The dawn of the RNA World: Toward functional complexity through ligation of random RNA oligomers

RNA

Volumn 15, Issue 5, 2009, Pages 743-749

  Briones, Carlos ^a   Stich, Michael ^a   Manrubia, Susanna C ^a  

^a CENTRO DE ASTROBIOLOGÍA CSIC INTA   (Spain)

Author keywords

Hairpin ribozyme; Modular evolution; RNA folding; RNA ligation; RNA polymerase; Structural motif

Indexed keywords

OLIGOMER; RIBOZYME; RNA DIRECTED RNA POLYMERASE; RNA LIGASE; RNA POLYMERASE;

ARTICLE; CATALYSIS; ENZYME ACTIVITY; POLYMERIZATION; PRIORITY JOURNAL; RNA BINDING; RNA REPLICATION; RNA SEQUENCE; RNA STRUCTURE; UBIQUITINATION;

BIOGENESIS; EVOLUTION, MOLECULAR; INVERTED REPEAT SEQUENCES; NUCLEIC ACID CONFORMATION; RNA, CATALYTIC;

EID: 65249110487     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1488609     Document Type: Article

References (61)

1. Ancel, L.W. and Fontana, W. 2000. Plasticity, evolvability, and modularity in RNA. J. Exp. Zool. 288: 242-283.
2. Bartel, D.P. and Szostak, J.W. 1993. Isolation of new ribozymes of random sequences. Science 261: 1411-1418.
3. Bourdeau, V., Ferbeyre, G., Pageau, M., Paquin, B., and Cedergren, R. 1999. The distribution of RNA motifs in natural sequences. Nucleic Acids Res. 27: 4457-467.
4. Burke, D.H. and Willis, J.H. 1998. Recombination, RNA evolution, and bifunctional RNA molecules isolated through chimeric SELEX. RNA 4: 1165-1175.
5. Buzayan, J.M., Gerlach, W.L., and Bruening, G. 1986. Nonenzymatic cleavage and ligation of RNAs complementary to a plant virus satellite RNA. Nature 323: 349-353.
6. Cheng, C.P., Panavas, T., Luo, G., and Nagy, P.D. 2005. Heterologous RNA replication enhancer stimulates in vitro RNA synthesis and template-switching by the carmovirus, but not by the tombusvi- rus, RNA- dependent RNA polymerase: implication for modular evolution of RNA viruses. Virology 341: 107-121.
7. Deamer, D.W. 1998. Membrane compartments in prebiotic evolution. In The molecular origins of life (ed. A. Brack), pp. 189-205. Cambridge University Press, Cambridge, UK.
8. Eigen, M. 1971. Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften 58: 465-523.
9. Ekland, E.H., Szostak, J.W., and Bartel, D.P. 1995. Structurally complex and highly active RNA ligases derived from random RNA sequences. Science 269: 364-370.
10. Ertem, G., Hazen, R.M., and Dworkin, J.P. 2007. Sequence analysis of trimer isomers formed by montmorillonite catalysis in the reaction of binary monomer mixtures. Astrobiology 7: 715-722.
11. Fedor, M.J. 1999. Tertiary structure stabilization promotes hairpin ribozyme ligation. Biochemistry 38: 11040-11050.
12. Ferris, J.P. 2002. Montmorillonite catalysis of 30-50 mer oligonucleotides: laboratory demonstration of potential steps in the origin of the RNA world. Orig. Life Evol. Biosph. 32: 311-332.
13. Ferris, J.P. 2006. Montmorillonite-catalysed formation of RNA oligomers: The possible role of catalysis in the origins of life. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361: 1777-1786.
14. Ferris, J.P. and Ertem, G. 1993. Montmorillonite catalysis of RNA oligomer formation in aqueous solution. A model for the prebiotic formation of RNA. J. Am. Chem. Soc. 115: 12270-12275.
15. Flores, R., Delgado, S., Gas, M.E., Carbonell, A., Molina, D., Gago, S., and De la Peña, M. 2004. Viroids: The minimal noncoding RNAs with autonomous replication. FEBS Lett. 567: 42-48.
16. Fontana, W., Konings, D.A.M., Stadler, P.F., and Schuster, P. 1993. Statistics of RNA secondary structures. Biopolymers 33: 13891404.
