The dimeric proto-ribosome: Structural details and possible implications on the origin of life

International Journal of Molecular Sciences

Volumn 10, Issue 7, 2009, Pages 2921-2934

  Agmon, Ilana ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Origin of life; Proto ribosome; Ribosome symmetrical region

Indexed keywords

PEPTIDE; RNA;

ANTICODON; ARTICLE; BINDING SITE; BIOGENESIS; CHEMICAL STRUCTURE; DIMERIZATION; ESCHERICHIA COLI; PROTEIN INTERACTION; PROTEIN SYNTHESIS; RIBOSOME SUBUNIT; RNA SEQUENCE; RNA TRANSLATION;

ORIGIN OF LIFE; PROTO-RIBOSOME; RIBOSOME SYMMETRICAL REGION;

BIOGENESIS; EVOLUTION, MOLECULAR; NUCLEIC ACID CONFORMATION; RIBOSOMES; RNA, RIBOSOMAL;

EID: 68949156176     PISSN: None     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms10072921     Document Type: Article

References (52)

1. Woese, C.R. Translation: in retrospect and prospect. RNA 2001, 7, 1055-1067.
2. Agmon, I.; Bashan, A.; Yonath, A. On ribosome conservation and evolution. Israel Journal of Ecology and Evolution 2006, 52, 359-374.
3. Agmon, I.; Davidovich, C.; Bashan, A.; Yonath, A. Identification of the prebiotic translation apparatus within the contemporary ribosome, 2009. http://precedings.nature.com/documents/-2921/version/1, accessed 18 March 2009.
4. Agmon, I.; Auerbach, T.; Baram, D.; Bartels, H.; Bashan, A.; Berisio, R.; Fucini, P.; Hansen, H.A.; Harms, J.; Kessler, M.; Peretz, M.; Schluenzen, F.; Yonath, A.; Zarivach, R. On peptide bond formation, translocation, nascent protein progression and the regulatory properties of ribosomes. Eur. J. Biochem. 2003, 270, 2543-2556.
5. Agmon, I.; Bashan, A.; Zarivach, R.; Yonath, A. Symmetry at the active site of the ribosome: Structural and functional implications. Biol. Chem. 2005, 386, 833-844.
6. 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.; Yonath, A. Structural basis of the ribosomal machinery for peptide bond formation, translocation, and nascent chain progression. Mol. Cell 2003, 11, 91-102.
7. Bashan, A.; Zarivach, R.; Schluenzen, F.; Agmon, I.; Harms, J.; Auerbach, T.; Baram, D.; Berisio, R.; Bartels, H.; Hansen, H.A.S.; Fucini, P.; Wilson, D.; Peretz, M.; Kessler, M.; Yonath, A. Ribosomal crystallography: Peptide bond formation and its inhibition. Biopolymers 2003, 70, 19-41.
8. Bashan, A.; Yonath, A. Correlating ribosome function with high-resolution structures. Trends Microbiol. 2008, 16, 326-335.
9. Bokov, K.; Steinberg, S.V. A hierarchical model for evolution of 23S ribosomal RNA. Nature 2009, 457, 977-980.
10. Anderson, R.M.; Kwon, M.; Strobel, S. A. Toward ribosomal RNA catalytic activity in the absence of protein. J. Mol. Evol. 2007, 64, 472-483.
11. Smith, T.F.; Lee, J.C.; Gutell, R.R.; Hartman, H. The origin and evolution of the ribosome. Biol. Direct. 2008, 3, 16.
12. Cannone, J.J.; Subramanian, S.; Schnare, M.N.; Collett, J.R.; D'Souza, L.M.; Du, Y.; Feng, B.; Lin, N.; Madabusi, L.V.; Müller, K.M.; Pande, N.; Shang, Z.; Yu, N.; Gutell, R.R. The Comparative RNA Web CRW. Site: An online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 2002, 3, 1-31. http://www.rna.ccbb. utexas.edu/, accessed July 24, 2004.
