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Thermodynamic Parameters for an Expanded Nearest-Neighbor Model for Formation of RNA Duplexes with Watson−Crick Base Pairs†

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Department of Chemistry, University of Rochester, Rochester, New York 14627-0216, Department of Chemistry, Wayne State University, Detroit, Michigan 48202, Institute of Bioorganic Chemistry, Polish Academy of Sciences, 60-704 Poznan, Noskowskiego 12/14, Poland, and Department of Biostatistics, School of Medicine, University of Rochester, Rochester, New York 14642
‡  Department of Chemistry, University of Rochester.
§  Wayne State University.
‖  Polish Academy of Sciences.
⊥  Department of Biostatistics, University of Rochester.
 To whom correspondence should be addressed.
Cite this: Biochemistry 1998, 37, 42, 14719–14735
Publication Date (Web):October 1, 1998
https://doi.org/10.1021/bi9809425
Copyright © 1998 American Chemical Society
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Abstract

Improved thermodynamic parameters for prediction of RNA duplex formation are derived from optical melting studies of 90 oligoribonucleotide duplexes containing only Watson−Crick base pairs. To test end or base composition effects, new sets of duplexes are included that have identical nearest neighbors, but different base compositions and therefore different ends. Duplexes with terminal GC pairs are more stable than duplexes with the same nearest neighbors but terminal AU pairs. Penalizing terminal AU base pairs by 0.45 kcal/mol relative to terminal GC base pairs significantly improves predictions of ΔG°37 from a nearest-neighbor model. A physical model is suggested in which the differential treatment of AU and GC ends accounts for the dependence of the total number of Watson−Crick hydrogen bonds on the base composition of a duplex. On average, the new parameters predict ΔG°37, ΔH°, ΔS°, and TM within 3.2%, 6.0%, 6.8%, and 1.3 °C, respectively. These predictions are within the limit of the model, based on experimental results for duplexes predicted to have identical thermodynamic parameters.

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One table showing thermodynamic parameters for duplex formation derived from 1/TM vs log(CT/a) and from the average of curve fittings for 99 two-state sequences and 10 non-two-state sequences, one table showing the nearest-neighbor parameters for INN and INN-24 models, a discussion of multiple linear regression analysis by singular-value decomposition, and three tables of variance−covariance matrixes for parameters of the INN-HB model (17 pages).

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  80. Nathan A. Siegfried, Ryszard Kierzek and Philip C. Bevilacqua . Role of Unsatisfied Hydrogen Bond Acceptors in RNA Energetics and Specificity. Journal of the American Chemical Society 2010, 132 (15) , 5342-5344. https://doi.org/10.1021/ja9107726
  81. Kamila Réblová, Zora Střelcová, Petr Kulhánek, Ivana Beššeová, David H. Mathews, Keith Van Nostrand, Ilyas Yildirim, Douglas H. Turner and Jiří Šponer. An RNA Molecular Switch: Intrinsic Flexibility of 23S rRNA Helices 40 and 68 5′-UAA/5′-GAN Internal Loops Studied by Molecular Dynamics Methods. Journal of Chemical Theory and Computation 2010, 6 (3) , 910-929. https://doi.org/10.1021/ct900440t