17. Gaur, S., Heckman, J.E., and Burke, J.M. 2008. Mutational inhibition of ligation in the hairpin ribozyme: Substitutions of conserved nucleobases A9 and A10 destabilize tertiary structure and selectively promote cleavage. RNA 14: 55-65.
18. Gevertz, J., Gan, H.H., and Schlick, T. 2005. In vitro RNA random pools are not structurally diverse: A computational analysis. RNA 11: 853-863.
19. Gilbert, W. 1986. Origin of life- The RNA world. Nature 319: 618. doi: 10.1038/319618a0.
20. Gugliotti, L.A., Feldheim, D.L., and Eaton, B.E. 2004. RNA- mediated metal-metal bond formation in the synthesis of hexagonal palladium nanoparticles. Science 304: 850-852.
21. Hampel, A. and Tritz, R. 1989. RNA catalytic properties of the minimum (-)sTRSV sequence. Biochemistry 28: 4929-4933.
22. Hanczyc, M.M., Fujikawa, S.M., and Szostak, J.W. 2003. Experimental models of primitive cellular compartments: Encapsulation, growth, and division. Science 302: 618-622.
23. Hazen, R.M., Griffin, P.L., Carothers, J.M., and Szostak, J.W. 2007. Functional information and the emergence of biocomplexity. Proc. Natl. Acad. Sci. 104: 8574-8581.
24. Hendrix, D.K., Brenner, S.E., and Holbrook, S.R. 2005. RNA structural motifs: Building blocks of a modular biomolecule. Q. Rev. Biophys. 38: 221-243.
25. Hofacker, I.L., Fontana, W., Stadler, P.F., Bonhoeffer, L.S., Tacker, M., and Schuster, P. 1994. Fast folding and comparison of RNA secondary structures. Monatsh. Chem. 125: 167-188.
26. Horiya, S., Li, X., Kawai, G., Saito, R., Katoh, A., Kobayashi, K., and Harada, K. 2003. RNA LEGO: Magnesium-dependent formation of specific RNA assemblies through kissing interactions. Chem. Biol. 10: 645-654.
27. Huang, W. and Ferris, J.P. 2003. Synthesis of 35-40 mers of RNA oligomers from unblocked monomers. A simple approach to the RNA world. Chem. Commun. (Camb.) 12: 1458-1459.
28. Huang, W. and Ferris, J.P. 2006. One-step, regioselective synthesis of up to 50-mers of RNA oligomers by montmorillonite catalysis. J. Am. Chem. Soc. 128: 8914-8919.
29. Ivanov, S.A., Vauléon, S., and Müller, S. 2005. Efficient RNA ligation by reverse-joined hairpin ribozymes and engineering of twin ribozymes consisting of conventional and reverse-joined hairpin ribozyme units. FEBS J. 272: 4464-4474.
30. Jaeger, L., Wright, M.C., and Joyce, G.F. 1999. A complex ligase ribozyme evolved in vitro from a group I ribozyme domain. Proc. Natl. Acad. Sci. 96: 14712-14717.
31. Johnston, W.K., Unrau, P.J., Lawrence, M.S., Glasner, M.E., and Bartel, D.P. 2001. RNA-catalyzed RNA polymerization: Acurate and general RNA- templated primer extension. Science 292: 1319-1325.
32. Joshi, P.C., Pitsch, S., and Ferris, J.P. 2007. Selectivity of montmoril- lonite catalyzed prebiotic reactions of D, L-nucleotides. Orig. Life Evol. Biosph. 37: 3-26.
33. Joyce, G.F. 2002. The antiquity of RNA- based evolution. Nature 418: 214-221.
34. Joyce, G.F. 2004. Directed evolution of nucleic acid enzymes. Annu. Rev. Biochem. 73: 791-836.
35. Joyce, G.F. and Orgel, L.E. 2006. Progress toward understanding the origin of the RNA world. In The RNA world (eds. R.F. Gesteland et al.), 3rd ed., pp. 23-56. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. Kazakov, S.A., Balatskaya, S.V., and Johnston, B.H. 2006. Ligation of the hairpin ribozyme in cis induced by freezing and dehydration. RNA 12: 446-56.
37. Knight, R. and Yarus, M. 2003. Finding specific RNA motifs: Function in a zeptomole world? RNA 9: 218-230.
38. Kumar, R.M. and Joyce, G.F. 2003. A modular, bifunctional RNA that integrates itself into a target RNA. Proc. Natl. Acad. Sci. 100: 9738-9743.
39. Lincoln, T.A. and Joyce, G.F. 2009. Self-sustained replication of an RNA enzyme. Science 323: 1229-1232.
