Ligation of RNA Oligomers by the Schistosoma mansoni Hammerhead Ribozyme in Frozen Solution

详细信息    查看全文

• 作者：Lively Lie ; Shweta Biliya ; Fredrik Vannberg…
• 关键词：Ribozyme ; RNA ligation ; RNA world ; Dehydration
• 刊名：Journal of Molecular Evolution
• 出版年：2016
• 出版时间：March 2016
• 年：2016
• 卷：82
• 期：2-3
• 页码：81-92
• 全文大小：1,081 KB
• 参考文献：Adamala K, Szostak JW (2013) Nonenzymatic template-directed RNA synthesis inside model protocells. Science 342:1098CrossRef PubMed PubMedCentral
  Anderson M, Schultz EP, Martick M, Scott WG (2013) Active-site monovalent cations revealed in a 1.55-angstrom-resolution hammerhead ribozyme structure. J Mol Biol 425:3790CrossRef PubMed PubMedCentral
  Attwater J, Wochner A, Pinheiro VB, Coulson A, Holliger P (2010) Ice as a protocellular medium for RNA replication. Nat Commun 1:76CrossRef PubMed
  Auffinger P, Grover N, Westhof E (2011) Metal ion binding to RNA. Met Ions Life Sci 9:1CrossRef PubMed
  Bada JL, Lazcano A (2002) Origin of life. Some like it hot, but not the first biomolecules. Science 296:1982CrossRef PubMed
  Biondi E, Maxwell AW, Burke DH (2012) A small ribozyme with dual-site kinase activity. Nucleic Acids Res 40:7528CrossRef PubMed PubMedCentral
  Birikh KR, Heaton PA, Eckstein F (1997) The structure, function and application of the hammerhead ribozyme. Eur J Biochem 245:1CrossRef PubMed
  Canny MD, Jucker FM, Kellogg E, Khvorova A, Jayasena SD, Pardi A (2004) Fast cleavage kinetics of a natural hammerhead ribozyme. J Am Chem Soc 126:10848CrossRef PubMed
  Canny MD, Jucker FM, Pardi A (2007) Efficient ligation of the Schistosoma hammerhead ribozyme. Biochemistry 46:3826CrossRef PubMed PubMedCentral
  Chi YI, Martick M, Lares M, Kim R, Scott WG, Kim SH (2008) Capturing hammerhead ribozyme structures in action by modulating general base catalysis. PLoS Biol 6:2060
  Collins KD (2006) Ion hydration: implications for cellular function, polyelectrolytes, and protein crystallization. Biophys Chem 119:271CrossRef PubMed
  Darnell J (2011) RNA: life’s indispensable molecule. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
  de la Pena M, Garcia-Robles I (2010) Ubiquitous presence of the hammerhead ribozyme motif along the tree of life. RNA 16:1943CrossRef PubMed PubMedCentral
  De la Pena M, Gago S, Flores R (2003) Peripheral regions of natural hammerhead ribozymes greatly increase their self-cleavage activity. EMBO J 22:5561CrossRef PubMed PubMedCentral
  Ditzler MA, Lange MJ, Bose D, Bottoms CA, Virkler KF, Sawyer AW, Whatley AS, Spollen W, Givan SA, Burke DH (2013) High-throughput sequence analysis reveals structural diversity and improved potency among RNA inhibitors of HIV reverse transcriptase. Nucleic Acids Res 41:1873CrossRef PubMed PubMedCentral
  Fedor MJ (2009) Comparative Enzymology and Structural Biology of RNA Self-Cleavage. Annu Rev Biophys 38:271CrossRef PubMed
  Ferris JP, Hill AR Jr, Liu R, Orgel LE (1996) Synthesis of long prebiotic oligomers on mineral surfaces. Nature 381:59CrossRef PubMed
  Franks F (2000) Water a matrix of life. Royal Society of Chemistry, Cambridge xii, 225
  Gao JY, Xie C, Wang YL, Xu Z, Hao HX (2012) Solubility data of trisodium citrate hydrates in aqueous solution and crystal-solution interfacial energy of the pentahydrate. Cryst Res Technol 47:397CrossRef
  Gilbert W (1986) Origin of Life—the Rna World. Nature 319:618CrossRef
  Hammann C, Luptak A, Perreault J, de la Pena M (2012) The ubiquitous hammerhead ribozyme. RNA 18:871CrossRef PubMed PubMedCentral
  Han J, Burke JM (2005) Model for general acid-base catalysis by the hammerhead ribozyme: pH-activity relationships of G8 and G12 variants at the putative active site. Biochemistry 44:7864CrossRef PubMed
  Haynes CM (2013) The CRC handbook of chemistry and physics. Libr J 94:192
  Hertel KJ, Herschlag D, Uhlenbeck OC (1994) A kinetic and thermodynamic framework for the hammerhead ribozyme reaction. Biochemistry 33:3374CrossRef PubMed
  Hertel KJ, Herschlag D, Uhlenbeck OC (1996) Specificity of hammerhead ribozyme cleavage. EMBO J 15:3751PubMed PubMedCentral
  Higashi K, Terui Y, Suganami A, Tamura Y, Nishimura K, Kashiwagi K, Igarashi K (2008) Selective structural change by spermidine in the bulged-out region of double-stranded RNA and its effect on RNA function. J Biol Chem 283:32989CrossRef PubMed
  Hsiao C, Chou IC, Okafor CD, Bowman JC, O’Neill EB, Athavale SS, Petrov AS, Hud NV, Wartell RM, Harvey SC, Williams LD (2013) RNA with iron(II) as a cofactor catalyses electron transfer. Nat Chem 5:525CrossRef PubMed
  Hutchins CJ, Rathjen PD, Forster AC, Symons RH (1986) Self-cleavage of plus and minus Rna transcripts of avocado sunblotch viroid. Nucleic Acids Res 14:3627CrossRef PubMed PubMedCentral
  Johnston WK, Unrau PJ, Lawrence MS, Glasner ME, Bartel DP (2001) RNA-catalyzed RNA polymerization: accurate and general RNA-templated primer extension. Science 292:1319CrossRef PubMed
