Ligation of the hairpin ribozyme in cis induced by freezing and dehydration

RNA

Volumn 12, Issue 3, 2006, Pages 446-456

  Kazakov, Sergei A ^a   Balatskaya, Svetlana V ^a,c   Johnston, Brian H ^a,b  

^a SomaGenics Inc   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c R and D Project Development and Management   (United States)

Author keywords

Dehydration; Ethanol; Freezing; Hairpin ribozyme; Ligation; RNA world

Indexed keywords

2',3' CYCLIC PHOSPHATE; ALCOHOL; ANION; HYDROXYL GROUP; METAL ION; MONOVALENT CATION; PHOSPHATE; RIBOZYME; SOLVENT; UNCLASSIFIED DRUG;

AQUEOUS SOLUTION; ARTICLE; COMPLEX FORMATION; COOLING; EQUILIBRIUM CONSTANT; EVAPORATION; FREEZING; GENE INDUCTION; HYPOTHESIS; LIGATION; LINEAR SYSTEM; MOLECULAR EVOLUTION; MOLECULAR MECHANICS; OBSERVATION; PRIORITY JOURNAL; RNA ANALYSIS; RNA DEGRADATION; STIMULATION;

BASE SEQUENCE; BIOGENESIS; CATIONS, DIVALENT; DESICCATION; ETHANOL; EVOLUTION, MOLECULAR; FREEZING; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RNA, CATALYTIC; SODIUM CHLORIDE;

EID: 33344462715     PISSN: 13558382     EISSN: None     Source Type: Journal    
DOI: 10.1261/rna.2123506     Document Type: Article

References (77)