  82. Biao Liu, Neelaabh Shankar and Douglas H. Turner . Fluorescence Competition Assay Measurements of Free Energy Changes for RNA Pseudoknots. Biochemistry 2010, 49 (3) , 623-634. https://doi.org/10.1021/bi901541j
  83. Daniel Svozil, Pavel Hobza and Jiří Šponer . Comparison of Intrinsic Stacking Energies of Ten Unique Dinucleotide Steps in A-RNA and B-DNA Duplexes. Can We Determine Correct Order of Stability by Quantum-Chemical Calculations?. The Journal of Physical Chemistry B 2010, 114 (2) , 1191-1203. https://doi.org/10.1021/jp910788e
  84. Hui-Ting Lee, Irine Khutsishvili and Luis A. Marky. DNA Complexes Containing Joined Triplex and Duplex Motifs: Melting Behavior of Intramolecular and Bimolecular Complexes with Similar Sequences. The Journal of Physical Chemistry B 2010, 114 (1) , 541-548. https://doi.org/10.1021/jp9084074
  85. U. Deva Priyakumar, Changbong Hyeon, D. Thirumalai and Alexander D. MacKerell, Jr. . Urea Destabilizes RNA by Forming Stacking Interactions and Multiple Hydrogen Bonds with Nucleic Acid Bases. Journal of the American Chemical Society 2009, 131 (49) , 17759-17761. https://doi.org/10.1021/ja905795v
  86. Elzbieta Kierzek. Binding of Short Oligonucleotides to RNA: Studies of the Binding of Common RNA Structural Motifs to Isoenergetic Microarrays. Biochemistry 2009, 48 (48) , 11344-11356. https://doi.org/10.1021/bi901264v
  87. Marta Carlucci, Elzbieta Kierzek, Anna Olejnik, Douglas H. Turner and Ryszard Kierzek . Chemical Synthesis of LNA-2-thiouridine and Its Influence on Stability and Selectivity of Oligonucleotide Binding to RNA. Biochemistry 2009, 48 (46) , 10882-10893. https://doi.org/10.1021/bi901506f
  88. Binh Nguyen and W. David Wilson. The Effects of Hairpin Loops on Ligand−DNA Interactions. The Journal of Physical Chemistry B 2009, 113 (43) , 14329-14335. https://doi.org/10.1021/jp904830m
  89. Amritraj Patra and Clemens Richert . High Fidelity Base Pairing at the 3′-Terminus. Journal of the American Chemical Society 2009, 131 (35) , 12671-12681. https://doi.org/10.1021/ja9033654
  90. Joshua M. Blose, David J. Proctor, Narayanan Veeraraghavan, Vinod K. Misra and Philip C. Bevilacqua . Contribution of the Closing Base Pair to Exceptional Stability in RNA Tetraloops: Roles for Molecular Mimicry and Electrostatic Factors. Journal of the American Chemical Society 2009, 131 (24) , 8474-8484. https://doi.org/10.1021/ja900065e
  91. Gang Chen, Scott D. Kennedy and Douglas H. Turner . A CA+ Pair Adjacent to a Sheared GA or AA Pair Stabilizes Size-Symmetric RNA Internal Loops. Biochemistry 2009, 48 (24) , 5738-5752. https://doi.org/10.1021/bi8019405
  92. Elzbieta Kierzek, Anna Pasternak, Karol Pasternak, Zofia Gdaniec, Ilyas Yildirim, Douglas H. Turner and Ryszard Kierzek . Contributions of Stacking, Preorganization, and Hydrogen Bonding to the Thermodynamic Stability of Duplexes between RNA and 2′-O-Methyl RNA with Locked Nucleic Acids. Biochemistry 2009, 48 (20) , 4377-4387. https://doi.org/10.1021/bi9002056
  93. Srividya Mohan, Chiaolong Hsiao, Halena VanDeusen, Ryan Gallagher, Eric Krohn, Benson Kalahar, Roger M. Wartell and Loren Dean Williams. Mechanism of RNA Double Helix-Propagation at Atomic Resolution. The Journal of Physical Chemistry B 2009, 113 (9) , 2614-2623. https://doi.org/10.1021/jp8039884