  Joyce GF (1989) RNA evolution and the origins of life. Nature 338:217CrossRef PubMed
  Kanavarioti A, Monnard PA, Deamer DW (2001) Eutectic phases in ice facilitate nonenzymatic nucleic acid synthesis. Astrobiology 1:271CrossRef PubMed
  Kazakov SA, Balatskaya SV, Johnston BH (1998) Freezing-induced self-ligation of the hairpin ribozyme: cationic effects. Struct Motion Interact Expr Biol Macromol 2:155
  Kazakov SA, Balatskaya SV, Johnston BH (2006) Ligation of the hairpin ribozyme in cis induced by freezing and dehydration. Rna 12:446CrossRef PubMed PubMedCentral
  Khvorova A, Lescoute A, Westhof E, Jayasena SD (2003) Sequence elements outside the hammerhead ribozyme catalytic core enable intracellular activity. Nat Struct Biol 10:708CrossRef PubMed
  Kupakuwana GV, Crill JE 2nd, McPike MP, Borer PN (2011) Acyclic identification of aptamers for human alpha-thrombin using over-represented libraries and deep sequencing. PLoS One 6:e19395CrossRef PubMed PubMedCentral
  Lambert D, Draper DE (2007) Effects of osmolytes on RNA secondary and tertiary structure stabilities and RNA-Mg2+ interactions. J Mol Biol 370:993CrossRef PubMed PubMedCentral
  Levy M, Miller SL (1998) The stability of the RNA bases: implications for the origin of life. Proc Natl Acad Sci USA 95:7933CrossRef PubMed PubMedCentral
  Li YF, Breaker RR (1999) Kinetics of RNA degradation by specific base catalysis of transesterification involving the 2 ‘-hydroxyl group. J Am Chem Soc 121:5364CrossRef
  Murray JB, Seyhan AA, Walter NG, Burke JM, Scott WG (1998) The hammerhead, hairpin and VS ribozymes are catalytically proficient in monovalent cations alone. Chem Biol 5:587CrossRef PubMed
  Mutschler H, Holliger P (2014) Non-canonical 3′-5′ extension of RNA with prebiotically plausible ribonucleoside 2′,3′-cyclic phosphates. J Am Chem Soc 136:5193CrossRef PubMed PubMedCentral
  Mutschler H, Wochner A, Holliger P (2015) Freeze-thaw cycles as drivers of complex ribozyme assembly. Nat Chem 7:502CrossRef PubMed PubMedCentral
  O’Rear JL, Wang SL, Feig AL, Beigelman L, Uhlenbeck OC, Herschlag D (2001) Comparison of the hammerhead cleavage reactions stimulated by monovalent and divalent cations. Rna 7:537CrossRef PubMed PubMedCentral
  Pace NR (1991) Origin of life–facing up to the physical setting. Cell 65:531CrossRef PubMed
  Perreault J, Weinberg Z, Roth A, Popescu O, Chartrand P, Ferbeyre G, Breaker RR (2011) Identification of hammerhead ribozymes in all domains of life reveals novel structural variations. PLoS Comput Biol 7:e1002031CrossRef PubMed PubMedCentral
  Prody GA, Bakos JT, Buzayan JM, Schneider IR, Bruening G (1986) Autolytic processing of dimeric plant-virus satellite Rna. Science 231:1577CrossRef PubMed
  Renz M, Lohrmann R, Orgel LE (1971) Catalysts for polymerization of adenosine cyclic 2′,3′-phosphate on a poly (U) template. Biochim Biophys Acta 240:463CrossRef PubMed
  Roy S (2008) Cleavage and ligation studies in hairpin and hammerhead ribozymes using site specific nucleotide modifications. University of Vermont, Burlington, p 176
  Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
  Serganov A, Patel DJ (2009) Amino acid recognition and gene regulation by riboswitches. Biochim Biophys Acta Gene Regul Mech 1789:592CrossRef
  Shepotinovskaya IV, Uhlenbeck OC (2008) Catalytic diversity of extended hammerhead ribozymes. Biochemistry 47:7034CrossRef PubMed PubMedCentral
  Stage-Zimmermann TK, Uhlenbeck OC (1998) Hammerhead ribozyme kinetics. RNA 4:875CrossRef PubMed PubMedCentral
  Stage-Zimmermann TK, Uhlenbeck OC (2001) A covalent crosslink converts the hammerhead ribozyme from a ribonuclease to an RNA ligase. Nat Struct Biol 8:863CrossRef PubMed
  Sun X, Li JM, Wartell RM (2007) Conversion of stable RNA hairpin to a metastable dimer in frozen solution. RNA 13:2277CrossRef PubMed PubMedCentral
  Tokumoto Y, Saigo K (1992) RNA-RNA and RNA-DNA ligation with the sTobRV(+) hammerhead ribozyme. Nucleic Acids Symp Ser 27:21PubMed
  Trinks H, Schroder W, Biebricher CK (2005) Ice and the origin of life. Orig Life Evol Biosph 35:429CrossRef PubMed
  Turk RM, Chumachenko NV, Yarus M (2010) Multiple translational products from a five-nucleotide ribozyme. Proc Natl Acad Sci USA 107:4585CrossRef PubMed PubMedCentral
  Uhlenbeck OC (1987) A small catalytic oligoribonucleotide. Nature 328:596CrossRef PubMed
  Vlassov AV, Johnston BH, Landweber LF, Kazakov SA (2004) Ligation activity of fragmented ribozymes in frozen solution: implications for the RNA world. Nucleic Acids Res 32:2966CrossRef PubMed PubMedCentral
  Vlassov AV, Kazakov SA, Johnston BH, Landweber LF (2005) The RNA world on Ice: a new scenario for the emergence of RNA information. J Mol Evol 61:264CrossRef PubMed
  