1. Anderson, C.F. and Record Jr., M.T. 1995. Salt-nucleic acid interactions. Annu. Rev. Phys. Chem. 46: 657-700.
2. Bada, J.L. and Lazcano, A. 2002. Origin of life. Some like it hot, but not the first biomolecules. Science 296: 1982-1983.
3. Barciszewski, J., Jurczak, J., Porowski, S., Specht, T., and Erdmann, V.A. 1999. The decisive role of the water structure in changes of conformation of nucleic acids. Acta Biochim. Pol. 46: 133-144.
4. Beneventi, S. and Onori, G. 1986. Effect of ethanol on the thermal stability of tRNA molecules. Biophys. Chem. 25: 181-190.
5. Bruice, T.C. and Butler, A.R. 1964. Catalysis in water and ice. II. The reaction of thiolactones with morpholine in frozen systems. J. Am. Chem. Soc. 86: 4104-4108.
6. Butler, A.R. and Bruice, T.C. 1964. Catalysis in water and ice. A comparison of the kinetics of hydrolysis of acetic anhydride, β-propiolactone, and p-nitrophenyl acetate and the dehydration of 5-hydro-6-hydroxy-deoxyuridine in water and ice. J. Am. Chem. Soc. 86: 313-319.
7. Buzayan, J.M., Gerlach, W.L., and Bruening, G. 1986. Non-enzymatic cleavage and ligation of RNAs complementary to a plant virus satellite RNA. Nature 323: 349-353.
8. Carothers, J.M., Oestreich, S.C., Davis, J.H., and Szostak, J.W. 2004. Informational complexity and functional activity of RNA structures. J. Am. Chem. Soc. 126: 5130-5137.
9. Cech, T.R. 1993. The efficiency and versatility of catalytic RNA: Implications for an RNA world. Gene 135: 33-36.
10. Chowrira, B.M., Berzal-Herranz, A., and Burke, J.M. 1993. Ionic requirements for RNA binding, cleavage, and ligation by the hairpin ribozyme. Biochemistry 32: 1088-1095.
11. Dallas, A., Vlassov, A.V., and Kazakov, S.A. 2004. Principles of cleavage of nucleic acids by metal ions. In Artificial nucleases (ed. M.A. Zenkova), Nucleic acids and molecular biology (ed. H.J. Gross), Vol. 13, pp. 61-88. Springer-Verlag, Heidelberg, Germany.
12. Dean, J.A., ed. 1985. Lange's handbook of chemistry, 13th ed. McGraw-Hill, New York.
13. Donahue, C.P. and Fedor, M.J. 1997. Kinetics of hairpin ribozyme cleavage in yeast. RNA 3: 961-973.
14. 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.
15. Elghanian, R., Storhoff, J.J., Mucic, R.C., Letsinger, R.L, and Mirkin, C.A. 1997. Selective colorimetric detection of polynucleotides based on the distance-dependent optical properties of gold nanoparticles. Science 277: 1078-1081.
16. Esteban, J.A., Banerjee, A.R., and Burke, J.M. 1997. Kinetic mechanism of the hairpin ribozyme. Identification and characterization of two non-exchangeable conformations. J. Biol. Chem. 272: 13629-13639.
17. Fedor, M. 1999. Tertiary structure stabilization promotes hairpin ribozyme ligation. Biochemistry 38: 11040-11050.
18. _. 2000. Structure and function of the hairpin ribozyme. J. Mol. Biol. 297: 269-291.
19. _. 2002. The role of metal ions in RNA catalysis. Curr. Opin. Struct. Biol. 12: 289-295.
20. Feig, A.L., Ammons, G.E., and Uhlenbeck, O.C. 1998. Cryoenzymology of the hammerhead ribozyme. RNA 4: 1251-1258.
21. Feldstein, P.A. and Bruening, G. 1993. Catalytically active geometry in the reversible circularization of 'mini-monomer' RNAs derived from the complementary strand of tobacco ringspot virus satellite RNA. Nucleic Acids Res. 21: 1991-1998.
22. Fink, A.L. and Greeves, M.A. 1979. Cryoenzymology: The study of enzyme catalysis at subzero temperatures. Methods Enzymol. 63: 336-370.
23. Gardiner, K.J., Marsh, T.L., and Pace, N.R. 1985. Ion dependence of the Bacillus subtilis RNase P reaction. J. Biol. Chem. 260: 5415-5419.
24. Geyer, C.R. and Sen, D. 1997. Evidence for the metal-cofactor independence of an RNA phosphodiester-cleaving DNA enzyme. Chem. Biol. 4: 579-593.
25. Gilbert, W. 1986. The RNA world. Nature 319: 618.
26. Hampel, A. and Tritz, R. 1989. RNA catalytic properties of the minimum (-)sTRSV sequence. Biochemistry 28: 4929-4933.