  94. Hans Binder, Jan Brücker and Conrad J. Burden . Nonspecific Hybridization Scaling of Microarray Expression Estimates: A Physicochemical Approach for Chip-to-Chip Normalization. The Journal of Physical Chemistry B 2009, 113 (9) , 2874-2895. https://doi.org/10.1021/jp808118m
  95. Koree Clanton-Arrowood, John McGurk and Susan J. Schroeder. 3′ Terminal Nucleotides Determine Thermodynamic Stabilities of Mismatches at the Ends of RNA Helices. Biochemistry 2008, 47 (50) , 13418-13427. https://doi.org/10.1021/bi801594k
  96. Amber R. Davis and Brent M. Znosko. Thermodynamic Characterization of Naturally Occurring RNA Single Mismatches with G-U Nearest Neighbors. Biochemistry 2008, 47 (38) , 10178-10187. https://doi.org/10.1021/bi800471z
  97. James M. Hart, Scott D. Kennedy, David H. Mathews and Douglas H. Turner . NMR-Assisted Prediction of RNA Secondary Structure: Identification of a Probable Pseudoknot in the Coding Region of an R2 Retrotransposon. Journal of the American Chemical Society 2008, 130 (31) , 10233-10239. https://doi.org/10.1021/ja8026696
  98. John D. Liu, Liang Zhao and Tianbing Xia. The Dynamic Structural Basis of Differential Enhancement of Conformational Stability by 5′- and 3′-Dangling Ends in RNA. Biochemistry 2008, 47 (22) , 5962-5975. https://doi.org/10.1021/bi800210t
  99. Martha E. Christiansen and Brent M. Znosko. Thermodynamic Characterization of the Complete Set of Sequence Symmetric Tandem Mismatches in RNA and an Improved Model for Predicting the Free Energy Contribution of Sequence Asymmetric Tandem Mismatches. Biochemistry 2008, 47 (14) , 4329-4336. https://doi.org/10.1021/bi7020876
  100. Anna Pasternak,, Elzbieta Kierzek,, Karol Pasternak,, Agata Fratczak,, Douglas H. Turner, and, Ryszard Kierzek. The Thermodynamics of 3‘-Terminal Pyrene and Guanosine for the Design of Isoenergetic 2‘-O-Methyl-RNA-LNA Chimeric Oligonucleotide Probes of RNA Structure. Biochemistry 2008, 47 (5) , 1249-1258. https://doi.org/10.1021/bi701758z
  101. Joshua M. Blose,, Michelle L. Manni,, Kelly A. Klapec,, Yukiko Stranger-Jones,, Allison C. Zyra,, Vasiliy Sim,, Chad A. Griffith,, Jason D. Long, and, Martin J. Serra. Non-Nearest-Neighbor Dependence of the Stability for RNA Bulge Loops Based on the Complete Set of Group I Single-Nucleotide Bulge Loops. Biochemistry 2007, 46 (51) , 15123-15135. https://doi.org/10.1021/bi700736f
  102. Jaya Badhwar,, Saradasri Karri,, Cody K. Cass,, Erica L. Wunderlich, and, Brent M. Znosko. Thermodynamic Characterization of RNA Duplexes Containing Naturally Occurring 1 × 2 Nucleotide Internal Loops. Biochemistry 2007, 46 (50) , 14715-14724. https://doi.org/10.1021/bi701024w
  103. Neelaabh Shankar,, Tianbing Xia,, Scott D. Kennedy,, Thomas R. Krugh,, David H. Mathews, and, Douglas H. Turner. NMR Reveals the Absence of Hydrogen Bonding in Adjacent UU and AG Mismatches in an Isolated Internal Loop from Ribosomal RNA,. Biochemistry 2007, 46 (44) , 12665-12678. https://doi.org/10.1021/bi700802s
  104. Amber R. Davis and, Brent M. Znosko. Thermodynamic Characterization of Single Mismatches Found in Naturally Occurring RNA. Biochemistry 2007, 46 (46) , 13425-13436. https://doi.org/10.1021/bi701311c