• 作者单位：Lively Lie (1) (2)
  Shweta Biliya (1) (2)
  Fredrik Vannberg (1) (2)
  Roger M. Wartell (1) (2)
  
  1. School of Biology, Georgia Institute of Technology, Atlanta, GA, 30332, USA
  2. Parker H. Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA, 30332, USA
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Cell Biology
  Microbiology
  Plant Sciences
  
• 出版者：Springer New York
• ISSN：1432-1432

文摘

The interstitial liquid phase within frozen aqueous solutions is an environment that minimizes RNA degradation and facilitates reactions that may have relevance to the RNA World hypothesis. Previous work has shown that frozen solutions support condensation of activated nucleotides into RNA oligomers, RNA ligation by the hairpin ribozyme, and RNA synthesis by a RNA polymerase ribozyme. In the current study, we examined the activity of a hammerhead ribozyme (HHR) in frozen solution. The Schistosoma mansoni hammerhead ribozyme, which predominantly cleaves RNA, can ligate its cleaved products (P1 and P2) with yields up to ~23 % in single turnover experiments at 25 °C in the presence of Mg2+. Our studies show that this HHR ligates RNA oligomers in frozen solution in the absence of divalent cations. Citrate and other anions that exhibit strong ion-water affinity enhanced ligation. Yields up to 43 % were observed in one freeze–thaw cycle and a maximum of 60 % was obtained after several freeze–thaw cycles using wild-type P1 and P2. Truncated and mutated P1 substrates were ligated to P2 with yields of 14–24 % in one freeze–thaw cycle. A pool of P2 substrates with mixtures of all four bases at five positions were ligated with P1 in frozen solution. High-throughput sequencing indicated that 70 of the 1024 possible P2 sequences were represented in ligated products at 1000 or more read counts per million reads. The results indicate that the HHR can ligate a range of short RNA oligomers into an ensemble of diverse sequences in ice.