13. Chworos, A.; Severcan, I.; Koyfman, A.Y.; Weinkam, P.; Oroudjev, E.; Hansma, H.G.; Jaeger, L. Building programmable jigsaw puzzles with RNA. Science 2004, 306, 2068-2072.
14. Jaeger, L.; Chworos, A. The architectonics of programmable RNA and DNA nanostructures. Curr. Opin. Struct. Biol. 2006, 16, 531-543.
15. Severcan, I.; Geary, C.; Verzemnieks, E.; Chworos, A.; Jaeger, L. Square-shaped RNA particles from different RNA folds. Nano Lett. 2009, 9, 1270-1277.
16. Doshi, K.J.; Cannone, J.J.; Cobaugh, C.W.; Gutell, R.R. Evaluation of the suitability of free-energy minimization using nearest-neighbor energy parameters for RNA secondary structure prediction. BMC Bioinformatics 2004, 5, 105.
17. Zuker, M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003, 31, 3406-3415.
18. Mathews, D.H.; Sabina, J.; Zuker, M.; Turner, D.H. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol. 1999, 288, 911-940.
19. Ishitani, R.; Nureki, O.; Nameki, N.; Okada, N.; Nishimura, S.; Yokoyama, S. Alternative tertiary structure of tRNA for recognition by a posttranscriptional modification enzyme. Cell 2003, 113, 383-394.
20. Madore, E.; Florentz, C.; Giegé, R.; Lapointe, J. Magnesium-dependent alternative foldings of active and inactive Escherichia coli tRNAGlu. revealed by chemical probing. Nucleic Acids Res 1999, 27, 3583-3588.
21. Ohtsuki, T.; Kawai, G.; Watanabe, K. The minimal tRNA: Unique structure of Ascaris suum mitochondrial tRNASer.UCU having a short T arm and lacking the entire D arm. FEBS Lett. 2002, 514, 37-43.
22. Frazer-Abel, A.A.; Hagerman, P.J. Variation of the acceptor-anticodon interstem angles among mitochondrial and non-mitochondrial tRNAs. J. Mol. Biol. 2004, 343, 313-325.
23. Wilkinson, K.A.; Merino, E.J.; Weeks, K.M. RNA SHAPE chemistry reveals nonhierarchical interactions dominate equilibrium structural transitions in tRNA(Asp) transcripts. J. Am. Chem. Soc. 2005, 127, 4659-4667.
24. Jaeger, L.; Westhof, E.; Leontis, N.B. TectoRNA: Modular assembly units for the construction of RNA nano-objects. Nucleic Acids Res. 2001, 29, 455-463.
25. Eigen, M.; Lindemann, B.F.; Tietze, M.; Winkler-Oswatitsch, R.; Dress, A.; von Haeseler, A. How old is the genetic code? Statistical geometry of tRNA provides an answer. Science 1989, 244, 673-679.
26. Maizels, N.; Weiner, A.M. Phylogeny from function: Evidence from the molecular fossil record that tRNA originated in replication, not translation. Proc. Natl. Acad. Sci. USA 1994, 91, 6729-6734.
27. Bailey, S. The CCP4 suite - programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 1994, 50, 760-763.
28. Kholod, N.S. Dimer formation by tRNAs. Biochemistry Mosc. 1999, 64, 298-306.
29. Roy, M.D.; Wittenhagen, L.M.; Kelley, S.O. Structural probing of a pathogenic tRNA dimer. RNA 2005, 11, 254-260.
30. Sun, X.; Li, J.M.; Wartell, R.M. Conversion of stable RNA hairpin to a metastable dimer in frozen solution. RNA 2007, 13, 2277-2286.
31. Pyle, A.M. Metal ions in the structure and function of RNA. J. Biol. Inorg. Chem. 2002, 7, 679-690.
32. Draper, D.E. A guide to ions and RNA structure. RNA 2004, 10, 335-343.