  105. Jeffrey J. Schwinefus,, Mikhail J. Kuprian,, John W. Lamppa,, Wolf E. Merker,, Kristin N. Dorn, and, Gregory W. Muth. Human Telomerase RNA Pseudoknot and Hairpin Thermal Stability with Glycine Betaine and Urea:  Preferential Interactions with RNA Secondary and Tertiary Structures. Biochemistry 2007, 46 (31) , 9068-9079. https://doi.org/10.1021/bi602637v
  106. Annie Schwartz,, Céline Walmacq,, A. Rachid Rahmouni, and, Marc Boudvillain. Noncanonical Interactions in the Management of RNA Structural Blocks by the Transcription Termination Rho Helicase. Biochemistry 2007, 46 (33) , 9366-9379. https://doi.org/10.1021/bi700493m
  107. Gang Chen,, Ryszard Kierzek,, Ilyas Yildirim,, Thomas R. Krugh,, Douglas H. Turner, and, Scott D. Kennedy. Stacking Effects on Local Structure in RNA:  Changes in the Structure of Tandem GA Pairs when Flanking GC Pairs Are Replaced by isoG−isoC Pairs. The Journal of Physical Chemistry B 2007, 111 (24) , 6718-6727. https://doi.org/10.1021/jp068732m
  108. Daniel J. Wright,, Jamie L. Rice,, Dawn M. Yanker, and, Brent M. Znosko. Nearest Neighbor Parameters for Inosine·Uridine Pairs in RNA Duplexes. Biochemistry 2007, 46 (15) , 4625-4634. https://doi.org/10.1021/bi0616910
  109. Blanton S. Tolbert,, Scott D. Kennedy,, Susan J. Schroeder,, Thomas R. Krugh, and, Douglas H. Turner. NMR Structures of (rGCUGAGGCU)2 and (rGCGGAUGCU)2:  Probing the Structural Features That Shape the Thermodynamic Stability of GA Pairs,. Biochemistry 2007, 46 (6) , 1511-1522. https://doi.org/10.1021/bi061350m
  110. Nathan A. Siegfried,, Shana L. Metzger, and, Philip C. Bevilacqua. Folding Cooperativity in RNA and DNA Is Dependent on Position in the Helix. Biochemistry 2007, 46 (1) , 172-181. https://doi.org/10.1021/bi061375l
  111. Martin Almlöf,, Martin Andér, and, Johan Åqvist. Energetics of Codon−Anticodon Recognition on the Small Ribosomal Subunit. Biochemistry 2007, 46 (1) , 200-209. https://doi.org/10.1021/bi061713i
  112. T. Heim,, L.-C. Tranchevent,, E. Carlon, and, G. T. Barkema. Physical-Chemistry-Based Analysis of Affymetrix Microarray Data. The Journal of Physical Chemistry B 2006, 110 (45) , 22786-22795. https://doi.org/10.1021/jp062889x
  113. Neelaabh Shankar,, Scott D. Kennedy,, Gang Chen,, Thomas R. Krugh, and, Douglas H. Turner. The NMR Structure of an Internal Loop from 23S Ribosomal RNA Differs from Its Structure in Crystals of 50S Ribosomal Subunits,. Biochemistry 2006, 45 (39) , 11776-11789. https://doi.org/10.1021/bi0605787
  114. Shenghua Duan,, David H. Mathews, and, Douglas H. Turner. Interpreting Oligonucleotide Microarray Data To Determine RNA Secondary Structure:  Application to the 3‘ End of Bombyx mori R2 RNA. Biochemistry 2006, 45 (32) , 9819-9832. https://doi.org/10.1021/bi052618x
  115. Gang Chen,, Scott D. Kennedy,, Jing Qiao,, Thomas R. Krugh, and, Douglas H. Turner. An Alternating Sheared AA Pair and Elements of Stability for a Single Sheared Purine-Purine Pair Flanked by Sheared GA Pairs in RNA,. Biochemistry 2006, 45 (22) , 6889-6903. https://doi.org/10.1021/bi0524464
  116. Gang Chen and, Douglas H. Turner. Consecutive GA Pairs Stabilize Medium-Size RNA Internal Loops. Biochemistry 2006, 45 (12) , 4025-4043. https://doi.org/10.1021/bi052060t
  117. Christopher D. Downey,, Julie L. Fiore,, Colby D. Stoddard,, Jose H. Hodak,, David J. Nesbitt, and, Arthur Pardi. Metal Ion Dependence, Thermodynamics, and Kinetics for Intramolecular Docking of a GAAA Tetraloop and Receptor Connected by a Flexible Linker. Biochemistry 2006, 45 (11) , 3664-3673. https://doi.org/10.1021/bi0520941
