A Computational Study of RNA Tetraloop Thermodynamics, Including Misfolded States

Zerze, Gül H.; Piaggi, Pablo M.; Debenedetti, Pablo G.

doi:10.1021/acs.jpcb.1c08038

Title: A Computational Study of RNA Tetraloop Thermodynamics, Including Misfolded States

Journal Article · Fri Dec 10 00:00:00 EST 2021 · Journal of Physical Chemistry. B

DOI:https://doi.org/10.1021/acs.jpcb.1c08038· OSTI ID:1994991

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Princeton Univ., NJ (United States)

An important characteristic of RNA folding is the adoption of alternative configurations of similar stability, often referred to as misfolded configurations. These configurations are considered to compete with correctly folded configurations, although their rigorous thermodynamic and structural characterization remains elusive. Tetraloop motifs found in large ribozymes are ideal systems for an atomistically detailed computational quantification of folding free energy landscapes and the structural characterization of their constituent free energy basins, including nonnative states. In this work, we studied a group of closely related 10-mer tetraloops using a combined parallel tempering and metadynamics technique that allows a reliable sampling of the free energy landscapes, requiring only knowledge that the stem folds into a canonical A-RNA configuration. Here we isolated and analyzed unfolded, folded, and misfolded populations that correspond to different free energy basins. We identified a distinct misfolded state that has a stability very close to that of the correctly folded state. This misfolded state contains a predominant population that shares the same structural features across all tetraloops studied here and lacks the noncanonical A-G base pair in its loop portion. Further analysis performed with biased trajectories showed that although this competitive misfolded state is not an essential intermediate, it is visited in most of the transitions from unfolded to correctly folded states. Moreover, the tetraloops can transition from this misfolded state to the correctly folded state without requiring extensive unfolding.

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Research Organization:: Princeton Univ., NJ (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Science Foundation (NSF)

Grant/Contract Number:: SC0019394; CHE-1856704

OSTI ID:: 1994991

Journal Information:: Journal of Physical Chemistry. B, Vol. 125, Issue 50; ISSN 1520-6106

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (80)