40. Liu, D., Gugliotti, L.A., Wu, T., Dolska, M., Tkachenko, A.G., Shipton, M.K., Eaton, B.E., and Feldheim, D.L. 2006. RNA- mediated synthesis of palladium nanoparticles on Au surfaces. Langmuir 22: 5862-5866.
41. Manrubia, S.C. and Briones, C. 2007. Modular evolution and increase of functional complexity in replicating RNA molecules. RNA 13:97-107.
42. Mansy, S.S., Schrum, J.P., Krishnamurthy, M., Tobé, S., Treco, D.A., and Szostak, J.W. 2008. Template-directed synthesis of a genetic polymer in a model protocell. Nature 454: 122-125.
43. Miyakawa, S. and Ferris, J.P. 2003. Sequence- and regioselectivity in the montmorillonite-catalyzed synthesis of RNA. J. Am. Chem. Soc. 125: 8202-8208.
44. Monnard, P.A. 2005. Catalysis in abiotic structured media: An approach to selective synthesis of biopolymers. Cell. Mol. Life Sci. 62: 520-534.
45. Monnard, P.A. and Szostak, J.W. 2008. Metal-ion catalyzed polymerization in the eutectic phase in water-ice: A possible approach to template-directed RNA polymerization. J. Inorg. Biochem. 102:1104-1111.
46. Muller, U.F. and Bartel, D.P. 2008. Improved polymerase ribozyme efficiency on hydrophobic assemblies. RNA 14: 552-562.
47. Nesbitt, S.M., Erlacher, H.A., and Fedor, M.J. 1999. The internal equilibrium of the hairpin ribozyme: Temperature, ion, and pH effects. J. Mol. Biol. 286: 1009-1024.
48. Orgel, L.E. 2004. Prebiotic chemistry and the origin of the RNA world. Crit. Rev. Biochem. Mol. Biol. 39: 99-123.
49. Pasquali, S., Gan, H.H., and Schlick, T. 2005. Modular RNA architecture revealed by computational analysis of existing pseu- doknots and ribosomal RNAs. Nucleic Acids Res. 33: 1384-1398.
50. Paul, N. and Joyce, G.F. 2002. A self-replicating ligase ribozyme. Proc. Natl. Acad. Sci. 99: 12733-12740.
51. Puerta-Fernáindez, E., Romero-Lóipez, C., Barroso- delJesúi s, A., and Berzal- Herranz, A. 2003. Ribozymes: Recent advances in the development of RNA tools. FEMS Microbiol. Rev. 27: 75-97.
52. Robertson, M.P. and Scott, W.G. 2007. The structural basis of ribozyme- catalyzed RNA assembly. Science 315: 1549-1553.
53. Schultes, E.A., Spasic, A., Mohanty, U., and Bartel, D.P. 2005. Compact and ordered collapse of randomly generated RNA sequences. Nat. Struct. Mol. Biol. 12: 1130-1136.
54. Schuster, P., Fontana, W., Stadler, P.F., and Hofacker, I. 1994. From sequences to shapes and back: A case study in RNA secondary structures. Proc. R. Soc. Lond. B. Biol. Sci. 255: 279-284.
55. Stich, M., Briones, C., and Manrubia, S.C. 2008. On the structural repertoire of pools of short, random RNA sequences. J. Theor. Biol. 252: 750-763.
56. Stoltenburg, R., Reinemann, C., and Strehlitz, B. 2007. SELEX-a (r)evolutionary method to generate high-affinity nucleic acid ligands. Biomol. Eng. 24: 381-403.
57. Svoboda, P. and Di Cara, A. 2006. Hairpin RNA: A secondary structure of primary importance. Cell. Mol. Life Sci. 63: 901-918.
58. Takeuchi, N. and Hogeweg, P. 2008. Evolution ofcomplexityin RNA- like replicator systems. Biol. Direct 3: 11. doi: 10.1186/1745-6150-3- 11.
59. Vlassov, A.V., Johnston, B.H., Landweber, L.F., and Kazakov, S.A. 2004. Ligation activity of fragmented ribozymes in frozen solution: Implications for the RNA world. Nucleic Acids Res. 32: 2966-2974.
60. Voytek, S.B. and Joyce, G.F. 2007. Emergence of a fast-reacting ribozyme that is capable of undergoing continuous evolution. Proc. Natl. Acad. Sci. 104: 15288-15293.
61. Zaher, H.S. and Unrau, P.J. 2007. Selection of an improved RNA polymerase ribozyme with superior extension and fidelity. RNA 13: 1017-1026.