  118. Kensuke Akamatsu,, Mio Kimura,, Yoko Shibata,, Shu-ichi Nakano,, Daisuke Miyoshi,, Hidemi Nawafune, and, Naoki Sugimoto. A DNA Duplex with Extremely Enhanced Thermal Stability Based on Controlled Immobilization on Gold Nanoparticles. Nano Letters 2006, 6 (3) , 491-495. https://doi.org/10.1021/nl0524748
  119. Hairong Ma,, David J. Proctor,, Elzbieta Kierzek,, Ryszard Kierzek,, Philip C. Bevilacqua, and, Martin Gruebele. Exploring the Energy Landscape of a Small RNA Hairpin. Journal of the American Chemical Society 2006, 128 (5) , 1523-1530. https://doi.org/10.1021/ja0553856
  120. Elzbieta Kierzek,, Ryszard Kierzek,, Douglas H. Turner, and, Irina E. Catrina. Facilitating RNA Structure Prediction with Microarrays. Biochemistry 2006, 45 (2) , 581-593. https://doi.org/10.1021/bi051409+
  121. Brooke N. Bourdélat-Parks and, Roger M. Wartell. Thermodynamics of RNA Duplexes with Tandem Mismatches Containing a Uracil-Uracil Pair Flanked by C·G/G·C or G·C/A·U Closing Base Pairs. Biochemistry 2005, 44 (50) , 16710-16717. https://doi.org/10.1021/bi051659q
  122. Ilyas Yildirim and, Douglas H. Turner. RNA Challenges for Computational Chemists. Biochemistry 2005, 44 (40) , 13225-13234. https://doi.org/10.1021/bi051236o
  123. Magdalena Broda,, Elżbieta Kierzek,, Zofia Gdaniec,, Tadeusz Kulinski, and, Ryszard Kierzek. Thermodynamic Stability of RNA Structures Formed by CNG Trinucleotide Repeats. Implication for Prediction of RNA Structure. Biochemistry 2005, 44 (32) , 10873-10882. https://doi.org/10.1021/bi0502339
  124. Yun Fang,, Qi Cai, and, Peter Z. Qin. The Procapsid Binding Domain of φ29 Packaging RNA Has a Modular Architecture and Requires 2‘-Hydroxyl Groups in Packaging RNA Interaction. Biochemistry 2005, 44 (26) , 9348-9358. https://doi.org/10.1021/bi0475020
  125. J. Isaksson and, J. Chattopadhyaya. A Uniform Mechanism Correlating Dangling-End Stabilization and Stacking Geometry. Biochemistry 2005, 44 (14) , 5390-5401. https://doi.org/10.1021/bi047414f
  126. Kevin A. Wilkinson,, Edward J. Merino, and, Kevin M. Weeks. RNA SHAPE Chemistry Reveals Nonhierarchical Interactions Dominate Equilibrium Structural Transitions in tRNAAsp Transcripts. Journal of the American Chemical Society 2005, 127 (13) , 4659-4667. https://doi.org/10.1021/ja0436749
  127. Gang Chen,, Brent M. Znosko,, Scott D. Kennedy,, Thomas R. Krugh, and, Douglas H. Turner. Solution Structure of an RNA Internal Loop with Three Consecutive Sheared GA Pairs,. Biochemistry 2005, 44 (8) , 2845-2856. https://doi.org/10.1021/bi048079y
  128. Dana A. Baum,, Joy Sinha, and, Stephen M. Testa. Molecular Recognition in a Trans Excision-Splicing Ribozyme:  Non-Watson−Crick Base Pairs at the 5‘ Splice Site and ωG at the 3‘ Splice Site Can Play a Role in Determining the Binding Register of Reaction Substrates. Biochemistry 2005, 44 (3) , 1067-1077. https://doi.org/10.1021/bi0482304
  129. M. Sundaralingam and, P. K. Ponnuswamy. Stability of DNA Duplexes with Watson−Crick Base Pairs:  A Predicted Model. Biochemistry 2004, 43 (51) , 16467-16476. https://doi.org/10.1021/bi048158+
  130. Brent M. Znosko,, Scott D. Kennedy,, Pamela C. Wille,, Thomas R. Krugh, and, Douglas H. Turner. Structural Features and Thermodynamics of the J4/5 Loop from the Candida albicans and Candida dubliniensis Group I Introns,. Biochemistry 2004, 43 (50) , 15822-15837. https://doi.org/10.1021/bi049256y