27. Hanna, M. and Szostak, J.W. 1994. Suppression of mutations in the core of the Tetrahymena ribozyme by spermidine, ethanol and by substrate stabilization. Nucleic Acids Res. 22: 5326-5331.
28. Harrison, B. and Zimmerman, S.B. 1984. Polymer-stimulated ligation: Enhanced ligation of oligo- and polynucleotides by T4 RNA ligase in polymer solutions. Nucleic Acids Res. 12: 8235-8251.
29. Hegg, L.A. and Fedor, M.J. 1995. Kinetics and thermodynamics of intermolecular catalysis by hairpin ribozyme. Biochemistry 34: 15813-15828.
30. Hirao, I. and Ellington, A.D. 1995. Re-creating the RNA world. Curr. Biol. 5: 1017-1022.
31. Israelachvili, J. and Wennerström, H. 1996. Role of hydration and water structure in biological and colloidal intertactions. Nature 379: 219-225.
32. Joyce, G.F. 2002. The antiquity of RNA-based evolution. Nature 418: 214-221.
33. Joyce, G.F. and Orgel, L.E. 1993. Prospects for understanding the origin of the RNA world. In The RNA world (eds. R.F. Gesteland and J.F. Atkins), pp. 1-25. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
34. Kanavarioti, A., Monnard, P.A., and Deamer, D.W. 2001. Eutectic phases in ice facilitate nonenzymatic nucleic acid synthesis. Astrobiology 1: 271-281.
35. Kazakov, S.A., Balatskaya, S.V., and Johnston, B.H. 1998. Freezinginduced self-ligation of the hairpin ribozyme: Cationic effects. In Structure, motion, interaction and expression of biological macromolecules (eds. R.H. Sarma and M.H. Sarma), Vol. 2, pp. 155-161. Adenine Press, Albany, NY.
36. Kiovsky, T.E. and Pincock, R.E. 1966. The mutarotation of glucose in frozen aqueous solutions. J. Am. Chem. Soc. 88: 4704-4710.
37. Komatsu, Y., Koizumi, M., Sekiguchi, A., and Ohtsuka, E. 1993. Cross-ligation and exchange reactions catalyzed by hairpin ribozymes. Nucleic Acids Res. 21: 185-190.
38. Komatsu, Y., Kanzaki, M., Koizumi, A., and Ohtsuka, E. 1995. Modification of primary structures of hairpin ribozymes for probing active conformations. J. Mol. Biol. 252: 296-304.
39. Kuntz, I.D., Brassfield, T.S., Law, G.D., and Purcell, G.V. 1969. Hydration of macromolecules. Science 163: 1329-1331.
40. Lazcano, A. and Miller, S.L. 1996. The origin and early evolution of life: Prebiotic chemistry, the pre-RNA world, and time. Cell 85: 793-798.
41. Levy, M., Miller, S.L., and Oró, J. 1999. Production of guanine from NH(4)CN polymerizations. J. Mol. Evol. 49: 165-168.
42. Li, Y. and Breaker, R.R. 1999. Kinetics of RNA degradation by specific base catalysis of transesterification involving the 2′-hydroxyl group. J. Am. Chem. Soc. 121: 5364-5372.
43. Miyakawa, S., Cleaves, H.J., and Miller, S.L. 2002. The cold origin of life: B. Implications based on pyrimidines and purines produced from frozen ammonium cyanide solutions. Orig. Life Evol. Biosph. 32: 209-218.
44. Monnard, P.A., Apel, C.L., Kanavarioti, A., and Deamer, D.W. 2002. Influence of ionic inorganic solutes on self-assembly and polymerization processes related to early forms of life: Implications for a prebiotic aqueous medium. Astrobiology 2: 139-152.
45. Murray, J.B., Seyhan, A.A., Walter, N.G., Burke, J.M., and Scott, W.G. 1998. The hammerhead, hairpin and VS ribozymes are catalytically proficient in monovalent cations alone. Chem. Biol. 5: 587-595.
46. Nesbitt, S., Hegg, L.A., and Fedor, M.J. 1997. An unusual pH-independent and metal-ion-independent mechanism for hairpin ribozyme catalysis. Chem. Biol. 4: 619-630.
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. Pace, N.R. 1991. Origin of life - Facing up to the physical setting. Cell 65: 531-533.
49. Pincock, R.E. 1969. Reactions in frozen systems. Acc. Chem. Res. 4: 97-103.
50. Prestrelski, S.J., Arakawa, T., and Carpenter, J.F. 1993. Separation of freezing- and drying-induced denaturation of lyophilized proteins using stress-specific stabilization. II. Structural studies using infrared spectroscopy. Arch. Biochem. Biophys. 303: 465-473.