RNA Chaperones and the RNA Folding Problem Herschlag, Daniel Journal of Biological Chemistry, Vol. 270, Issue 36 https://doi.org/10.1074/jbc.270.36.20871	journal	September 1995
Constant pressure molecular dynamics for molecular systems Nosé, Shuichi; Klein, M. L. Molecular Physics, Vol. 50, Issue 5 https://doi.org/10.1080/00268978300102851	journal	December 1983
Self-splicing RNA: Autoexcision and autocyclization of the ribosomal RNA intervening sequence of tetrahymena Kruger, Kelly; Grabowski, Paula J.; Zaug, Arthur J. Cell, Vol. 31, Issue 1 https://doi.org/10.1016/0092-8674(82)90414-7	journal	November 1982
Folding of RNA involves parallel pathways Pan, Jie; Thirumalai, D.; Woodson, Sarah A. Journal of Molecular Biology, Vol. 273, Issue 1 https://doi.org/10.1006/jmbi.1997.1311	journal	October 1997
A Network of Heterogeneous Hydrogen Bonds in GNRA Tetraloops Jucker, Fiona M.; Heus, Hans A.; Yip, Ping F. Journal of Molecular Biology, Vol. 264, Issue 5 https://doi.org/10.1006/jmbi.1996.0690	journal	December 1996
Base-stacking and base-pairing contributions into thermal stability of the DNA double helix Yakovchuk, P. Nucleic Acids Research, Vol. 34, Issue 2 https://doi.org/10.1093/nar/gkj454	journal	January 2006
Free-energy landscape of a hyperstable RNA tetraloop Miner, Jacob C.; Chen, Alan A.; García, Angel E. Proceedings of the National Academy of Sciences, Vol. 113, Issue 24 https://doi.org/10.1073/pnas.1603154113	journal	May 2016
RNA folding pathways in stop motion Bottaro, Sandro; Gil-Ley, Alejandro; Bussi, Giovanni Nucleic Acids Research, Vol. 44, Issue 12 https://doi.org/10.1093/nar/gkw239	journal	April 2016
Exposing the kinetic traps in RNA folding Treiber, Daniel K.; Williamson, James R. Current Opinion in Structural Biology, Vol. 9, Issue 3 https://doi.org/10.1016/S0959-440X(99)80045-1	journal	June 1999
Free Energy Landscape of GAGA and UUCG RNA Tetraloops Bottaro, Sandro; Banáš, Pavel; Šponer, Jiří The Journal of Physical Chemistry Letters, Vol. 7, Issue 20 https://doi.org/10.1021/acs.jpclett.6b01905	journal	September 2016
GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation Hess, Berk; Kutzner, Carsten; van der Spoel, David Journal of Chemical Theory and Computation, Vol. 4, Issue 3 https://doi.org/10.1021/ct700301q	journal	February 2008
RNA force field with accuracy comparable to state-of-the-art protein force fields Tan, Dazhi; Piana, Stefano; Dirks, Robert M. Proceedings of the National Academy of Sciences, Vol. 115, Issue 7 https://doi.org/10.1073/pnas.1713027115	journal	January 2018
Recognition of Planar and Nonplanar Ligands in the Malachite Green-RNA Aptamer Complex Flinders, Jeremy; DeFina, Steven C.; Brackett, David M. ChemBioChem, Vol. 5, Issue 1 https://doi.org/10.1002/cbic.200300701	journal	December 2003
Isolation of new ribozymes from a large pool of random sequences [see comment] Bartel, D.; Szostak, J. Science, Vol. 261, Issue 5127, p. 1411-1418 https://doi.org/10.1126/science.7690155	journal	September 1993
How to understand atomistic molecular dynamics simulations of RNA and protein-RNA complexes?: Atomistic molecular dynamics simulations of RNA and protein-RNA complexes Šponer, Jiří; Krepl, Miroslav; Banáš, Pavel Wiley Interdisciplinary Reviews: RNA, Vol. 8, Issue 3 https://doi.org/10.1002/wrna.1405	journal	November 2016
Mapping the Universe of RNA Tetraloop Folds Bottaro, Sandro; Lindorff-Larsen, Kresten Biophysical Journal, Vol. 113, Issue 2 https://doi.org/10.1016/j.bpj.2017.06.011	journal	July 2017
Architecture of ribosomal RNA: constraints on the sequence of "tetra-loops". Woese, C. R.; Winker, S.; Gutell, R. R. Proceedings of the National Academy of Sciences, Vol. 87, Issue 21 https://doi.org/10.1073/pnas.87.21.8467	journal	November 1990