  131. David J. Proctor,, Hairong Ma,, Elzbieta Kierzek,, Ryszard Kierzek,, Martin Gruebele, and, Philip C. Bevilacqua. Folding Thermodynamics and Kinetics of YNMG RNA Hairpins:  Specific Incorporation of 8-Bromoguanosine Leads to Stabilization by Enhancement of the Folding Rate. Biochemistry 2004, 43 (44) , 14004-14014. https://doi.org/10.1021/bi048213e
  132. Shu-ichi Nakano,, Hisae Karimata,, Tatsuo Ohmichi,, Junji Kawakami, and, Naoki Sugimoto. The Effect of Molecular Crowding with Nucleotide Length and Cosolute Structure on DNA Duplex Stability. Journal of the American Chemical Society 2004, 126 (44) , 14330-14331. https://doi.org/10.1021/ja0463029
  133. Gang Chen,, Brent M. Znosko,, Xiaoqi Jiao, and, Douglas H. Turner. Factors Affecting Thermodynamic Stabilities of RNA 3 × 3 Internal Loops. Biochemistry 2004, 43 (40) , 12865-12876. https://doi.org/10.1021/bi049168d
  134. Christopher J. Vecenie and, Martin J. Serra. Stability of RNA Hairpin Loops Closed by AU Base Pairs. Biochemistry 2004, 43 (37) , 11813-11817. https://doi.org/10.1021/bi049954i
  135. Fumiaki Tanaka,, Atsushi Kameda,, Masahito Yamamoto, and, Azuma Ohuchi. Thermodynamic Parameters Based on a Nearest-Neighbor Model for DNA Sequences with a Single-Bulge Loop. Biochemistry 2004, 43 (22) , 7143-7150. https://doi.org/10.1021/bi036188r
  136. Patricia M. McTigue,, Raymond J. Peterson, and, Jason D. Kahn. Sequence-Dependent Thermodynamic Parameters for Locked Nucleic Acid (LNA)−DNA Duplex Formation. Biochemistry 2004, 43 (18) , 5388-5405. https://doi.org/10.1021/bi035976d
  137. Peter J. Mikulecky,, Jennifer C. Takach, and, Andrew L. Feig. Entropy-Driven Folding of an RNA Helical Junction:  An Isothermal Titration Calorimetric Analysis of the Hammerhead Ribozyme. Biochemistry 2004, 43 (19) , 5870-5881. https://doi.org/10.1021/bi0360657
  138. Michael A. Bell,, Joy Sinha,, Ashley K. Johnson, and, Stephen M. Testa. Enhancing the Second Step of the Trans Excision-Splicing Reaction of a Group I Ribozyme by Exploiting P9.0 and P10 for Intermolecular Recognition. Biochemistry 2004, 43 (14) , 4323-4331. https://doi.org/10.1021/bi035874n
  139. Richard Owczarzy,, Yong You,, Bernardo G. Moreira,, Jeffrey A. Manthey,, Lingyan Huang,, Mark A. Behlke, and, Joseph A. Walder. Effects of Sodium Ions on DNA Duplex Oligomers:  Improved Predictions of Melting Temperatures. Biochemistry 2004, 43 (12) , 3537-3554. https://doi.org/10.1021/bi034621r
  140. Shu-ichi Nakano,, Takayuki Kanzaki, and, Naoki Sugimoto. Influences of Ribonucleotide on a Duplex Conformation and Its Thermal Stability:  Study with the Chimeric RNA−DNA Strands. Journal of the American Chemical Society 2004, 126 (4) , 1088-1095. https://doi.org/10.1021/ja037314h
  141. Susan J. Schroeder,, Matthew A. Fountain,, Scott D. Kennedy,, Peter J. Lukavsky,, Joseph D. Puglisi,, Thomas R. Krugh, and, Douglas H. Turner. Thermodynamic Stability and Structural Features of the J4/5 Loop in a Pneumocystis carinii Group I Intron. Biochemistry 2003, 42 (48) , 14184-14196. https://doi.org/10.1021/bi0301587
  142. Brent M. Znosko,, Mark E. Burkard,, Susan J. Schroeder,, Thomas R. Krugh, and, Douglas H. Turner. Sheared Aanti·Aanti Base Pairs in a Destabilizing 2 × 2 Internal Loop:  The NMR Structure of 5‘(rGGCAAGCCU)2,. Biochemistry 2002, 41 (50) , 14969-14977. https://doi.org/10.1021/bi020326f
