Pressure Modulates the Self-cleavage Step of the Hairpin Ribozyme

Overview

Journal Nat Commun

Specialty Biology

Date 2017 Mar 31

PMID 28358002

Citations 6

Authors

Caroline Schuabb

Narendra Kumar

Salome Pataraia

Dominik Marx

Roland Winter

Affiliations

Soon will be listed here.

Abstract

The ability of certain RNAs, denoted as ribozymes, to not only store genetic information but also catalyse chemical reactions gave support to the RNA world hypothesis as a putative step in the development of early life on Earth. This, however, might have evolved under extreme environmental conditions, including the deep sea with pressures in the kbar regime. Here we study pressure-induced effects on the self-cleavage of hairpin ribozyme by following structural changes in real-time. Our results suggest that compression of the ribozyme leads to an accelerated transesterification reaction, being the self-cleavage step, although the overall process is retarded in the high-pressure regime. The results reveal that favourable interactions between the reaction site and neighbouring nucleobases are strengthened under pressure, resulting therefore in an accelerated self-cleavage step upon compression. These results suggest that properly engineered ribozymes may also act as piezophilic biocatalysts in addition to their hitherto known properties.

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References

Patriksson A, van der Spoel D . A temperature predictor for parallel tempering simulations. Phys Chem Chem Phys. 2008; 10(15):2073-7. DOI: 10.1039/b716554d. View

Suladze S, Cinar S, Sperlich B, Winter R . Pressure Modulation of the Enzymatic Activity of Phospholipase A2, A Putative Membrane-Associated Pressure Sensor. J Am Chem Soc. 2015; 137(39):12588-96. DOI: 10.1021/jacs.5b07009. View

Ito S, Kato H, Taniguchi R, Iwata T, Nureki O, Kandori H . Water-containing hydrogen-bonding network in the active center of channelrhodopsin. J Am Chem Soc. 2014; 136(9):3475-82. DOI: 10.1021/ja410836g. View

Mlynsky V, Banas P, Hollas D, Reblova K, Walter N, Sponer J . Extensive molecular dynamics simulations showing that canonical G8 and protonated A38H+ forms are most consistent with crystal structures of hairpin ribozyme. J Phys Chem B. 2010; 114(19):6642-52. PMC: 2872159. DOI: 10.1021/jp1001258. View

Rupert P, Ferre-DAmare A . Crystal structure of a hairpin ribozyme-inhibitor complex with implications for catalysis. Nature. 2001; 410(6830):780-6. DOI: 10.1038/35071009. View

Nissen P, Hansen J, Ban N, Moore P, Steitz T . The structural basis of ribosome activity in peptide bond synthesis. Science. 2000; 289(5481):920-30. DOI: 10.1126/science.289.5481.920. View

Donahue C, Yadava R, Nesbitt S, Fedor M . The kinetic mechanism of the hairpin ribozyme in vivo: influence of RNA helix stability on intracellular cleavage kinetics. J Mol Biol. 2000; 295(3):693-707. DOI: 10.1006/jmbi.1999.3380. View

Earl D, Deem M . Parallel tempering: theory, applications, and new perspectives. Phys Chem Chem Phys. 2009; 7(23):3910-6. DOI: 10.1039/b509983h. View

Joung I, Cheatham 3rd T . Determination of alkali and halide monovalent ion parameters for use in explicitly solvated biomolecular simulations. J Phys Chem B. 2008; 112(30):9020-41. PMC: 2652252. DOI: 10.1021/jp8001614. View

10.

Joyce G . The antiquity of RNA-based evolution. Nature. 2002; 418(6894):214-21. DOI: 10.1038/418214a. View

11.

Kuzmin Y, Da Costa C, Cottrell J, Fedor M . Role of an active site adenine in hairpin ribozyme catalysis. J Mol Biol. 2005; 349(5):989-1010. DOI: 10.1016/j.jmb.2005.04.005. View

12.

Decaneto E, Suladze S, Rosin C, Havenith M, Lubitz W, Winter R . Pressure and Temperature Effects on the Activity and Structure of the Catalytic Domain of Human MT1-MMP. Biophys J. 2015; 109(11):2371-81. PMC: 4675863. DOI: 10.1016/j.bpj.2015.10.023. View

13.

Chen J, Ganguly A, Miswan Z, Hammes-Schiffer S, Bevilacqua P, Golden B . Identification of the catalytic Mg²⁺ ion in the hepatitis delta virus ribozyme. Biochemistry. 2013; 52(3):557-67. PMC: 3558840. DOI: 10.1021/bi3013092. View

14.

Muth G, Strobel S . A single adenosine with a neutral pKa in the ribosomal peptidyl transferase center. Science. 2000; 289(5481):947-50. DOI: 10.1126/science.289.5481.947. View

15.

Doudna J, Cech T . The chemical repertoire of natural ribozymes. Nature. 2002; 418(6894):222-8. DOI: 10.1038/418222a. View

16.

Takahashi S, Sugimoto N . Effect of pressure on thermal stability of g-quadruplex DNA and double-stranded DNA structures. Molecules. 2013; 18(11):13297-319. PMC: 6270079. DOI: 10.3390/molecules181113297. View

17.

Dang Y, Li Q, Wang K, Wu Y, Lian L, Zou B . Hydrostatic pressure effects on the fluorescence and FRET behavior of Cy3-labeled phycocyanin system. J Phys Chem B. 2012; 116(36):11010-6. DOI: 10.1021/jp306466j. View

18.

Shirts M, Chodera J . Statistically optimal analysis of samples from multiple equilibrium states. J Chem Phys. 2008; 129(12):124105. PMC: 2671659. DOI: 10.1063/1.2978177. View

19.

Miner J, Chen A, Garcia A . Free-energy landscape of a hyperstable RNA tetraloop. Proc Natl Acad Sci U S A. 2016; 113(24):6665-70. PMC: 4914146. DOI: 10.1073/pnas.1603154113. View

20.

Hoover . Canonical dynamics: Equilibrium phase-space distributions. Phys Rev A Gen Phys. 1985; 31(3):1695-1697. DOI: 10.1103/physreva.31.1695. View