Highly sampled tetranucleotide and tetraloop motifs enable evaluation of common RNA force fields Bergonzo, Christina; Henriksen, Niel M.; Roe, Daniel R. RNA, Vol. 21, Issue 9 https://doi.org/10.1261/rna.051102.115	journal	June 2015
Tertiary Motifs in RNA Structure and Folding Batey, Robert T.; Rambo, Robert P.; Doudna, Jennifer A. Angewandte Chemie International Edition, Vol. 38, Issue 16 https://doi.org/10.1002/(SICI)1521-3773(19990816)38:16<2326::AID-ANIE2326>3.0.CO;2-3	journal	August 1999
Free Energy Profile of RNA Hairpins: A Molecular Dynamics Simulation Study Deng, Nan-Jie; Cieplak, Piotr Biophysical Journal, Vol. 98, Issue 4 https://doi.org/10.1016/j.bpj.2009.10.040	journal	February 2010
Promoting transparency and reproducibility in enhanced molecular simulations Nature Methods, Vol. 16, Issue 8, p. 670-673 https://doi.org/10.1038/s41592-019-0506-8	journal	July 2019
Involvement of a GNRA tetraloop in long-range RNA tertiary interactions Jaeger, Luc; Michel, François; Westhof, Eric Journal of Molecular Biology, Vol. 236, Issue 5 https://doi.org/10.1016/0022-2836(94)90055-8	journal	March 1994
Exceptionally Stable Nucleic Acid Hairpins Varani, G. Annual Review of Biophysics and Biomolecular Structure, Vol. 24, Issue 1 https://doi.org/10.1146/annurev.bb.24.060195.002115	journal	June 1995
Fine-Tuning of the AMBER RNA Force Field with a New Term Adjusting Interactions of Terminal Nucleotides Mlýnský, Vojtěch; Kührová, Petra; Kühr, Tomáš Journal of Chemical Theory and Computation, Vol. 16, Issue 6 https://doi.org/10.1021/acs.jctc.0c00228	journal	May 2020
All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins ^† MacKerell, A. D.; Bashford, D.; Bellott, M. The Journal of Physical Chemistry B, Vol. 102, Issue 18 https://doi.org/10.1021/jp973084f	journal	April 1998
Native contacts determine protein folding mechanisms in atomistic simulations Best, R. B.; Hummer, G.; Eaton, W. A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 44 https://doi.org/10.1073/pnas.1311599110	journal	October 2013
Improving the Performance of the Amber RNA Force Field by Tuning the Hydrogen-Bonding Interactions Kührová, Petra; Mlýnský, Vojtěch; Zgarbová, Marie Journal of Chemical Theory and Computation, Vol. 15, Issue 5 https://doi.org/10.1021/acs.jctc.8b00955	journal	March 2019
Structural Motifs in RNA Moore, P. B. Annual Review of Biochemistry, Vol. 68, Issue 1 https://doi.org/10.1146/annurev.biochem.68.1.287	journal	June 1999
Structural Insight into RNA Hairpin Folding Intermediates Bowman, Gregory R.; Huang, Xuhui; Yao, Yuan Journal of the American Chemical Society, Vol. 130, Issue 30 https://doi.org/10.1021/ja8032857	journal	July 2008
PLUMED 2: New feathers for an old bird Tribello, Gareth A.; Bonomi, Massimiliano; Branduardi, Davide Computer Physics Communications, Vol. 185, Issue 2 https://doi.org/10.1016/j.cpc.2013.09.018	journal	February 2014
Equilibrium conformational dynamics in an RNA tetraloop from massively parallel molecular dynamics DePaul, A. J.; Thompson, E. J.; Patel, S. S. Nucleic Acids Research, Vol. 38, Issue 14 https://doi.org/10.1093/nar/gkq134	journal	March 2010
Crystal Structure of a Group I Ribozyme Domain: Principles of RNA Packing Cate, J. H.; Gooding, A. R.; Podell, E. Science, Vol. 273, Issue 5282 https://doi.org/10.1126/science.273.5282.1678	journal	September 1996
A Second Generation Force Field for the Simulation of Proteins, Nucleic Acids, and Organic Molecules Cornell, Wendy D.; Cieplak, Piotr; Bayly, Christopher I. Journal of the American Chemical Society, Vol. 117, Issue 19 https://doi.org/10.1021/ja00124a002	journal	May 1995
