Aminoacylating urzymes challenge the RNA world hypothesis

Journal of Biological Chemistry

Volumn 288, Issue 37, 2013, Pages 26856-26863

  Li, Li ^a   Francklyn, Christopher ^b   Carter Jr , Charles W ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLASS I; CLASS II; PEPTIDE SYNTHESIS; RNA WORLD;

BIOCHEMISTRY; BIOLOGY;

RNA;

AMINO ACID TRANSFER RNA LIGASE; TRANSFER RNA; UNCLASSIFIED DRUG; URZYME;

ACYLATION; ANTICODON; ARTICLE; BINDING AFFINITY; BINDING SITE; CATALYST; ENZYME DEGRADATION; ENZYME STRUCTURE; ENZYME SYNTHESIS; PRIORITY JOURNAL; PROTEIN RNA BINDING; RNA TRANSLATION;

AMINOACYL TRNA SYNTHESIS; AMINOACYL TRNA SYNTHETASE; CATALYTIC RNA; ENZYME CATALYSIS; ENZYME PROFICIENCY; MOLECULAR EVOLUTION; ORIGIN OF TRANSLATION; PROTEIN SYNTHESIS; TRNA;

AMINO ACYL-TRNA SYNTHETASES; AMINOACYLATION; ANTICODON; CATALYSIS; CATALYTIC DOMAIN; EVOLUTION, MOLECULAR; GEOBACILLUS STEAROTHERMOPHILUS; HUMANS; MODELS, BIOLOGICAL; NUCLEOTIDES; PEPTIDES; RHODOPSEUDOMONAS; RNA, TRANSFER;

EID: 84884171822     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.496125     Document Type: Article

References (42)