51. Prody, G.A., Bakos, J.T., Buzayan, J.M., Schneider, I.R., and Bruening, G. 1986. Autolytic processing of dimeric plant virus satellite RNA. Science 231: 1577-1580.
52. Prusoff, W.H. 1963. Low-temperature reversal of the ultraviolet photochemical reaction product of 2′-deoxyuridive. Biochim. Biophys. Acta 68: 302-310.
53. Pyle, A.M. 2002. Metal ions in the structure and function of RNA. J. Biol. Inorg. Chem. 7: 679-690.
54. Renz, M., Lohrmann, R., and Orgel, L.E. 1971. Catalysts for the polymerization of adenosine cyclic 2′, 3′-phosphate on a poly(U) template. Biochim. Biophys. Acta 240: 463-471.
55. Rozners, E. and Moulder, J. 2004. Hydration of short DNA, RNA and 2′-OMe oligonucleotides determined by osmotic stressing. Nucleic Acids Res. 32: 248-254.
56. Sanchez, R., Ferris, J., and Orgel, L.E. 1966. Condition for purine synthesis: Did prebiotic synthesis occur at low temperatures? Science 153: 72-73.
57. Saville, B.J. and Collins, R.A. 1991. RNA-mediated ligation of self-cleavage products of a Neurospora mitochondrial plasmid transcript. Proc. Natl. Acad. Sci. 88: 8826-8830.
58. Sawai, H. and Wada, M. 2000. Nonenzymatic template-directed condensation of short-chained oligouridylates on a poly(A) template. Orig. Life Evol. Biosph. 30: 503-511.
59. Scott, W.G. 1999. RNA structure, metal ions, and catalysis. Curr. Opin. Chem. Biol. 3: 705-709.
60. 2+-independent hairpin ribozyme catalysis in hydrated RNA films. RNA 6: 189-198.
61. Sharmeen, L., Kuo, M.Y., and Taylor, J. 1989. Self-ligating RNA sequences on the antigenome of human hepatitis delta virus. J. Virol. 63: 1428-1430.
62. Stage-Zimmermann, T.K., and Uhlenbeck, O.C. 2001. A covalent cross-link converts the hammerhead ribozyme from a ribonuclease to an RNA ligase. Nat. Struct. Biol. 8: 863-867.
63. Stein, A. and Crothers, D.M. 1976. Conformational changes of transfer RNA. The role of magnesium(II). Biochemistry 15: 160-168.
64. Stribling, R. and Miller, S.L. 1991. Template-directed synthesis of oligonucleotides under eutectic conditions. J. Mol. Evol. 32: 289-295.
65. Tokumoto, Y. and Saigo, K. 1992. RNA-RNA and RNA-DNA ligation with the sTobRV(+) hammerhead ribozyme. Nucleic Acids Symp. Ser. 27: 21-22.
66. Trinks, H., Schroder, W., and Biebricher, C.K. 2005. Ice and the origin of life. Orig. Life Evol. Biosph. 35: 429-445.
67. Usher, D.A. and McHale, A.H. 1976. Nonenzymatic joining of oligoadenylates on a polyuridylic acid template. Science 192: 53-54.
68. Usher, D.A. and Yee, D. 1979. Geometry of the dry-state oligomerization of 2′,3′-cyclic phosphates. J. Mol. Evol. 13: 287-293.
69. Vajda, T. 1999. Cryo-bioorganic chemistry: Molecular interactions at low temperature. Cell. Mol. Life Sci. 56: 398-414.
70. Vary, C.P.H. and Vournakis, J.N. 1984. RNA structure analysis using T2 ribonuclease: Detection of pH and metal ion induced conformational changes in yeast tRNAPhe. Nucleic Acids Res. 12: 6763-6779.
71. Verlander, M.S. and Orgel, L.E. 1974. Analysis of high molecular weight material from the polymerization of adenosine cyclic 2′, 3′-phosphate. J. Mol. Evol. 3: 115-120.
72. 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.
73. Vlassov, A.V., Kazakov, S.A., Johnston, B.H., and Landweber, L.F. 2005a. The RNA world on ice: A new scenario for the emergence of RNA information. J. Mol. Evol. 61: 264-273.
74. Vlassov, A.V., Johnston, B.H., and Kazakov, S.A. 2005b. Hairpin ribozyme-catalyzed ligation in water-alcohol solutions. Oligonucleotides (in press).
75. Vollenweider, H.J., James, A., and Szybalski, W. 1978. Discrete length classes of DNA depend on mode of dehydration. Proc. Natl. Acad. Sci. 75: 710-714.
76. Westhof, E., Dumas, P., and Moras, D. 1988. Hydration of transfer RNA molecules: A crystallographic study. Biochimie 70: 145-165.
77. Zimmerman, S.B. and Coleman, N.F. 1972. An ordered precipitate of polyadenylic acid formed by freezing at acidic pH. Biopolymers 11: 1943-1960.