Empirical Corrections to the Amber RNA Force Field with Target Metadynamics Gil-Ley, Alejandro; Bottaro, Sandro; Bussi, Giovanni Journal of Chemical Theory and Computation, Vol. 12, Issue 6 https://doi.org/10.1021/acs.jctc.6b00299	journal	May 2016
Direct Revelation of Multiple Conformations in RNA by Femtosecond Dynamics Zhao, Liang; Xia, Tianbing Journal of the American Chemical Society, Vol. 129, Issue 14 https://doi.org/10.1021/ja068391q	journal	April 2007
Exploring the Energy Landscape of a Small RNA Hairpin Ma, Hairong; Proctor, David J.; Kierzek, Elzbieta Journal of the American Chemical Society, Vol. 128, Issue 5 https://doi.org/10.1021/ja0553856	journal	February 2006
CUUCGG hairpins: extraordinarily stable RNA secondary structures associated with various biochemical processes. Tuerk, C.; Gauss, P.; Thermes, C. Proceedings of the National Academy of Sciences, Vol. 85, Issue 5 https://doi.org/10.1073/pnas.85.5.1364	journal	March 1988
Insights into RNA structure and function from genome-wide studies Mortimer, Stefanie A.; Kidwell, Mary Anne; Doudna, Jennifer A. Nature Reviews Genetics, Vol. 15, Issue 7 https://doi.org/10.1038/nrg3681	journal	May 2014
Free-Energy Landscape for β Hairpin Folding from Combined Parallel Tempering and Metadynamics Bussi, Giovanni; Gervasio, Francesco Luigi; Laio, Alessandro Journal of the American Chemical Society, Vol. 128, Issue 41 https://doi.org/10.1021/ja062463w	journal	October 2006
A molecular dynamics method for simulations in the canonical ensemble Nosé, Shūichi Molecular Physics, Vol. 52, Issue 2 https://doi.org/10.1080/00268978400101201	journal	June 1984
Structural features that give rise to the unusual stability of RNA hairpins containing GNRA loops Heus, H.; Pardi, A. Science, Vol. 253, Issue 5016 https://doi.org/10.1126/science.1712983	journal	July 1991
Loop and stem dynamics during RNA hairpin folding and unfolding Sarkar, Krishnarjun; Nguyen, Duc A.; Gruebele, Martin RNA, Vol. 16, Issue 12 https://doi.org/10.1261/rna.2253310	journal	October 2010
High-resolution reversible folding of hyperstable RNA tetraloops using molecular dynamics simulations Chen, A. A.; Garcia, A. E. Proceedings of the National Academy of Sciences, Vol. 110, Issue 42 https://doi.org/10.1073/pnas.1309392110	journal	September 2013
GROMACS: A message-passing parallel molecular dynamics implementation Berendsen, H. J. C.; van der Spoel, D.; van Drunen, R. Computer Physics Communications, Vol. 91, Issue 1-3 https://doi.org/10.1016/0010-4655(95)00042-E	journal	September 1995
Conformational ensembles of RNA oligonucleotides from integrating NMR and molecular simulations Bottaro, Sandro; Bussi, Giovanni; Kennedy, Scott D. Science Advances, Vol. 4, Issue 5 https://doi.org/10.1126/sciadv.aar8521	journal	May 2018
Structures, Kinetics, Thermodynamics, and Biological Functions of RNA Hairpins Bevilacqua, Philip C.; Blose, Joshua M. Annual Review of Physical Chemistry, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.physchem.59.032607.093743	journal	May 2008
Well-Tempered Metadynamics: A Smoothly Converging and Tunable Free-Energy Method Barducci, Alessandro; Bussi, Giovanni; Parrinello, Michele Physical Review Letters, Vol. 100, Issue 2 https://doi.org/10.1103/PhysRevLett.100.020603	journal	January 2008
Insights into Stability and Folding of GNRA and UNCG Tetraloops Revealed by Microsecond Molecular Dynamics and Well-Tempered Metadynamics Haldar, Susanta; Kührová, Petra; Banáš, Pavel Journal of Chemical Theory and Computation, Vol. 11, Issue 8 https://doi.org/10.1021/acs.jctc.5b00010	journal	July 2015
