The evolving ribosome: from non-coded peptide bond formation to sophisticated translation machinery

Research in Microbiology

Volumn 160, Issue 7, 2009, Pages 487-492

  Davidovich, Chen ^a   Belousoff, Matthew ^a   Bashan, Anat ^a   Yonath, Ada ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Evolution; Peptidyl transferase center; Proto ribosome; Ribosome

Indexed keywords

AMINO ACID; OLIGOMER; PEPTIDE; POLYMER; RIBOSOME RNA; RIBOZYME; RNA POLYMERASE; TRANSFER RNA;

ARTICLE; CATALYSIS; ENZYME SUBSTRATE; GENE DUPLICATION; GENETIC CONSERVATION; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; MUTAGENESIS; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN QUATERNARY STRUCTURE; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; RIBOSOME; RIBOSOME SUBUNIT; RNA CONFORMATION; RNA SEQUENCE; RNA STABILITY; RNA STRUCTURE; RNA SYNTHESIS; RNA TRANSLATION;

EVOLUTION; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PEPTIDES; PROTEIN BIOSYNTHESIS; RIBOSOMES;

EID: 70349988824     PISSN: 09232508     EISSN: 17697123     Source Type: Journal    
DOI: 10.1016/j.resmic.2009.07.004     Document Type: Article

References (65)

