa of adenine 2451 in the ribosomal peptidyl transferase center remains elusive. RNA. 7:2001;1365-1369.
23. 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.
24. 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. USA. 98:2001;10096-10101.
25. 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 peptidyltransferase active site of the 50S ribosomal subunit. Proc. Natl. Acad. Sci. USA. 98:2001;9002-9007.
26. 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.
27. Braakman I., Hoover-Litty H., Wagner K.R., Helenius A. Folding of influenza hemagglutinin in the endoplasmic reticulum. J. Cell. Biol. 114:1991;401-411.
28. Sorensen M.A., Pedersen S. Absolute in vivo translation rates of individual codons in Escherichia coli. The two glutamic acid codons GAA and GAG are translated with a threefold difference in rate. J. Mol. Biol. 222:1991;265-280.
29. Katunin V.I., Muth G.W., Strobel S.A., Wintermeyer W., Rodnina M.V. Important contribution to catalysis of peptide bond formation by a single ionizing group within the ribosome. Mol. Cell. 10:2002;339-346 The authors directly monitored the chemical step of the peptidyl transferase reaction by quench flow experiments using purified post-translocational ribosomal complexes. The measured reaction rates are comparable to the rate of in vivo protein synthesis. The kinetics reveals a single ionizing group in the catalytic center of the ribosome whose observation depends on the presence of A2451.
30. Tamura K., Schimmel P. Oligonucleotide-directed peptide synthesis in a ribosome- and ribozyme-free system. Proc. Natl. Acad. Sci. USA. 98:2001;1393-1397.
31. Gabashvili I.S., Gregory S.T., Valle M., Grassucci R., Worbs M., Wahl M.C., Dahlberg A.E., Frank J. The polypeptide tunnel system in the ribosome and its gating in erythromycin resistance mutants of L4 and L22. Mol. Cell. 8:2001;181-188.
32. Spahn C.M., Beckmann R., Eswar N., Penczek P.A., Sali A., Blobel G., Frank J. Structure of the 80S ribosome from Saccharomyces cerevisiae-tRNA-ribosome and subunit-subunit interactions. Cell. 107:2001;373-386.
33. Retsema J., Fu W. Macrolides: structures and microbial targets. Int. J. Antimicrob. Agents. 18(suppl 1):2001;S3-S10.
34. Chittum H.S., Champney W.S. Ribosomal protein gene sequence changes in erythromycin-resistant mutants of Escherichia coli. J. Bacteriol. 176:1994;6192-6198.
35. Schlunzen F., Zarivach R., Harms J., Bashan A., Tocilj A., Albrecht R., Yonath A., Franceschi F. Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature. 413:2001;814-821 The first high-resolution structure of the large ribosomal subunit with bound antibiotics. The mode of protein synthesis inhibition through the action of different antibiotics is structurally explained.
36. Hansen J.L., Ippolito J.A., Ban N., Nissen P., Moore P.B., Steitz T.A. The structures of four macrolide antibiotics bound to the large ribosomal subunit. Mol. Cell. 10:2002;117-128 The mode of protein synthesis inhibition by macrolide antibiotics bound to the large ribosomal subunit is crystallographically visualized. The structures explain the correlation between macrolide size and the extent of protein synthesis by the ribosome.
37. Tenson T., Ehrenberg M. Regulatory nascent peptides in the ribosomal tunnel. Cell. 108:2002;591-594.
38. Nakatogawa H., Ito K. Secretion monitor, SecM, undergoes self-translation arrest in the cytosol. Mol. Cell. 7:2001;185-192.
39. Nakatogawa H., Ito K. The ribosomal exit tunnel functions as a discriminating gate. Cell. 108:2002;629-636 A polypeptide sequence motif is identified that stalls translation of the ribosome by interacting with the exit tunnel. A genetic screen allows the isolation of suppressor mutations in rRNA and proteins. The mutations cluster at the inside wall of the tunnel. This study shows that the ribosomal exit tunnel may serve as a discriminating gate.
40. Gong F., Yanofsky C. Instruction of translating ribosome by nascent peptide. Science. 297:2002;1864-1867.
41. Hayes C.S., Bose B., Sauer R.T. Proline residues at the C terminus of nascent chains induce SsrA tagging during translation termination. J. Biol. Chem. 277:2002;33825-33832.
42. Gillet R., Felden B. Emerging views on tmRNA-mediated protein tagging and ribosome rescue. Mol. Microbiol. 42:2001;879-885.
43. Hartl F.U., Hayer-Hartl M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science. 295:2002;1852-1858.
44. Albanese V., Frydman J. Where chaperones and nascent polypeptides meet. Nat. Struct. Biol. 9:2002;716-718.
45. Kramer G., Rauch T., Rist W., Vorderwulbecke S., Patzelt H., Schulze-Specking A., Ban N., Deuerling E., Bukau B. L23 protein functions as a chaperone docking site on the ribosome. Nature. 419:2002;171-174 In this study, the function of ribosomal protein L23 is biochemically and genetically dissected.
46. Keenan R.J., Freymann D.M., Stroud R.M., Walter P. The signal recognition particle. Annu. Rev. Biochem. 70:2001;755-775.
47. Rinke-Appel J., Osswald M., von Knoblauch K., Mueller F., Brimacombe R., Sergiev P., Avdeeva O., Bogdanov A., Dontsova O. Crosslinking of 4.5S RNA to the Escherichia coli ribosome in the presence or absence of the protein Ffh. RNA. 8:2002;612-625.
48. Pool M.R., Stumm J., Fulga T.A., Sinning I., Dobberstein B. Distinct modes of signal recognition particle interaction with the ribosome. Science. 297:2002;1345-1348 The SRP is cross-linked to the ribosome at different functional stages during targeting of RNCs.
49. Beckmann R., Bubeck D., Grassucci R., Penczek P., Verschoor A., Blobel G., Frank J. Alignment of conduits for the nascent polypeptide chain in the ribosome-Sec61 complex. Science. 278:1997;2123-2126.
50. Menetret J.F., Neuhof A., Morgan D.G., Plath K., Radermacher M., Rapoport T.A., Akey C.W. The structure of ribosome-channel complexes engaged in protein translocation. Mol. Cell. 6:2000;1219-1232.
51. Beckmann R., Spahn C.M., Eswar N., Helmers J., Penczek P.A., Sali A., Frank J., Blobel G. Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell. 107:2001;361-372.