Quality Threshold Clustering of Molecular Dynamics: A Word of Caution González-Alemán, Roy; Hernández-Castillo, David; Caballero, Julio Journal of Chemical Information and Modeling, Vol. 60, Issue 2 https://doi.org/10.1021/acs.jcim.9b00558	journal	September 2019
The molecular configuration of deoxyribonucleic acid Langridge, R.; Marvin, D. A.; Seeds, W. E. Journal of Molecular Biology, Vol. 2, Issue 1 https://doi.org/10.1016/S0022-2836(60)80005-8	journal	April 1960
Enhanced Sampling in the Well-Tempered Ensemble Bonomi, M.; Parrinello, M. Physical Review Letters, Vol. 104, Issue 19 https://doi.org/10.1103/PhysRevLett.104.190601	journal	May 2010
The Paradoxical Behavior of a Highly Structured Misfolded Intermediate in RNA Folding Russell, Rick; Das, Rhiju; Suh, Hyejean Journal of Molecular Biology, Vol. 363, Issue 2 https://doi.org/10.1016/j.jmb.2006.08.024	journal	October 2006
Dynamics of the RNA Hairpin GNRA Tetraloop ^† Menger, Marcus; Eckstein, Fritz; Porschke, Dietmar Biochemistry, Vol. 39, Issue 15 https://doi.org/10.1021/bi992297n	journal	April 2000
Computer Folding of RNA Tetraloops: Identification of Key Force Field Deficiencies Kührová, Petra; Best, Robert B.; Bottaro, Sandro Journal of Chemical Theory and Computation, Vol. 12, Issue 9 https://doi.org/10.1021/acs.jctc.6b00300	journal	August 2016
Protein Folding and Ligand-Enzyme Binding from Bias-Exchange Metadynamics Simulations Baftizadeh, Fahimeh; Cossio, Pilar; Pietrucci, Fabio Current Physical Chemistry, Vol. 2, Issue 1 https://doi.org/10.2174/1877946811202010079	journal	January 2012
Refinement of the AMBER Force Field for Nucleic Acids: Improving the Description of α/γ Conformers Pérez, Alberto; Marchán, Iván; Svozil, Daniel Biophysical Journal, Vol. 92, Issue 11 https://doi.org/10.1529/biophysj.106.097782	journal	June 2007
Performance of Molecular Mechanics Force Fields for RNA Simulations: Stability of UUCG and GNRA Hairpins Banáš, Pavel; Hollas, Daniel; Zgarbová, Marie Journal of Chemical Theory and Computation, Vol. 6, Issue 12 https://doi.org/10.1021/ct100481h	journal	November 2010
Folding intermediates of a self-splicing RNA: mispairing of the catalytic core Pan, Jie; Woodson, Sarah A. Journal of Molecular Biology, Vol. 280, Issue 4 https://doi.org/10.1006/jmbi.1998.1901	journal	July 1998
Polymorphic transitions in single crystals: A new molecular dynamics method Parrinello, M.; Rahman, A. Journal of Applied Physics, Vol. 52, Issue 12 https://doi.org/10.1063/1.328693	journal	December 1981
Integrating NMR and simulations reveals motions in the UUCG tetraloop Bottaro, Sandro; Nichols, Parker J.; Vögeli, Beat Nucleic Acids Research, Vol. 48, Issue 11 https://doi.org/10.1093/nar/gkaa399	journal	May 2020
Fitting Corrections to an RNA Force Field Using Experimental Data Cesari, Andrea; Bottaro, Sandro; Lindorff-Larsen, Kresten Journal of Chemical Theory and Computation, Vol. 15, Issue 6 https://doi.org/10.1021/acs.jctc.9b00206	journal	April 2019
Balance between α and β Structures in Ab Initio Protein Folding Best, Robert B.; Mittal, Jeetain The Journal of Physical Chemistry B, Vol. 114, Issue 26 https://doi.org/10.1021/jp102575b	journal	June 2010
A Time-Independent Free Energy Estimator for Metadynamics Tiwary, Pratyush; Parrinello, Michele The Journal of Physical Chemistry B, Vol. 119, Issue 3 https://doi.org/10.1021/jp504920s	journal	July 2014
Canonical dynamics: Equilibrium phase-space distributions Hoover, William G. Physical Review A, Vol. 31, Issue 3 https://doi.org/10.1103/PhysRevA.31.1695	journal	March 1985