1. Agmon I., Bashan A., Zarivach R., and Yonath A. Symmetry at the active site of the ribosome: structural and functional implications. Biol. Chem. 386 (2005) 833-844
2. Agmon I., Bashan A., and Yonath A. On ribosome conservation and evolution. Isr. J. Ecol. Evol. 52 (2006) 359-379
3. Agmon I., Davidovich C., Bashan A., and Yonath A. Identification of the prebiotic translation apparatus within the contemporary ribosome (2009). http://precedings.nature.com/documents/2921/
4. Anderson R.M., Kwon M., and Strobel S.A. Toward ribosomal RNA catalytic activity in the absence of protein. J. Mol. Evol. 64 (2007) 472-483
5. Ban N., Nissen P., Hansen J., Moore P.B., and Steitz T.A. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 289 (2000) 905-920
6. Bashan A., Agmon I., Zarivach R., Schluenzen F., Harms J., Berisio R., Bartels H., Franceschi F., Auerbach T., Hansen H.A.S., 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
7. Bashan A., and Yonath A. Correlating ribosome function with high-resolution structures. Trends Microbiol. 16 (2008) 326-335
8. Bieling P., Beringer M., Adio S., and Rodnina M.V. Peptide bond formation does not involve acid-base catalysis by ribosomal residues. Nat. Struct. Mol. Biol. 13 (2006) 424-428
9. Bokov K., and Steinberg S.V. A hierarchical model for evolution of 23S ribosomal RNA. Nature 457 (2009) 977-980
10. Davis J.H., Tonelli M., Scott L.G., Jaeger L., Williamson J.R., and Butcher S.E. RNA helical packing in solution: NMR structure of a 30 kDa GAAA tetraloop-receptor complex. J. Mol. Biol. 351 (2005) 371-382
11. Dick T.P., and Schamel W.A. Molecular evolution of transfer RNA from two precursor hairpins: implications for the origin of protein synthesis. J. Mol. Evol. 41 (1995) 1-9
12. Di Giulio M. On the origin of the transfer RNA molecule. J. Theor. Biol. 159 (1992) 199-214
13. Doudna J.A., and Cech T.R. The chemical repertoire of natural ribozymes. Nature 418 (2002) 222-228
14. Eigen M., and Schuster P. The hypercycle. A principle of natural self-organization. Part A: emergence of the hypercycle. Naturwissenschaften 64 (1977) 541-565
15. Eigen M., Lindemann B.F., Tietze M., Winkler-Oswatitsch R., Dress A., and von Haeseler A. How old is the genetic code? Statistical geometry of tRNA provides an answer. Science 244 (1989) 673-679
16. Eigen M. The origin of genetic information: viruses as models. Gene 135 (1993) 37-47
17. Ferris J.P., and Montmorillonite. Catalysis of 30-50 mer oligonucleotides: laboratory demonstration of potential steps in the origin of the RNA world. Orig. Life Evol. Biosph. 32 (2002) 311-312
18. Fani R., and Fondi R. Origin and evolution of metabolic pathways. Phys. Life Rev. 6 (2009) 23-52
19. Fondi, R., et al, this issue.
20. Fox G.E., and Naik A.K. The evolutionary history of the ribosome. In: Ribas de Pouplana L. (Ed). The Genetic Code and the Origin of Life (2004), Landes Bioscience 92-105
21. Giel-Pietraszuk M., and Barciszewski J. Charging of tRNA with non-natural amino acids at high pressure. FEBS J. 273 (2006) 3014-3023
22. Gregory S.T., and Dahlberg A.E. Peptide bond formation is all about proximity. Nat. Struct. Mol. Biol. 11 (2004) 586-587
23. Harms J., Schluenzen F., Zarivach R., Bashan A., Gat S., Agmon I., Bartels H., Franceschi F., and Yonath A. High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell 107 (2001) 679-688
24. Holcomb D.N., and Tinoco jun I. Conformation of polyriboadenylic acid: pH and temperature dependence. Biopolymers 3 (1965) 121-133
25. Ilangasekare M., Sanchez G., Nickles T., and Yarus M. Aminoacyl-RNA synthesis catalyzed by an RNA. Science 267 (1995) 643-647
26. Jaeger L., and Leontis N.B. Tecto-RNA: one-dimensional self-assembly through tertiary interactions. Angew. Chem. Int. Ed. Engl. 39 (2000) 2521-2524
27. Jeffares D.C., Poole A.M., and Penny D. Relics from the RNA world. J. Mol. Evol. 46 (1998) 18-36
28. Kholod N.S. Dimer formation by tRNAs. Biochemistry (Mosc) 64 (1999) 298-306
29. Korostelev A., Trakhanov S., Laurberg M., and Noller H.F. Crystal structure of a 70s ribosome-tRNA complex reveals functional interactions and rearrangements. Cell 126 (2006) 1065-1077
30. Krzyaniak A., Barciszewski J., Salahski P., and Jurczak J. The non-enzymatic specific aminoacylation of transfer RNA at high pressure. Int. J. Biol. Macromol. 16 (1994) 153-158
31. Lehmann J., Reichel A., Buguin A., and Libchaber A. Efficiency of a self-aminoacylating ribozyme: effect of the length and base-composition of its 3′ extension. RNA 13 (2008) 1191-1197
32. Lincoln T.A., and Joyce G.F. Self-sustained replication of an RNA enzyme. Science 323 (2009) 1229-1232
33. Londei P. Evolution of translational initiation: new insights from the archaea. FEMS Microbiol. Rev. 29 (2005) 185-200
34. Maizels N., and Weiner A.M. Phylogeny from function: evidence from the molecular fossil record that tRNA originated in replication, not translation. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 6729-6734
35. Mears J.A., Cannone J.J., Stagg S.M., Gutell R.R., Agrawal R.K., and Harvey S.C. Modeling a minimal ribosome based on comparative sequence analysis. J. Mol. Biol. 321 (2002) 215-234
36. Moore P.B., and Steitz T.A. After the ribosome structures: how does peptidyl transferase work?. RNA 9 (2003) 155-159
37. Nagaswamy U., and Fox G.E. RNA ligation and the origin of tRNA. Orig. Life Evol. Biosph. 33 (2003) 199-209
38. Nissen P., Ippolito J.A., Ban N., Moore P.B., and 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
39. Orgel L.E. The Origins of Life: Molecules and Natural Selection (1973), John Wiley and Sons, New York
40. Pino S., Ciciriello F., Costanzo G., and Di Mauro E. Nonenzymatic RNA ligation in water. J. Biol. Chem. 283 (2008) 36494-36503
41. Pley H.W., Flaherty K.M., and McKay D.B. Model for an RNA tertiary interaction from the structure of an intermolecular complex between a GAAA tetraloop and an RNA helix. Nature 372 1994 (1994) 111-113
42. Polacek N., and Mankin A.S. The ribosomal peptidyl transferase center: structure, function, evolution, inhibition. Crit. Rev. Biochem. Mol. Biol. 40 2005 (2005) 285-311
43. Powner M.W., Gerland B., and Sutherland J.D. Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459 (2009) 239-242
44. Roy M.D., Wittenhagen L.M., and Kelley S.O. Structural probing of a pathogenic tRNA dimer. RNA 11 (2005) 254-260
45. Russell R. RNA misfolding and the action of chaperones. Front Biosci. 13 (2008) 1-20
46. Samanta D., Mukhopadhyay D., Chowdhury S., Ghosh J., Pal S., Basu A., Bhattacharya A., Das A., Das D., and DasGupta C. Protein folding by domain V of Escherichia coli 23S rRNA: specificity of RNA protein interactions. J. Bacteriol. 190 (2008) 3344-3352
47. Sato N.S., Hirabayashi N., Agmon I., Yonath A., and Suzuki T. Comprehensive genetic selection revealed essential bases in the peptidyl-transferase center. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 15386-15391
48. Schuwirth B.S., Borovinskaya M.A., Hau C.W., Zhang W., Vila-Sanjurjo A., Holton J.M., and Cate J.H.D. Structures of the bacterial ribosome at 3.5 A resolution. Science 310 (2005) 827-834
49. 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
50. Smith J.M., and Szathmáry E. The Major Transitions in Evolution (1995), Oxford University Press
51. Smith T.F., Lee J.C., Gutell R.R., and Hartman H. The origin and evolution of the ribosome. Biol. Direct. 3 (2008) 16
52. Sun X., Li J.M., and Wartell R.M. Conversion of stable RNA hairpin to a metastable dimer in frozen solution. RNA 13 (2007) 2277-2286
53. Szostak J.W. Systems chemistry on early earth. Nature 459 (2009) 171-172
54. Talini, G., et al., this issue.
55. Voytek S.B., and Joyce G.F. Emergence of a fast-reacting ribozyme that is capable of undergoing continuous evolution. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 15288-15293
56. Weiner A.M., and Maizels N. tRNA-like structures tag the 3′ ends of genomic RNA molecules for replication: implications for the origin of protein synthesis. Proc. Natl. Acad. Sci. U.S.A. 84 (1987) 7383-7387
57. 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
58. Weinger, J.S., Strobel, S.A. (2007) Exploring the mechanism of protein synthesis with modified substrates and novel intermediate mimics. Blood Cells Mol. Dis. 38, 110-116.
59. Weixlbaumer A., Jin H., Neubauer C., Voorhees R.M., Petry S., Kelley A.C., and Ramakrishnan V. Insights into translational termination from the structure of RF2 bound to the ribosome. Science 322 (2008) 953-956
60. Woese C.R. The Emergence of Genetic Organization (1972), North-Holland Publishing pp. 302-332
61. Woese C.R. Evolution of the genetic code. Naturwissenschaften 60 (1973) 447-459
62. Woese C.R. Translation: in retrospect and prospect. RNA 7 (2001) 1055-1067
63. Yarus M. Primordial genetics: phenotype of the ribocyte. Annu. Rev. Genet. 36 (2002) 125-151
64. Yonath A. Ribosomal tolerance and peptide bond formation. Biol. Chem. 384 (2003) 1411-1419
65. 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