1. Gilbert, W. (1986) Nature 319, 618
2. Yarus, M. (2011) Life from an RNA World: The Ancestor Within, pp. 132-155, Harvard University Press, Cambridge, MA
3. Koonin, E. V. (2012) The Logic of Chance: The Nature and Origin of Biological Evolution, pp. 351-395, Pearson Education, FT Press Science, Upper Saddle River, NJ
4. Augustine, J., and Francklyn, C. (1997) Design of an active fragment of a class II aminoacyl-tRNA synthetase and its significance for synthetase evolution. Biochemistry 36, 3473-3482
5. Schwob, E., and Söll, D. (1993) Selection of a "minimal" glutaminyl-tRNA synthetase and the evolution of class I synthetases. EMBO J. 12, 5201-5208
6. Francklyn, C., and Schimmel, P. (1989) Aminoacylation of RNA minihelices with alanine. Nature 337, 478-481
7. Francklyn, C., Musier-Forsyth, K., and Schimmel, P. (1992) Small RNA helices as substrates for aminoacylation and their relationship to charging of transfer RNAs. Eur. J. Biochem. 206, 315-321
8. Schimmel, P., Giegé, R., Moras, D., and Yokoyama, S. (1993) An operationalRNAcode for amino acids and possible relationship to genetic code. Proc. Natl. Acad. Sci. U.S.A. 90, 8763-8768
9. Pham, Y., Kuhlman, B., Butterfoss, G. L., Hu, H., Weinreb, V., and Carter, C. W., Jr. (2010) Tryptophanyl-tRNA synthetase Urzyme: a model to recapitulate molecular evolution and investigate intramolecular complementation. J. Biol. Chem. 285, 38590-38601
10. Pham, Y., Li, L., Kim, A., Erdogan, O., Weinreb, V., Butterfoss, G. L., Kuhlman, B., and Carter, C. W., Jr. (2007) A minimal TrpRS catalytic domain supports sense/antisense ancestry of class I and II aminoacyltRNA synthetases. Mol. Cell 25, 851-862
11. Li, L., Weinreb, V., Francklyn, C., and Carter, C. W., Jr. (2011) HistidyltRNA synthetase Urzymes: class I and II aminoacyl-tRNA synthetase Urzymes have comparable catalytic activities for cognate amino acid activation. J. Biol. Chem. 286, 10387-10395
12. Schroeder, G. K., and Wolfenden, R. (2007) The rate enhancement produced by the ribosome: an improved model. Biochemistry 46, 4037-4044
13. Wolfson, A. D., Pleiss, J. A., and Uhlenbeck, O. C. (1998) A new assay for tRNA aminoacylation kinetics. RNA 4, 1019-1023
14. SAS (2007) Version 6, SAS Institute, Cary NC
15. Weinreb, V., Li, L., and Carter, C. W., Jr. (2012) A master switch couples Mg2+-assisted catalysis to domain motion in B. stearothermophilus tryptophanyl- tRNA synthetase. Structure 20, 128-138
16. Kirby, A. J., and Younas, M. (1970) The reactivity of phosphate esters: reactions of diesters with nucleophiles. J. Chem. Soc. B 1165-1172
17. Schall, O. F., Suzuki, I., Murray, C. L., Gordon, J. I., and Gokel, G. W. (1998) Characterization of acyl adenyl anhydrides: Differences in the hydrolytic rates of fatty acyl-AMP and aminoacyl-AMP derivatives. J. Org. Chem. 63, 8661-8667
18. O'Donoghue, P., and Luthey-Schulten, Z. (2003) On the evolution of structure in aminoacyl-tRNA synthetases. Microbiol. Mol. Biol. Rev. 67, 550-573
19. Fournier, G. P., Andam, C. P., Alm, E. J., and Gogarten, J. P. (2011) Molecular evolution of aminoacyl tRNA synthetase proteins in the early history of life. Orig. Life Evol. Biosph. 41, 621-632
20. Härtlein, M., and Cusack, S. (1995) Structure, function and evolution of seryl-tRNA synthetases: implications for the evolution of aminoacyltRNA synthetases and the genetic code. J. Mol. Evol. 40, 519-530
21. Xin, Y., Li, W., and First, E. A. (2000) Stabilization of the transition state for the transfer of tyrosine to tRNA(Tyr) by tyrosyl-tRNA synthetase. J. Mol. Biol. 303, 299-310
22. Cammer, S., and Carter, C. W., Jr. (2010) Six Rossmannoid folds, including the class I aminoacyl-tRNA synthetases, share a partial core with the anticodon- binding domain of a class II aminoacyl-tRNA synthetase. Bioinformatics 26, 709-714
23. Chandrasekaran, S. N., Yardimci, G. G., Erdogan, O., Roach, J., and Carter, C. W., Jr. (2013) Statistical evaluation of the Rodin-Ohno hypothesis: sense/antisense coding of ancestral class I and II aminoacyl-tRNA synthetases. Mol. Biol. Evol. 30, 1588-1604
24. Carter, C. W., Jr. (1993) Cognition, mechanism, and evolutionary relationships in aminoacyl-tRNA synthetases. Annu. Rev. Biochem. 62, 715-748
25. Delarue, M. (2007) KISS: the kinetoplastid RNA editing sequence search tool. RNA 13, 161-169
26. Kamtekar, S., Schiffer, J. M., Xiong, H., Babik, J. M., and Hecht, M. H. (1993) Protein design by binary patterning of polar and nonpolar amino acids. Science 262, 1680-1685
27. Moffet, D. A., Foley, J., and Hecht, M. H. (2003) Midpoint reduction potentials and heme binding stoichiometries of de novo proteins from designed combinatorial libraries. Biophys. Chem. 105, 231-239
28. Patel, S. C., Bradley, L. H., Jinadasa, S. P., and Hecht, M. H. (2009) Cofactor binding and enzymatic activity in an unevolved superfamily of de novo designed 4-helix bundle proteins. Protein Sci. 18, 1388-1400
29. Tuerk, C., and Gold, L. (1990) Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249, 505-510
30. Ellington, A. D., and Szostak, J. W. (1990) In vitro selection of RNA molecules that bind specific ligands. Nature 346, 818-822
31. Kumar, R. K., and Yarus, M. (2001) RNA-catalyzed amino acid activation. Biochemistry 40, 6998-7004
32. Illangasekare, M., and Yarus, M. (1999) A tiny RNA that catalyzes both aminoacyl-RNA and peptidyl-RNA synthesis. RNA 5, 1482-1489
33. Yarus, M. (2000) RNA-ligand chemistry: a testable source for the genetic code. RNA 6, 475-484
34. Zhang, B., and Cech, T. R. (1997) Peptide bond formation by in vitro selected ribozymes. Nature 390, 96-100
35. Thornton, J. W. (2004) Resurrecting ancient genes: experimental analysis of extinct molecules. Nat. Rev. Genet. 5, 366-375
36. Carter, C. W., Jr., and Kraut, J. (1974) A proposed model for interaction of polypeptides with RNA. Proc. Natl. Acad. Sci. U.S.A. 71, 283-287
37. Church, G. M., Sussman, J. L., and Kim, S. H. (1977) Secondary structural complementarity betweenDNAand proteins. Proc. Natl. Acad. Sci. U.S.A. 74, 1458-1462
38. Harish, A., and Caetano-Anollés, G. (2012) Ribosomal history reveals origins of modern protein synthesis. PLoS ONE 7, e32776
39. Cech, T. (2009) Crawling out of the RNA world. Cell 136, 599-602
40. Stockbridge, R. B., and Wolfenden, R. (2009) The intrinsic reactivity of ATP and the catalytic proficiencies of kinases acting on glucose, N-acetylgalactosamine, and homoserine: a thermodynamic analysis. J. Biol. Chem. 284, 22747-22757
41. Berezovsky, I. N., Grosberg, A. Y., and Trifonov, E. N. (2000) Closed loops of nearly standard size: common basic element of protein structure. FEBS Lett. 466, 283-286
42. Joseph, D. R., and Muench, K. (1971) Tryptophanyl transfer ribonucleic acid synthetase of Escherichia coli. I. Purification of the enzyme and of tryptrophan transfer ribonucleic acid. J. Biol. Chem. 246, 7602-7609