Refinement of the Cornell et al. Nucleic Acids Force Field Based on Reference Quantum Chemical Calculations of Glycosidic Torsion Profiles Zgarbová, Marie; Otyepka, Michal; Šponer, Jiří Journal of Chemical Theory and Computation, Vol. 7, Issue 9 https://doi.org/10.1021/ct200162x	journal	August 2011
Geometric deep learning of RNA structure Townshend, Raphael J. L.; Eismann, Stephan; Watkins, Andrew M. Science, Vol. 373, Issue 6558 https://doi.org/10.1126/science.abe5650	journal	August 2021
Visualizing transient low-populated structures of RNA Dethoff, Elizabeth A.; Petzold, Katja; Chugh, Jeetender Nature, Vol. 491, Issue 7426 https://doi.org/10.1038/nature11498	journal	October 2012
Computer Folding of RNA Tetraloops? Are We There Yet? Kührová, Petra; Banáš, Pavel; Best, Robert B. Journal of Chemical Theory and Computation, Vol. 9, Issue 4 https://doi.org/10.1021/ct301086z	journal	March 2013
Peptide Folding: When Simulation Meets Experiment Daura, Xavier; Gademann, Karl; Jaun, Bernhard Angewandte Chemie International Edition, Vol. 38, Issue 1-2 https://doi.org/10.1002/(SICI)1521-3773(19990115)38:1/2<236::AID-ANIE236>3.0.CO;2-M	journal	January 1999
RNA simulations: probing hairpin unfolding and the dynamics of a GNRA tetraloop 1 1Edited by J. Dovdna Sorin, Eric J.; Engelhardt, Mark A.; Herschlag, Daniel Journal of Molecular Biology, Vol. 317, Issue 4 https://doi.org/10.1006/jmbi.2002.5447	journal	April 2002
Thermodynamics of DNA Hybridization from Atomistic Simulations Zerze, Gül H.; Stillinger, Frank H.; Debenedetti, Pablo G. The Journal of Physical Chemistry B, Vol. 125, Issue 3 https://doi.org/10.1021/acs.jpcb.0c09237	journal	January 2021
A smooth particle mesh Ewald method Essmann, Ulrich; Perera, Lalith; Berkowitz, Max L. The Journal of Chemical Physics, Vol. 103, Issue 19 https://doi.org/10.1063/1.470117	journal	November 1995
The mechanism of RNA base fraying: Molecular dynamics simulations analyzed with core-set Markov state models Pinamonti, Giovanni; Paul, Fabian; Noé, Frank The Journal of Chemical Physics, Vol. 150, Issue 15 https://doi.org/10.1063/1.5083227	journal	April 2019
The Ribosome Is a Ribozyme Cech, Thomas R. Science, Vol. 289, Issue 5481 https://doi.org/10.1126/science.289.5481.878	journal	August 2000
Revised AMBER Parameters for Bioorganic Phosphates Steinbrecher, T.; Latzer, J.; Case, D. A. Journal of Chemical Theory and Computation, Vol. 8, Issue 11 https://doi.org/10.1021/ct300613v	journal	October 2012
Escaping free-energy minima Laio, A.; Parrinello, M. Proceedings of the National Academy of Sciences, Vol. 99, Issue 20 https://doi.org/10.1073/pnas.202427399	journal	September 2002
Hierarchy and Dynamics of rna Folding Brion, Philippe; Westhof, Eric Annual Review of Biophysics and Biomolecular Structure, Vol. 26, Issue 1 https://doi.org/10.1146/annurev.biophys.26.1.113	journal	June 1997
A boundary correction algorithm for metadynamics in multiple dimensions McGovern, Michael; de Pablo, Juan The Journal of Chemical Physics, Vol. 139, Issue 8 https://doi.org/10.1063/1.4818153	journal	August 2013
Enhanced Conformational Sampling Using Replica Exchange with Collective-Variable Tempering Gil-Ley, Alejandro; Bussi, Giovanni Journal of Chemical Theory and Computation, Vol. 11, Issue 3 https://doi.org/10.1021/ct5009087	journal	February 2015
Water Dispersion Interactions Strongly Influence Simulated Structural Properties of Disordered Protein States Piana, Stefano; Donchev, Alexander G.; Robustelli, Paul The Journal of Physical Chemistry B, Vol. 119, Issue 16 https://doi.org/10.1021/jp508971m	journal	April 2015

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