  143. Brent M. Znosko,, Mark E. Burkard,, Thomas R. Krugh, and, Douglas H. Turner. Molecular Recognition in Purine-Rich Internal Loops:  Thermodynamic, Structural, and Dynamic Consequences of Purine for Adenine Substitutions in 5‘(rGGCAAGCCU)2,. Biochemistry 2002, 41 (50) , 14978-14987. https://doi.org/10.1021/bi0203278
  144. M. Ashley Spies and, Richard L. Schowen. The Trapping of a Spontaneously “Flipped-Out” Base from Double Helical Nucleic Acids by Host−Guest Complexation with β-Cyclodextrin:  The Intrinsic Base-Flipping Rate Constant for DNA and RNA. Journal of the American Chemical Society 2002, 124 (47) , 14049-14053. https://doi.org/10.1021/ja012272n
  145. David J. Proctor,, Janell E. Schaak,, Joanne M. Bevilacqua,, Christopher J. Falzone, and, Philip C. Bevilacqua. Isolation and Characterization of a Family of Stable RNA Tetraloops with the Motif YNMG That Participate in Tertiary Interactions. Biochemistry 2002, 41 (40) , 12062-12075. https://doi.org/10.1021/bi026201s
  146. Tatsuo Ohmichi,, Shu-ichi Nakano,, Daisuke Miyoshi, and, Naoki Sugimoto. Long RNA Dangling End Has Large Energetic Contribution to Duplex Stability. Journal of the American Chemical Society 2002, 124 (35) , 10367-10372. https://doi.org/10.1021/ja0255406
  147. Brent M. Znosko,, Sara B. Silvestri,, Heather Volkman,, Bob Boswell, and, Martin J. Serra. Thermodynamic Parameters for an Expanded Nearest-Neighbor Model for the Formation of RNA Duplexes with Single Nucleotide Bulges. Biochemistry 2002, 41 (33) , 10406-10417. https://doi.org/10.1021/bi025781q
  148. Paul L. Nixon,, Peter V. Cornish,, Saritha V. Suram, and, David P. Giedroc. Thermodynamic Analysis of Conserved Loop−Stem Interactions in P1−P2 Frameshifting RNA Pseudoknots from Plant Luteoviridae. Biochemistry 2002, 41 (34) , 10665-10674. https://doi.org/10.1021/bi025843c
  149. Matthew D. Disney and, Douglas H. Turner. Molecular Recognition by the Candida albicans Group I Intron:  Tertiary Interactions with an Imino G·A Pair Facilitate Binding of the 5‘ Exon and Lower the KM for Guanosine. Biochemistry 2002, 41 (25) , 8113-8119. https://doi.org/10.1021/bi020102x
  150. Ewa Biała and, Peter Strazewski. Internally Mismatched RNA:  pH and Solvent Dependence of the Thermal Unfolding of tRNAAla Acceptor Stem Microhairpins. Journal of the American Chemical Society 2002, 124 (14) , 3540-3545. https://doi.org/10.1021/ja0161305
  151. Peter Strazewski. Thermodynamic Correlation Analysis:  Hydration and Perturbation Sensitivity of RNA Secondary Structures. Journal of the American Chemical Society 2002, 124 (14) , 3546-3554. https://doi.org/10.1021/ja016131x
  152. David H. Mathews and, Douglas H. Turner. Experimentally Derived Nearest-Neighbor Parameters for the Stability of RNA Three- and Four-Way Multibranch Loops. Biochemistry 2002, 41 (3) , 869-880. https://doi.org/10.1021/bi011441d
  153. Thomas W. Barnes III and, Douglas H. Turner. C5-(1-Propynyl)-2‘-deoxy-Pyrimidines Enhance Mismatch Penalties of DNA:RNA Duplex Formation. Biochemistry 2001, 40 (42) , 12738-12745. https://doi.org/10.1021/bi011033+
  154. Susan J. Schroeder and, Douglas H. Turner. Thermodynamic Stabilities of Internal Loops with GU Closing Pairs in RNA. Biochemistry 2001, 40 (38) , 11509-11517. https://doi.org/10.1021/bi010489o