33. Davis, J.H.; Tonelli, M.; Scott, L.G.; Jaeger, L.; Williamson, J.R.; Butcher, S.E. RNA helical packing in solution: NMR structure of a 30 kDa GAAA tetraloop-receptor complex. J. Mol. Biol. 2005, 351, 371-382.
34. Pley, H.W.; Flaherty, K.M.; 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 1994, 372, 111-113.
35. Jaeger. L.; Michel, F.; Westhof, E. Involvement of a GNRA tetraloop in long-range RNA tertiary interactions. J. Mol. Biol. 1994, 236, 1271-1276.
36. Costa, M.; Michel, F. Rules for RNA recognition of GNRA tetraloops deduced by in vitro selection: Comparison with in vivo evolution. EMBO J. 1997, 16, 3289-3302.
37. Abramovitz, D.L.; Pyle, A.M. Remarkable morphological variability of a common RNA folding motif: The GNRA tetraloop-receptor interaction. J. Mol. Biol. 1997, 266, 493-506.
38. 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. USA 2001, 98, 4899-4903.
39. Battle, D.J.; Doudna, J.A. Specificity of RNA-RNA helix recognition. Proc. Natl. Acad. Sci. USA 2002, 99, 11676-11681.
40. Di Giulio, M. On the origin of the transfer RNA molecule. J. Theor. Biol. 1992, 159, 199-214.
41. Dick, T.P.; Schamel, W.A. Molecular evolution of transfer RNA from two precursor hairpins: Implications for the origin of protein synthesis. J. Mol. Evol. 1995, 41, 1-9.
42. Nagaswamy, U.; Fox, G.E. RNA ligation and the origin of tRNA. Orig. Life Evol. Biosphere 2003, 33, 199-209.
43. Samanta, D.; Mukhopadhyay, D.; Chowdhury, S.; Ghosh, J.; Pal, S.; Basu, A.; Bhattacharya, A.; Das, A.; Das, D.; DasGupta, C. Protein folding by domain V of Escherichia coli 23S rRNA: Specificity of RNA-protein interactions. J. Bacteriol. 2008, 190, 3344-3352.
44. Zarivach, R.; Bashan, A.; Berisio, R.; Harms, J.; Auerbach, T.; Schluenzen, F.; Bartels, H.; Baram, D.; Pyetan, E.; Sittner, A.; Amit, M.; Hansen, H.S.A.; Kessler, M.; Liebe, C.; Wolff, A.; Agmon, I.; Yonath, A. Functional aspects of ribosomal architecture: symmetry, chirality and regulation. J. Phys. Org. Chem. 2004, 17, 901-912.
45. Thirumoorthy, K.; Nandi, N. Homochiral preference in peptide synthesis in ribosome: Role of amino terminal, peptidyl terminal, and U2620. J. Phys. Chem. B 2007, 111, 9999-10004.
46. Gilbert, W. The RNA world. Nature 1986, 319, 618.
47. Woese, C. The Genetic Code; Harper & Row: New York, 1967.
48. Rich, A. On the problems of evolution and biochemical information transfer. In Horizons in Biochemistry; Pullman, K.M., Ed.; Academic Press: New York, NY, USA, 1962; pp. 103-126.
49. Szathmáry, E. The origin of the genetic code: Amino acids as cofactors in an RNA world. Trends Genet. 1999, 15, 223-229.
50. Joyce, C.M.; Steitz, T.A. Polymerase structures and function: variations on a theme? J. Bacteriol. 1995, 177, 6321-6329.
51. Arnold, E.; Ding, J.; Hughes, S.H.; Hostomsky, Z. Structures of DNA and RNA polymerases and their interactions with nucleic acid substrates. Curr. Opin. Struct. Biol. 1995, 5, 27-38.
52. Fox, G.E.; Naik, A.K. The Evolutionary history of the ribosome. In The Genetic Code and the Origin of Life; de Pouplana, L.R., Ed.; Landes Bioscience: Georgetown, Texas, USA, 2004; Chapter 6, pp. 92-105.