  155. Thomas W. Barnes III and, Douglas H. Turner. Long-Range Cooperativity Due to C5-Propynylation of Oligopyrimidines Enhances Specific Recognition by Uridine of ribo-Adenosine over ribo-Guanosine. Journal of the American Chemical Society 2001, 123 (37) , 9186-9187. https://doi.org/10.1021/ja0157752
  156. Naoki Sugimoto,, Naonori Satoh,, Kyohko Yasuda, and, Shu-ichi Nakano. Stabilization Factors Affecting Duplex Formation of Peptide Nucleic Acid with DNA. Biochemistry 2001, 40 (29) , 8444-8451. https://doi.org/10.1021/bi010480m
  157. Joshua M. Diamond,, Douglas H. Turner, and, David H. Mathews. Thermodynamics of Three-Way Multibranch Loops in RNA. Biochemistry 2001, 40 (23) , 6971-6981. https://doi.org/10.1021/bi0029548
  158. Matthew D. Disney,, Constantine G. Haidaris, and, Douglas H. Turner. Recognition Elements for 5‘ Exon Substrate Binding to the Candida albicans Group I Intron. Biochemistry 2001, 40 (21) , 6507-6519. https://doi.org/10.1021/bi002008r
  159. Thomas W. Barnes III and, Douglas H. Turner. Long-Range Cooperativity in Molecular Recognition of RNA by Oligodeoxynucleotides with Multiple C5-(1-Propynyl) Pyrimidines. Journal of the American Chemical Society 2001, 123 (18) , 4107-4118. https://doi.org/10.1021/ja003208t
  160. János Sági,, Anton B. Guliaev, and, B. Singer. 15-mer DNA Duplexes Containing an Abasic Site Are Thermodynamically More Stable with Adjacent Purines Than with Pyrimidines. Biochemistry 2001, 40 (13) , 3859-3868. https://doi.org/10.1021/bi0024409
  161. Mark E. Burkard,, Tianbing Xia, and, Douglas H. Turner. Thermodynamics of RNA Internal Loops with a Guanosine-Guanosine Pair Adjacent to Another Noncanonical Pair. Biochemistry 2001, 40 (8) , 2478-2483. https://doi.org/10.1021/bi0012181
  162. Xiaoying Chen,, Ryszard Kierzek, and, Douglas H. Turner. Stability and Structure of RNA Duplexes Containing Isoguanosine and Isocytidine. Journal of the American Chemical Society 2001, 123 (7) , 1267-1274. https://doi.org/10.1021/ja002623i
  163. Tatsuo Ohmichi,, Hiroyuki Nakamuta,, Kyohko Yasuda, and, Naoki Sugimoto. Kinetic Property of Bulged Helix Formation:  Analysis of Kinetic Behavior Using Nearest-Neighbor Parameters. Journal of the American Chemical Society 2000, 122 (46) , 11286-11294. https://doi.org/10.1021/ja001779f
  164. Matthew D. Disney,, Sergei M. Gryaznov, and, Douglas H. Turner. Contributions of Individual Nucleotides to Tertiary Binding of Substrate by a Pneumocystis carinii Group I Intron. Biochemistry 2000, 39 (46) , 14269-14278. https://doi.org/10.1021/bi001345x
  165. Katrina A. Lehmann and, Brenda L. Bass. Double-Stranded RNA Adenosine Deaminases ADAR1 and ADAR2 Have Overlapping Specificities. Biochemistry 2000, 39 (42) , 12875-12884. https://doi.org/10.1021/bi001383g
  166. Mark E. Burkard and, Douglas H. Turner. NMR Structures of r(GCAGGCGUGC)2 and Determinants of Stability for Single Guanosine−Guanosine Base Pairs,. Biochemistry 2000, 39 (38) , 11748-11762. https://doi.org/10.1021/bi000720i
  167. Naoki Sugimoto,, Mariko Nakano, and, Shu-ichi Nakano. Thermodynamics−Structure Relationship of Single Mismatches in RNA/DNA Duplexes. Biochemistry 2000, 39 (37) , 11270-11281. https://doi.org/10.1021/bi000819p
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